You are on page 1of 16

Revision and Biogeography of Centrolobium (Leguminosae - Papilionoideae)

Author(s): Michael D. Pirie , Bente B. Klitgaard , and R. Toby Pennington


Source: Systematic Botany, 34(2):345-359. 2009.
Published By: The American Society of Plant Taxonomists
URL: http://www.bioone.org/doi/full/10.1600/036364409788606262

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and
environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published
by nonprofit societies, associations, museums, institutions, and presses.
Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of
BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.
Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries
or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research
libraries, and research funders in the common goal of maximizing access to critical research.
Systematic Botany (2009), 34(2): pp. 345–359
© Copyright 2009 by the American Society of Plant Taxonomists

Revision and Biogeography of Centrolobium (Leguminosae - Papilionoideae)

Michael D. Pirie,1,5,6 Bente B. Klitgaard,2,4 and R. Toby Pennington3


1
Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, Zurich 8008 Switzerland
2
Department of Botany, Natural History Museum, Cromwell Road, London SW7 5BD U.K.
3
Royal Botanic Garden Edinburgh, 20a Inverleith Row, Edinburgh EH3 5LR U.K.
4
Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AE U.K.
5
Department of Biochemistry, University of Stellenbosch, Stellenbosch, Private Bag X1,
Matieland 7602 South Africa
6
Author for correspondence (mpirie@sun.ac.za)

Communicating Editor: Matt Lavin

Abstract—A taxonomic revision and biogeographic study of the genus Centrolobium (Leguminosae - Papilionoideae) is presented.
Centrolobium includes important timber trees distributed disjunctly in seasonally dry tropical forests and rain forests in Central and South
America, from Panama to south-eastern Brazil. It is characterized by large samaroid pods with a spiny seed case and an abundance of orange
peltate glands covering the leaves and inflorescences. Taxonomic distinctions between some species of Centrolobium have been a source of con-
fusion. Here, seven species are recognized: C. robustum, C. microchaete, C. tomentosum, C. ochroxylum, C. sclerophyllum, C. paraense, and C. yavi-
zanum. Previously recognized varieties of C. paraense, C. paraense var. paraense and C. paraense var. orinocense, are not maintained. Phylogenetic
analysis of DNA sequence data from the internal transcribed spacer region of nuclear ribosomal DNA and the plastid matK gene and trnL-trnF
intron and spacer support the monophyly of the genus. Different molecular dating methods indicate that the Centrolobium crown group and
lineages found to the west and east of the Andes diverged before the Pleistocene. Divergences between species occurring east of the Andes,
particularly in Bolivia and south-eastern Brazil are more recent, but nevertheless unlikely to be explained by Pleistocene climatic changes.

Keywords—Conservation assessments, Dalbergieae, molecular dating, Neotropics, phylogeny reconstruction, seasonally dry tropical forest

The Genus Centrolobium Mart. ex Benth—Centrolobium C. minus C.Presl, C. ochroxylum Rose ex Rudd, C. paraense Tul.,
(Leguminosae, Papilionoideae) is a neotropical genus of C. robustum Mart. ex Benth., C. tomentosum Guill. ex Benth,
seven species. It can be easily recognized, even when ster- and C. yavizanum Pittier. Two varieties were recognized within
ile, by an abundance of orange peltate glands covering most C. paraense Tul: var. orinocense Benth. and var. paraense.
parts. The genus comprises mostly large trees to 30 m tall, Although Rudd’s species delimitations were largely sound,
with a straight bole and broad, rounded crown of terminal new collections demonstrate that the characters that Rudd
branches. The fruits are large winged samaras to 30 cm long, used to diagnose some taxa vary continuously, such as leaf
with a conspicuous spiny basal seed chamber. A number of base shape in the varieties of C. paraense, and as a result,
species of Centrolobium are valued in the Neotropics for their Rudd’s species concepts should be re-evaluated. The extra-
timber, which is durable and richly colored yellowish-orange Amazonian Brazilian range of the genus was revised by Lima
with patches of dark red, purple, or black. (1985), who described one new species, C. sclerophyllum Lima,
Systematic Position—In his tribal classification of subfam- and redefined C. microchaete (Mart. ex Benth.) Lima, C. robus-
ily Papilionoideae, Polhill (1981; 1994) placed Centrolobium in tum, and C. tomentosum. Here, we present a taxonomic revi-
tribe Dalbergieae, which was diagnosed by free keel petals, sion of the whole genus over its entire geographical range.
staminal filaments partly fused and without basal fenestrae, Distribution of Centrolobium: Relevance to Neotropical
pods with specialized seed chambers, and seeds that accumu- Biogeographic History—Centrolobium species grow prin-
late alkaloids or other nonprotein amino acids. Recent mor- cipally in areas of seasonally dry tropical forest (SDTF; as
phological and molecular phylogenetic studies suggest that described in Prado and Gibbs 1993; Pennington et al. 2000,
tribe Dalbergieae sensu Polhill is not monophyletic (Lavin et al. 2006), but also in more humid forests. The genus is found in
2001, 2005). In a phylogenetic analysis of plastid (trnK-matK parts of Brazil, Bolivia, Ecuador, Peru, Colombia, Venezuela,
and trnL introns) and nuclear ribosomal (5.8S and ITS-1 and 2) Panama, and the Guianas (Fig. 1). Centrolobium shows a mix-
DNA sequences, Lavin et al. (2001) recovered a “dalbergioid” ture of species distribution patterns, with both widespread
clade comprising most of tribe Dalbergieae, but with mem- species and more geographically restricted endemics.
bers of tribes Aeschynomeneae and Adesmieae and subtribe The present day distribution of SDTF is highly discontin-
Bryinae of tribe Desmodieae nested within it. This redefined uous in the Neotropics. It roughly corresponds to the New
“dalbergioid” clade is characterized by short shoots, glan- World distribution of the “succulent biome” sensu Schrire
dular based trichomes, and aeschynomenoid root nodules. et al. (2005). Prado and Gibbs (1993) and Pennington et al.
Within the dalbergioid clade, Lavin et al. (2001) recovered (2000) highlighted a series of unrelated species with widely
three distinct subclades: the Adesmia clade, the Dalbergia discontinuous distributions in the separated nuclei of SDTF
clade, and the Pterocarpus clade. Centrolobium was placed in and suggested that during the Pleistocene, when climates
the Pterocarpus clade, together with Pterocarpus Jacq., Tipuana were drier and cooler; there was a widespread expanse of
Benth., Platypodium Vog., Platymiscium Vog., Ramorinoa Speg., seasonally dry vegetation in tropical South America. These
Inocarpus Forst, Paramachaerium Ducke, and Etaballia Benth. authors favored vicariance over dispersal as a more parsimo-
Taxonomic History—The generic name Centrolobium was nious explanation for repeated patterns of disjunction within
proposed by Martius and published by Bentham (1839) the SDTF. They also suggested that climatic fluctuations in the
based on Nissolia robusta Vell. The taxonomy of Centrolobium Pleistocene might have driven speciation in genera with high
was reviewed by Rudd (1954) who recognized six species: endemism in the SDTF.

345
346 SYSTEMATIC BOTANY [Volume 34

same taxa were combined (Appendix 1). Molecular markers were chosen
based on outgroup sequence availability and levels of variation within
Centrolobium and include the internal transcribed spacer regions of ribo-
somal DNA (ITS), chloroplast encoded matK (including spacer regions on
both sides of the matK exon), the trnL intron and the trnL-F spacer region.
DNA Extraction, PCR, and DNA Sequencing—Total genomic DNA was
extracted using a CTAB method (Doyle and Doyle 1987) without isopro-
panol precipitation, thus avoiding coprecipitation of oxidized material
(Savolainen et al. 1995); silica dried or herbarium leaf material was homog-
enized and incubated in CTAB for 20 minutes with 2-mercaptoethanol at
65°C, followed by 90 minutes ambient mixing with a mixture of chloroform
and isoamyl alcohol. After centrifugation, the supernatant was purified
using Wizard DNA purification system (Promega, Madison, Wisconsin).
The ITS region was amplified and sequenced using the primers of
Beyra and Lavin (1999). The matK and flanking trnK intron region was
amplified in two pieces using the primers trnK1L and 4R; and 1F and
trnK2R, and sequenced with the same primers plus 4R, 4F, 7L, and 32R
following Lavin et al. (2000). The universal primers of Taberlet et al. (1991)
were used to amplify and sequence the trnL intron (primers C/D) and the
trnL-trnF spacer (primers E/F). PCR amplifications were performed in 25
μl reactions containing 1 μl 0.4% BSA and 1 μl DMSO under the following
cycling conditions: an initial 4 min. at 94°C; 35 cycles of 30 sec. at 94°C,
Fig. 1. Distribution map for species of Centrolobium. C. yavizanum = 1 min. at 55°C, and 2 min. at 72°C; followed by 7 min. at 72°C. PCR
filled circles; C. paraense = filled squares; C. ochroxylum = filled triangles products were purified using QIAquick PCR purification kits (Qiagen,
(point up); C. microchaete = pentagons; C. tomentosum = open squares; Venlo, The Netherlands). Sequencing was performed on an ABI 3730XL
C. sclerophyllum = filled triangles (point down); C. robustum = stars. sequencer (Applied Biosystems, Foster City, California).
Phylogenetic Analysis—DNA sequences were edited and aligned
manually in SeqMan 4.0 (DNAStar Inc., Madison, Wisconsin), resulting in
Pennington et al. (2004) went on to test the second hypoth- alignments of 706 positions (ITS), 2,631 positions (matK), and 1,089 posi-
esis in four different clades with species confined to SDTF tions (trnL-F). Areas of the alignments where the assessment of homol-
ogy was ambiguous were excluded from the analyses. Gaps that could
using molecular dating approaches. They concluded that in
be inferred unambiguously were scored as presence/absence characters,
South America, species and clade ages largely predate the following the “simple gap coding” method of Simmons and Ochoterena
Pleistocene and are therefore inconsistent with a Pleistocene (2000).
diversification scenario. More recent work has called into Parsimony Analysis—Parsimony analyses were performed in the pro-
question the existence of widespread seasonally dry for- gram PAUP* 4.0b10 (Swofford 2002), assuming unordered character state
transformation and equal character weights (Fitch 1971). Shortest trees
est in South America during the Pleistocene (Lavin 2006; were obtained using the ‘branch and bound’ method. Bootstrap percent-
Pennington et al. 2006). High levels of geographic structure ages were calculated as follows: 500 replicates of 100 random addition
in phylogenies of SDTF clades indicate limited historical dis- sequences (RAS), with TBR branch swapping, saving a maximum of 50
persal between discontinuous areas of dry forest, suggesting trees per replicate. To test for conflict among data partitions, topologies
and bootstrap support were compared across data partitions. Congruence
that these areas have not been linked in the recent past (Lavin
among data partitions was further assessed with partition homogeneity
2006; Pennington et al. 2006). High geographic structure in tests as implemented in PAUP* (with 100 replicates of 1,000 RAS, sav-
phylogenies of STDF taxa such as robinioid legumes contrast ing a maximum of 10 trees). Based on the results of congruence testing,
with low geographic structure in phylogenies of some rain for- the data partitions were combined in further analyses. One accession
est taxa such as Inga reflecting the greater current geographic (C. tomentosum [e33]) with conflicting placements in the individual anal-
yses was excluded from the combined analyses. All other accessions,
continuity of neotropical rain forest (Lavin 2006; Pennington including those with missing data, were included in the combined analy-
et al. 2006). More dated phylogenies are needed to test poten- ses. Four of 26 Centrolobium accessions were lacking sequences for at least
tial generalities regarding the timing and geographical pat- one of the three sequenced cpDNA regions (corresponding to 12.3% of
terns of diversification in neotropical rain forests and SDTF aligned bases scored as missing data). Six Centrolobium accessions were
missing ITS sequences (13.8% of aligned bases).
(Pennington et al. 2006).
Bayesian Inference—The ITS and chloroplast datasets were com-
The aims of this paper are a) to produce a dated phylogeny bined in analyses using Bayesian inference, as implemented in MrBayes
for Centrolobium to determine the timing of diversification of version 3.1.2 (Huelsenbeck and Ronquist 2001). The dataset was divided
the genus and to assess the extent of geographic structure in into partitions corresponding to ITS, trnL-F and matK, and rates and sub-
its phylogeny; b) to test species delimitations in Centrolobium, stitution models were allowed to vary across the partitions. Modeltest 3.06
(Posada and Crandall 1998) was used to select the substitution model best
with particular focus on species with disjunct distributions fitting each sequence data partition. Geoffroea decorticans was designated
across discontinuous areas of SDTF; and c) to present a tax- as the single outgroup taxon. Two searches, each with four simultaneous
onomic revision of Centrolobium, including an identification MCMC chains, were run for 5,000,000 generations, saving one tree per
key to the species of the genus. 100 generations. Convergence was confirmed by analysis of the samples
using TRACER (Rambaut and Drummond 2003). The burn-in values were
determined empirically from the likelihood values of saved trees. The
burn-in was discarded and 50% majority rule consensus trees calculated
Materials and Methods together with approximations of the PP for the observed bipartitions from
the remaining trees. Trees have been posted to TreeBASE (study number
Molecular Phylogenetic Reconstruction: Taxon and Molecular Marker S2301).
Sampling—This study utilized previously unpublished sequence data from Molecular Dating—The combined chloroplast and ITS data were used
14 accessions, representing all seven species of Centrolobium. Sequences in molecular dating analyses. To test whether the sequence data had
from 16 individuals representing 10 (outgroup) taxa of the Pterocarpus evolved in a clocklike fashion, a likelihood ratio test was performed on
clade and Geoffroea decorticans (Gillies ex Hook. & Arn.) Burkart, the most the first of the most parsimonious tree topologies. Likelihoods of the data
distant outgroup, were obtained from published (Lavin et al. 2001) and with and without a molecular clock constraint were calculated and the
unpublished studies (Platymiscium ITS sequences, Saslis-Lagoudakis likelihood ratio statistic compared with χ2 critical value with 20 degrees of
et al. unpubl. results). Where not all markers were available for particu- freedom (Felsenstein 1981). The test rejected the molecular clock assump-
lar outgroup accessions, those from different accessions representing the tion (p < 0.001).
2009] PIRIE ET AL.: CENTROLOBIUM 347

We therefore applied two different molecular dating methods; penal- analyses, including numbers of variable and informative char-
ized likelihood (PL; Sanderson 2002a) and the Bayesian uncorrelated acters, are presented in Table 1. Direct comparison of analyses
relaxed clock method (Drummond et al. 2006) to correct for rate heteroge-
neity. While the latter method directly incorporates uncertainty in topol-
of the different markers is complicated by the differing sam-
ogy and branch length estimation into the error margins, such uncertainty ple sizes for each region (as indicated in Table 1). Inclusion of
can also be approximated when applying PL by using a variable sample of the single accession of Centrolobium yavizanum, which lacked
trees as input (see below). Both methods can also estimate absolute ages by a matK sequence, resulted in a much larger number of most
constraining the age(s) of one or more nodes (molecular clock calibration).
parsimonious trees.
In all analyses, Geoffroea decorticans and the accessions of Platymiscium,
which form two branches of a basal trichotomy in the cpDNA and com- Analysis of ITS resulted in a consensus topology that also
bined analyses, were ‘pruned’ from the trees, leaving a newly defined included groupings of the multiple accessions of C. ochrox-
root node, corresponding to the most recent common ancestor (mrca) ylum and of C. paraense, but which differed in a number of
of Grazielodendron and Centrolobium and to node 51 in the analysis Lavin places from the cpDNA consensus (Fig. 2). Comparison of
et al. (2005). The age of this node was fixed at 41.9 mya following the
results of Lavin et al. (2005; node 51, p.579, Fig. 2). The fossil Tipuana ecu-
trnL-F and ITS data partitions using the partition homogene-
atoriana Burnham (Burnham 1995) was used to impose a minimum age of ity test did not indicate significant conflict (p = 0.07), but com-
7.9 million years on the Tipuana stem node. Both calibrations are indicated parison of matK and ITS, and of combined trnL-F and matK
in the chronogram. with ITS, did indicate conflict (both p = 0.01). Only one topo-
Penalized likelihood (assuming rate autocorrelation) was implemented
logical difference received ≥ 70% BS, a sister group relation-
in the software package r8s (Sanderson 2002b). The optimum smooth-
ing parameter value was determined using the cross validation proce- ship between the two accessions of C. microchaete (e1 and e6)
dure in r8s, based on the MrBayes tree with the highest likelihood score. in the ITS tree, which conflicted with C. microchaete accession
This value was used to rate smooth the 1,000 last sampled trees from the e1 grouping with C. tomentosum accession e33 in the combined
MrBayes analysis (thus including variation in both topology and branch cpDNA analysis (Fig. 2). To eliminate this source of conflict,
lengths). Mean node ages and standard deviations were summarized
from the resulting ultrametric trees.
C. tomentosum (e33) was removed from the combined analy-
The Bayesian uncorrelated relaxed clock method was implemented ses of all of the data partitions. The partition homogeneity test
in the software package BEAST (Drummond and Rambaut 2007). We in the absence of this taxon did, however, still indicate conflict
applied a lognormal distribution to the rates. The root node was effec- between trnL-F/matK and ITS ( p = 0.01).
tively fixed at 41.9 (mya) by the designation of a uniform prior with mini-
Parsimony and Bayesian analyses of the combined cpDNA
mal bounds. Preliminary analyses indicated that the posterior distribution
of the age of the Tipuana stem node was greatly in excess of 7.9 mya, and and ITS data produced consistent results. BS and posterior
this prior was therefore omitted from the final BEAST analyses. The mcmc probability (PP) values are indicated on the Bayesian 50%
was run for five million generations, with sampling every 1,000 genera- majority rule consensus topology (Fig. 3). Of the three mark-
tions, after which convergence was confirmed by analysis of the samples ers sequenced, ITS was the most variable. However, the rel-
using TRACER (Rambaut and Drummond 2003). Burn-in values were
determined empirically from the likelihood values of sampled trees and
ative contribution of informative characters from nuclear
the burn-in from each run was excluded. The remaining trees were used (ribosomal) and chloroplast encoded markers was similar
to calculate a 50% majority rule consensus tree and node ages (mean and (see Table 1), and the combined analyses included roughly
95% confidence limits). double the number of informative characters in compari-
Taxonomic Treatment—The taxonomic account that follows is based
son to the individual analyses. Nevertheless, resolution and
on examination of 280 collections made available by the following her-
baria: A, AAU, BM, BR, E, F, GH, K, LPB, MO, NY, RB, U, US, and USZ. support values showed little improvement in the combined
A list of exsiccatae is provided in Appendix 2. Conservation status is analyses (compare Figs. 2 and 3).
based on IUCN categories of threat criteria (IUCN 2001). Vegetation type Molecular Dating—r8s Analyses—The cross validation
is assigned according to the following four major biomes: seasonally dry test for PL selected an optimal smoothing parameter of 3.2,
tropical forest (SDTF), lowland rain forest, savanna, and restinga, with
more specific vegetations described as appropriate. Definitions of SDTF
which was used in all further PL analyses. The mean age of the
and savanna follow Pennington et al. (2000). Savanna and SDTF change stem node of Tipuana was 28.1 mya, much older than the 7.9
to rain forest along transitions of rainfall; rain forest grows in areas of mya Tipuana fossil. The mean age of the mrca of Centrolobium
higher annual rainfall, but a key factor is that rainfall is less strongly sea- summarized across 1,000 MrBayes trees was 7.5 mya, with
sonal (with fewer entirely dry months) than in areas that support SDTF or
a standard deviation of 0.9, a minimum age of 5.1 mya and
savanna (Thomas and de Vansconcellos Barbosa 2008). Restinga is a scrub
vegetation growing on well-drained, sandy soils between the beach and maximum of 11.0 mya.
coastal rain forests of Eastern Brazil. It forms a narrow band of vegetation BEAST Analyses—Age estimations were consistent with
ranging from a few hundred meters to a few kilometers wide (Thomas those derived using r8s, although the (95%) confidence inter-
and de Vansconcellos Barbosa 2008). vals were wider (Fig. 4), thus providing a more conservative
test of biogeographic hypotheses. In the following discussion,
we will therefore refer to the results obtained using BEAST.
Results
The Tipuana stem node was estimated at between 14.2 and
Phylogenetic Analysis—Parsimony analysis of matK 39.7 mya, also much older than the Tipuana fossil. The confi-
and trnL-F resulted in relatively unresolved topologies (not dence interval for the mrca of Centrolobium was between 3.5–
shown), particularly in the case of trnL-F. The phylogenies 15.9 mya.
were without conflicting nodes with ≥ 70% bootstrap sup-
port (BS; data not shown). The partition homogeneity test
Discussion
for the chloroplast data did not indicate significant conflict
( p = 0.37), and the data were combined in further analyses. Species Delimitation—We mainly agree with the species
The monophyly of Centrolobium received high support (98% delimitations of Rudd. The species of Centrolobium display
BS), but the only internal nodes subject to ≥ 70% BS corre- two broad patterns of distribution. The first, exhibited by C.
sponded to multiple accessions of C. ochroxylum and of microchaete and C. paraense, is of wider distribution, in the case
C. paraense, plus a strongly supported sister group relation- of C. microchaete with populations found in different disjunct
ship between one of the accessions of C. microchaete (e1) and areas. The second, exhibited by C. robustum, C. tomentosum, C.
one of C. tomentosum (e33) (Fig. 2). Details of the parsimony sclerophyllum, C. ochroxylum, and C. yavizanum, is of restriction
348 SYSTEMATIC BOTANY [Volume 34

Fig. 2. Shortest trees (arbitrarily selected) from parsimony analysis of (a) nuclear ribosomal ITS and (b) chloroplast encoded matK and trnL-F data.
Bootstrap support (where > 50%) is indicated above the branches. Nodes that collapse in the strict consensus are indicated by arrows.
2009] PIRIE ET AL.: CENTROLOBIUM 349

logenetic conflict among data partitions. With the exclusion


of just one taxon from the analyses, we were able to eliminate
conflict supported by > 70% BS. Levels of phylogenetic reso-
lution were not substantially greater in the combined analyses
relative to the individual analyses, perhaps due to persisting
phylogenetic conflict caused by incomplete lineage sorting or
hybridization.
Biogeographic History—Pennington et al. (2004, 2006) noted
a preponderance of pre-Pleistocene speciation and high phy-
logenetic geographic structure in South American SDTF
clades. In Centrolobium, phylogenetic geographic structure
is limited, although the timing of lineage diversification also
appears to be largely pre-Pleistocene. Centrolobium began
diversifying a minimum of 3.5 mya. The most north-westerly
distributed species, C. yavizanum and C. ochroxylum, diverged
from a common ancestor at least two mya, before Pleistocene
climatic changes. The estimated ages of divergences between
species from Bolivia and Brazil (plus C. paraense from Brazil,
Guyana, Venezuela, and Colombia) span the Late Miocene
and Pliocene, with the margins of error for some nodes also
entering the Pleistocene. The distributions of C. yavizanum
and C. ochroxylum are separated from those of other species of
Centrolobium by the Andes Mountains, which may explain the
relatively deep phylogenetic divergence. There is little phylo-
genetic geographic structure in the species found east of the
Andes, as illustrated by the widespread, overlapping distri-
butions of C. robustum and C. microchaete and the widely dis-
junct distribution of C. microchaete.
The levels of phylogenetic geographic structure in Centrolo-
bium are lower than those observed in other South American
SDTF clades (Pennington et al. 2004). This may be because
some Centrolobium species are not SDTF specialists, as they
also grow in more humid, less seasonal formations such as
the Amazon rain forest (e.g. C. paraense) and the Brazilian
Fig. 3. 50% majority rule consensus tree from Bayesian analysis of
combined ITS and chloroplast data. Posterior probabilities of clades Atlantic Coastal rain forest (e.g. C. robustum, C. tomentosum).
(where > 0.50) are indicated above the branches, bootstrap support from Lavin (2006) and Pennington et al. (2006) argued that rain
parsimony analyses (where > 50%), below. forest clades show less geographic structure than dry forest
clades because of the greater continuity of rain forest com-
pared to SDTF. The wide ecological tolerance of Centrolobium
to a relatively narrow geographic range. Some species display may have allowed it greater opportunity for migration, lead-
relatively large amounts of morphological variation across ing to the lack of geographic structure observed in the east of
their ranges, e.g. Brazilian versus Bolivian populations of its range.
C. microchaete; and others relatively little, e.g. C. paraense.
Monophyly of Centrolobium and Species Relationships— Taxonomic Treatment
Analysis of both chloroplast and nuclear sequence data
yielded strong support for the monophyly of Centrolobium. Centrolobium Mart. ex Benth., Ann. Mus. Vind. 2: 95. 1839.
Within Centrolobium, multiple accessions of the same spe- Benth., in Mart. Fl. Bras. 15.1: 263–266. 1862; Rudd,
cies sometimes formed monophyletic groups. However, few J. Wash. Acad. Sci. 44: 284–288. 1954; Lima, Arq. Jard. Bot.
other conclusions regarding phylogenetic relationships could Rio de Janeiro 27: 177–191. 1985.—TYPE: Centrolobium
be drawn, due to low variation in the sequence data and phy- robustum (Vell.) Mart. ex Benth.

Table 1. Details of maximum parsimony analyses (all employing ‘branch and bound’ method as implemented in PAUP* to find all shortest trees).
Combined analyses in which taxa with missing data were excluded are indicated by “1”, otherwise all taxa with at least one marker sampled were
included.

No. taxa Included chars Variable chars Pars.inf. chars Inf. indels No. trees Tree length CI RI

matK 22 2634 299 152 10 23 360 0.886 0.882


trnLF 17 1119 89 31 9 84 98 0.908 0.859
matK/trnLF 23 3753 388 183 19 3192 462 0.883 0.868
matK/trnLF1 16 3753 349 99 17 16 409 0.890 0.815
ITS 19 673 260 164 - 24 484 0.698 0.653
Combined 23 4426 647 344 19 114 957 0.778 0.736
Combined1 12 4426 503 160 15 4 663 0.848 0.649
350 SYSTEMATIC BOTANY [Volume 34

Fig. 4. Chronogram from BEAST molecular dating analysis. The error margins for age estimations are indicated by bars at the nodes (thicker, lighter
bars representing BEAST posterior distributions, thinner, darker bars representing the mean ± SD summarised from penalized likelihood rate smoothing of
1,000 MrBayes trees). Timescale and age calibration points A (secondary calibration from Lavin et al. [2005]) and B (fossil Tipuana [Burnham, 1995]) are also
indicated, as are the timeframes of speciation within Centrolobium (large filled rectangle), and Pleistocene climatic changes (rectangle above the time scale).
2009] PIRIE ET AL.: CENTROLOBIUM 351

Trees, 4–35 m tall; trunk commonly buttressed at base, to brous, the standard petal spatulate or obovate, with a short,
100 cm in diameter; bark grayish, vertically fissured, the sap thick claw with darker central marking, reflexed, the wing
red; wood yellowish or orange with streaks of red, purple, petals basally auriculate, with a long narrow claw, the keel
or black; twigs mostly densely pubescent, the twigs, leaves, petals fused for 1/3 of their lower margin, the upper mar-
inflorescences, and fruits dotted with reddish-orange peltate gin auriculate at the base; stamens 10, fused monadelphously
glands. Leaves imparipinnate, (5-)9–17(-23)-foliolate; stipules into an open sheath, the anthers 1–1.5 mm long, dorsifixed,
usually caducous, rarely persistent, deltoid to broadly orbic- versatile. Fruits 1-few-seeded samaras, 6.8–22(-27) cm long;
ular, the apex acute; leaflets ovate, elliptic or oblong, sym- seed chamber basal, subcylindrical, externally echinate; wing
metrical or asymmetrical, the base cordate to rounded, the distal, chartaceous or coriaceous, usually indumented and
margins entire, the apex acute to shortly acuminate, the vena- covered with long-stalked to subsessile peltate glands; stylar
tion brochidodromous. Inflorescences of terminal panicles; spine fused to the samara wing for a variable distance, the
bracts narrowly to broadly ovate, rarely fan-shaped (only free apex at a ca. 45°, 90° or 120° angle with the wing mar-
in C. ochroxylum, Fig. 5K), usually persistent, rarely cadu- gin; spines of seed chambers sparsely to densely tomentose;
cous, reflexed or upright, the apex acute or obtuse; bracteoles seeds 2–3 × 1–1.5 cm, oblong, testa thin, green, albuminous.
narrowly or broadly ovate, persistent or caducous. Flowers Figures 5A-V, 6A-U.
10–22(-25) mm long, sweetly scented; calyx tubular, cam- Distribution—From Panama, throughout northern South
panulate or urceolate, sometimes adaxially gibbous, the base America to Bolivia and Santa Catarina state in southern
acute, obtuse or truncate, 5-lobed, the three abaxial lobes Brazil, but largely avoiding the Amazon Basin, from sea level
unequal, the apices acute or obtuse, the two adaxial lobes to 1,000 m elevation. Figure 1.
fused for almost their entire length, the apex emarginate; Habitat—Seasonally dry tropical forests to lowland rain
corolla yellow, sometimes suffused with red or violet, gla- forests.

Key to CENTROLOBIUM Species


1. Stipules persistent, ca. 15 × 15 mm, leaf-like, broadly ovate ..................................................................................................................................... 3. C. paraense.
1. Stipules caducous, 2–15 × 2–4 mm, not leaf-like, narrowly ovate, deltate. .................................................................................................................................. 2
2. Calyx urceolate. Bracts deltoid (Fig. 5P). Leaflets 5–11 × 2–5 cm, narrowly ovate or elliptic, coriaceous ........................................... 5. C. sclerophyllum.
2. Calyx campanulate or tubular. Bracts fan-shaped, narrowly or broadly ovate. Leaflets (4-)6–20 × (2–)4–9(-14) cm, oblong, elliptic or ovate, charta-
ceous or/to membranaceous, rarely coriaceous. ................................................................................................................................................................... 3
3. Leaflets membranaceous or coriaceous, the lower surface matted with twisting trichomes and dense glands. ...................................................... 4
4. Bract fan-shaped, 2–2.5 × 3–3.5 mm (Fig. 5K). Flower 15–18(-25) mm long. Samara covered by sparse trichomes. Western Ecuador and north
western Peru .......................................................................................................................................................................................2. C. ochroxylum.
4. Bract narrowly ovate, 4–5 × 3–4 mm (Fig. 5T). Flower 18–22 mm long. Samara covered by dense trichomes. Central eastern Brazil
............................................................................................................................................................................................................... 6. C. tomentosum.
3. Leaflets chartaceous or coriaceous, the lower surface glabrous or with sparse straight to curly trichomes and glands. ........................................ 5
5. Flowers 10–12 mm long. Calyx lobes 2–5 mm long, the apices acute. Leaflets usually chartaceous, rarely membranaceous. ................ 6
6. Leaves 9–13(-19)-foliolate. Leaflets elliptic or oblong, the base asymmetric (Fig. 5H). Bracts ovate, 1.5–4 × 1.5–3 mm. Fruiting stipe
1–10 mm long. Eastern Brazil and eastern Bolivia .......................................................................................................... 1. C. microchaete.
6. Leaves 13–17-foliolate. Leaflets elliptic, the base symmetric (Fig. 5U). Bracts narrowly ovate, 3–5 × 1.5–3 mm. Fruiting stipe 20–30 mm
long. Southern Panama and northern Colombia .............................................................................................................. 7. C. yavizanum.
5. Flowers 17–18 mm long. Calyx lobes 5–7 mm long, the apices obtuse. Leaflets usually coriaceous, rarely membranaceous
............................................................................................................................................................................................................ 4. C. robustum.

1. Centrolobium microchaete (Mart. ex Benth.) Lima, Arq. 2–3 mm long, the apex emarginate, acute; corolla reddish-yel-
Jard. Bot. Rio de Janeiro 27: 180. 1985. C. robustum (Vell.) low to dark tawny-brown, venation red; standard 10–11 × ca.
Mart. ex Benth. var. microchaete Mart. ex Benth. in Mart. 9 mm, suborbiculate, reflexed at anthesis, the wing petals ca.
Fl. Bras. 15(1): 263. 1862.—TYPE: BRAZIL. Rio de Janeiro: 10 × 4 mm, auriculate at the base of the blade, the keel petals
“prope Canta Gallo”, 1859, Th. Peckolt s.n. [in BR the col- ca.10 × 4 mm, auriculate at the base of the blade, fused for 1/3
lection contains a label: Peckolt n. 260] (lectotype BR!). of the lower margins; stamens 9–11 mm long, fused basally for
1/3 of their length. Samara 6.8–17.5 × 2.9–8 cm; seed chamber
Tree 7–26 m tall; trunk diameter 10–70 cm, the bark black- ca. 4 × 4 cm, the spines 6–17 × 0.5–1 mm, basal part sparsely
ish grey with light vertical and longitudinal fissures, inflo- indumented with curly trichomes, ca. 1 mm long, and short-
rescences drying blackish brown. Leaves 9–13(-19)-foliolate; stalked peltate glands, the apical part with similar trichomes,
stipules caducous, not observed; leaflets 4–13.4 × 2–4 cm, but lacking peltate glands; wing chartaceous with indumen-
usually elliptic or oblong, rarely ovate, the base asymmetric, tum and glands similar to those on the seed chamber; stylar
rounded, the apex shortly acuminate or acute, chartaceous or spine fused to samara wing for 8–20 mm, the free apex 5–15
coriaceous, both surfaces shiny green, covered with sparse pel- mm long, oriented at a 45° angle from the wing margin; stipe
tate glands and sparse trichomes, or glabrous. Inflorescence 10–15 mm long; seeds ca. 1 × 0.5 cm, oblong to triangular, the
axes, peduncles and calyces matted with dense dark brown testa glossy, light brown. Figures 5A, H-I; 6A-C.
trichomes and peltate glands; bracts 1.5–4 × 1.5–3 mm, ovate, Distribution—Eastern Brazil, from Santa Catarina to Ceará
persistent, reflexed, the apex acute; bracteoles 2–3 × 0.5–1.5 and Minas Gerais, and eastern Bolivia in the departments of
mm, elliptic, persistent, the apex obtuse or acute. Flowers La Paz and Santa Cruz, 30–680 m elevation. Figure 1.
10–12 mm long; pedicel 2–3 mm long; calyx campanulate, the Habitat and Phenology—Rain forest and SDTF. In Brazil
tube 5–7 mm, the base acute or obtuse, the three abaxial lobes it prefers riverine habitats, while in Bolivia it grows in rain
2–3 mm long, the apices acute, the two fused adaxial lobes forest to SDTF. Prolific flowering from November to May in
352 SYSTEMATIC BOTANY [Volume 34

Fig. 5. A–V. Part of an inflorescence, an open calyx with detail of indumentum, a bract, and a leaflet of all Centrolobium species. A, H, I. C. microchaete
[from Mendonça et al. 136, K]. B, J, K. C. ochroxylum [from Klitgaard et al. 421, K]. C, L, M. C. paraense [from Jansen-Jacobs et al. 4192, K]. D, Q, R. C. robustum
[from Corcovado 15921, K]. E, N, O, P. C. sclerophyllum [from Occhioni 16363, K]. F, S, T. C. tomentosum [from Hage 1646, K]. G, U, V. C. yavizanum [from Zarucchi
et al. 4957, K]. Scalebars: 1 mm in I, K, L, P, Q, T, V (shared: 3); 5 mm A, B, C, D, E, F, G (shared: 1); 10 mm in the leaflets of H, J, M, N, Q, S, U (shared: 2); and
5 mm in the inflorescences of H, J, M, O, Q, S, U. Drawn by Margaret Tebbs.
2009] PIRIE ET AL.: CENTROLOBIUM 353

Fig. 6. A–U. The samara seed chamber and detail of the base of a seed chamber spine; and part of the samara wing and detail of the samara wing of
all Centrolobium species. A, B, C. C. microchaete [from Saldías 377, K]. D, E, F. C. ochroxylum [from Palacios et al. 818, K]. G, H, I. C. robustum [from Martius
160, K]. J, K, L. C. sclerophyllum [from Santos 4, K]. M, N, O. C. yavizanum [from Zarucchi et al. 4957, K]. P, Q, R. C. paraense [from Davis 786, K]. S, T, U. C.
tomentosum [from Hatschbach & Zelma 49536, K]. Scalebars: 1 mm in A, D, G, J, M, P, S (shared: 3); 20 mm B, E, H, K, N, Q, T (shared: 1); and 2 mm in C, F,
I, L, O, R, U (shared: 2). Drawn by Margaret Tebbs.
354 SYSTEMATIC BOTANY [Volume 34

Brazil and from March to April in Bolivia; fruit set from May the wing petals ca. 15–4 mm long, blade oblong, auriculate at
to November in Brazil, and from May to October in Bolivia. the base of the blade, and with the basal ½ covered in sculp-
Centrolobium microchaete is deciduous, and the leafless stage turing, the keel petals ca. 15 × 5 mm, the blade triangular,
coincides with fruit set at the end of the dry season. auriculate at the base of the upper margin, fused for ¼ of the
Uses and Vernacular Names—Used in the manufacture lower margins; stamens ca. 15 mm long, fused basally for ½
of fine furniture, laminate sheets for decorative panels, floor their length. Samara 10.5–27 × 4.1–10 cm; seed chamber 3–5
panels, handicrafts, and railway sleepers (Lorenzi 2002). cm in diameter, the spines 15–40 × 0.5–1 mm, the basal parts
“Araribá” (Bahia, Santa Catarina, Parana, Rio de Janeiro and sparsely indumented with straight trichomes ca. 0.1 mm long
Minas Gerais), “gororoba” (Bahia), “lei nova” (Minas Gerais), and subsessile peltate glands; wing chartaceous, glabrous
“petimujú,” “putumujú,” “putumujú-mirim” (Bahia and Ceará), but with glands as on the seed chamber; stylar spine fused to
“tarara,” “tarara amarilla,” and “madera canaria” (Bolivia). samara wing for 3–14 mm long, the free apex 4–16 mm long,
Conservation Status—VU A1cd ~ vulnerable because of a at a 120° angle with the wing margin; stipe 6–10 mm long;
population size reduction of ≥ 50% over the last 10 yr due to seeds 2–3 × 1–1.5 cm, oblong, testa thin, green. Figures 5B,
a decline in area of occupancy, extent of occurrence and/or J-K; 6D-F.
quality of habitat, and due to actual and potential levels of Distribution—Ecuador, west of the Andes and the adjacent
exploitation. Tumbes area in Peru at 0–350 m. Figure 1.
Representative Specimens Examined—BOLIVIA. Beni: Ballivian, Feb Habitat and Phenology—The species is found in SDTF
1990, Smith et al. 14429 (MO). La Paz: Nor Yungas, 1 km from Buena on a mixture of soils. It is sometimes cultivated as a hedge-
Vista, 5 May 1989, (fr.) Beck 17203 (K, MO, NY, LPB). Santa Cruz: Andres
Ibañez, Santa Cruz, Velasco Ave, north of Irala Ave, 2001, (fr.) Pirie & row tree. Flowering has been recorded in October and fruit
Chatrou 1 (U). set in September, February, May, and June. Centrolobium
BRAZIL. Bahia: ROAD Itacaré-Ubaitaba, 16 May 1966, Belém & Pinheiro ochroxylum is a deciduous species in which the leafless stage
2219 (NY). Minas Gerais: Caratinga 10 Nov 1993, Klitgaard et al. 17 (AAU, coincides with fruit set, and trees develop new leaves while
K, RB). Paraná: Morretes 10 Mar 1983, Hatchbach 46250 (AAU, F, K). flowering.
Santa Catarina: Morro de Fazenda, Itajai, 10 Jun 1954, Reitz & Klein 1877
Uses and Vernacular Names—It is cultivated as a hedge tree
(K, NY).
and as coffee shade, and for timber used in house, boat, and
Notes—Centrolobium microchaete is primarily distinguished
furniture construction (Little and Dixon 1969). “Amarillo”,
by its small (10–12 mm) flowers vs. 12–22 mm in the other
“amarillo de Guyaquil”, “amarillo lagarto”, “araribá” (Rudd
Brazilian species. From C. robustum in particular it is fur-
1954; Acosta-Solis 1947).
ther distinguished by 9–13(-19)-foliolate leaves and 6.8–17.5
Conservation Status—Centrolobium ochroxylum is in the
cm long samaras vs. (13-)15–19(-23)-foliolate leaves and
Red List of endemic species of Ecuador 2000 (Neill 2000),
(10-)18–26 cm long samaras. C. microchaete is the only species
even though no threat category was attached to it in that pub-
of Centrolobium found in Bolivia. Despite variation in the size
lication. In a study that identifies biodiversity conservation
of fruits and flowers (generally larger in Bolivian material) all
priorities for coastal northern South America, Peralvo et al.
Bolivian specimens share characteristics diagnostic of C. micro-
(2007) calculated the percentage decline in potential distribu-
chaete, notably the persistent recurved bracts, indument type
tion (km2) to be 82.2% for C. ochroxylum, but still no category
and longer stipe found in neither C. ochroxylum nor C. tomen-
tosum (with which they have sometimes been confused). was attached. The conservation status of the species is, based
to the available information, judged to be Near Threatened
2. Centrolobium ochroxylum Rose ex Rudd, J. Wash. Acad. (NT).
Sc. 44: 9. 1954.—TYPE: ECUADOR. El Oro: Portovelo Representative Specimens Examined—ECUADOR. Cañar: La
(near Zaruma), 6 Oct. 1918, J.N. Rose & G. Rose 23370 Troncal, 2, Mar 1996, Neill et al. 10527 (MO). El Oro: Bosque Petrificado
Puyango, el Mirador, Klitgaard et al. 421 (AAU, K, LOJA, NY).
(holotype: US (no. 1022875)!; isotype: GH!, NY!).
Esmeraldas: Anchayacu, 9 Nov 1994, Pennington et al. 15012 (K, NY).
Tree 6–30 m tall; trunk diameter 15–60 cm, sometimes but- Guayas: Cerro Azul, 18 Mar 1980, (fl.) Dodson et al. 9651 (US, MO). Loja:
tressed to ca. 1 m tall; bark pale brown with grey patches Hacienda Banderones, 8 Jun 1997, Klitgaard et al. 551 (AAU, K, LOJA,
to whitish buff, smooth or lightly vertically and longitu- NY). Los Ríos: Canton Vinces, Jauneche Forest, 1 Oct 1979, Dodson
et al. 8646 (MO). Manabi: Jama Canton, 18 Dec 1998, Neill et al. 11644
dinally fissured, the slash exuding a cream/pink sap, the (K, MO, NY). Napo: Estación Experimental INIAP-Payamino, 3 km north
twigs and the inflorescences drying blackish brown. Leaves of Coca, 22 Sep 1985, (fr.) Palacios et al. 818 (K, MO, AAU, NY).
(7-)9–13(-17)-foliolate; stipules ca. 2 × 2 mm long, deltoid, PERU. Cerro de Pasco, Central Selva, 17 May 1985, Hartshorn et al. 2763
caducous; leaflets 6–20 × 5–14 cm, ovate or elliptic, the base (MO). Tumbes: Matapalo, Zarumilla, 7 Feb 1993, Diaz et al. 6606 (MO).
symmetric, cordate or rounded, the apex shortly acuminate, Notes—Centrolobium ochroxylum, the only species occurring
membranaceous, both the surfaces covered with sparse to in Ecuador, and just ranging into adjacent northwestern Peru,
dense curly trichomes, the lower surface also with dense pel- is easily distinguished by its large (10–27 cm long) samaras
tate glands. Inflorescence axes, peduncles and calyces with in which the stylar spine is at a 90–120° angle with the wing
dense dark brown (nearly black) trichomes and dense pel- margin (in the remaining species it is mostly at a 45° to 90°
tate glands; bracts 2–2.5 × 3–3.5 mm, fan-shaped, caducous, angle).
reflexed, the apex rounded; bracteoles 1.5–2 mm × 0.8–1.25
3. Centrolobium paraense Tul., Arch. Mus. Par. 4: 87. 1844.—
mm, narrowly ovate, the apex acute, usually caducous.
TYPE: GUYANA. Pirara, 1841, Schomburgk 314 (holotype
Flowers 15–18(-25) mm long; pedicel 4–6 mm long; calyx cam-
P!; isotypes: BM!, F!, G n.v., K!)
panulate, 12–16 mm long, the tube ca. 8 mm long, the three
abaxial lobes 5–8 mm long, the apices acute, the base obtuse Centrolobium paraense var. orinocense Benth., in Mart. Fl. Bras.
or acute, the two fused adaxial lobes ca. 5 mm long, the apex 15.1: 266. 1862. C. orinocense (Benth.) Pittier, Bol. Tecn.
emarginated, acute; corolla yellow, venation dark orange, Minist. Agric. 5: 123 1944.—TYPE: VENEZUELA. Bolivar:
the standard petal ca. 15 × 12 mm, suborbicular, reflexed by “prope Angustura” (Ciudad Bolívar), May 1851, Purdie
anthesis, with a central dark orange or pale yellow blotch, s.n. (holotype: K!, NY photo of type no. 2678).
2009] PIRIE ET AL.: CENTROLOBIUM 355

Centrolobium patinense Pittier, J. Wash. Acad. Sci. 5: 470. quality of habitat, and due to actual and potential levels of
1915.—TYPE: PANAMA: Darién, Punta Patiño, Pittier exploitation.
6611 (holotype: US!). Representative Specimens Examined—BRAZIL. Roraima: Rio Branco,
Boa Vista, Estação ecologica de Maracá, 8 Mar 1987, (fr.) Lewis 1420
Trees 4–30 m tall; trunk diameter 15–100 cm; bark red- (K, NY).
dish-brown with fine vertical fissures, the slash exuding COLOMBIA. Atlántico: Barranquilla, Jan 19, 38, Elias 1580F (A, NY,
US).
reddish sap; young twigs and inflorescences drying a green- GUYANA. Rupununi: Bushisland, Dadanawa, 9 Jun 1995, (fl.) Jansen-
ish-cream color. Leaves (5-)9–11-foliolate; stipules ca. 15 × 15 Jacobs et al. 4012 (K, NY, U, US).
mm, broadly ovate leaf-like, usually persistent, rarely cadu- PERU. Madre de Dios: Cocha Cashu, Manu National Park, 31 Aug
cous; leaflets 7–17 × 4–8 cm, ovate to broadly ovate, the base 1989, Foster 9940 (F, MO).
PANAMA. Darien: Punta Patiño, Darien, Pittier 6611 (US).
usually symmetric, subcordate or rounded, the apex acumi-
TRINIDAD. Port of Spain, Botanic Garden 10 Aug 1923, Fairchild 2844
nate or obtuse, membranaceous, the upper surface glabrate (NY, US).
or with dense curly trichomes, the lower surface venation VENEZUELA. Anzoategui: Bergantín, 14 Mar 1945, Steyermark 61487 (F,
covered with indumentum similar to that of the upper sur- MO). Aragua: Entre Villa de Cura y San Juan de los Morros, 26 Dec 1923,
face, the lower surface lamina with dense peltate glands. Pittier 11358 (NY, US). Bolivar: Monteco, 4 Aug 1978, Liesner & Gonzales
6000 (AAU, MO, NY). Guarico: Calabozo, Jun 1969, (fl.) Aristeguieta 7155
Inflorescence axes, peduncles and calyces with dense rusty (MO, NY, US). Portuguesa: Guanare, 13 Mar 1982, (fr.) Liesner et al. 12654
brown, curly trichomes and dense peltate glands; bracts (MO). Sucre: Fila de Guayuta, 18 Aug 1973, (fl.) Steyermark et al. 107725
5–10 × 5–10 mm, broadly ovate, persistent, the apex acum- (F, MO, NY). Zulia: Santa Rosa, 21 Aug 1967, (fr.) Steyermark & Fernandez
inate; bracteoles ca. 10 × 5 mm, broadly ovate, persistent. 99547 (F, NY, U, US).
Flowers 12–19 mm long; pedicel 5–8 mm long; calyx cam- Notes—Centrolobium paraense is easily distinguished from
panulate, the tube ca. 9–10 mm long, the base acute, the three all other Centrolobium species by its large leafy stipules that
abaxial lobes 6–8 mm long, the two fused adaxial lobes ca. leave a large scar when dropping off and by the large, broadly
6 mm long, the apex emarginated, obtuse; corolla dark yel- ovate bracts and bracteoles (5–10 × 5–10 mm).
low to orange, the venation red, the standard petal 12–14 × Bentham (1862) described two varieties of C. paraense: var.
12–14 mm, orbicular, reflexed by anthesis, with central paraense and var. orinocense. The latter was subsequently raised
bright red to purple blotch, the wing petals 12–15 × 5–5 mm, to the status of species by Pittier (1944). Variety orinocense was
blade ovate, auriculate at the base of the upper margins and distinguished from the typical variety by glabrescent leaf-
with the outer surface covered in sculpturing, the keel pet- lets with cordate bases vs. leaflets with dense indumentum
als 14–15 × 5 mm, the blade boomerang-shaped, auriculate and rounded bases. In our studies these differences are, how-
at the base of the upper margins, fused for 1/3 of the lower ever, not upheld as leaves posses a combination of cordate
margins; stamens 12.5–13 mm long, fused basally for ¼ to ½ and rounded leaflet bases, and as the amount of indumentum
of their length. Samara 12–22 × 4–8 cm; seed chamber 2–4.5 seems to be correlated with the age of the leaves.
cm in diameter, the spines 10–30 × 1–1.5 mm, the basal part 4. Centrolobium robustum (Vell.) Mart. ex Benth., Ann.
densely indumented with curly trichomes ca. 1 mm long and Wien Mus. 2: 95.1839. C. robustum var. macrochaete Mart.
subsessile peltate glands, the apical part similar to basal part ex Benth. Mart. Fl. Bras. 15(1): 263. 1862. Nissolia robusta
or glabrate; indumentum dense with ca. 0.5 mm long, curly Vell. Fl. Flum.: 298. 1825.—TYPE: BRAZIL. Rio de Janeiro:
trichomes and subsessile peltate glands; wing chartaceous, “habitat in silvis maritimis”, (lectotype: Fl. Flum. Icon. 7:
with indumentum and glands as of the seed chamber; stylar tab 85. 1827[1831].
spine fused to samara wing for 15–25 mm long, the free apex Centrolobium minus C. Presl., Bot. Bemerk.: 62. 1844.—TYPE:
7–12 mm long, often at a 90° angle rarely at a 45° angle with BRAZIL. Rio de Janeiro: “Habitat ad Rio de Janeiro
the wing margin; stipe 10–20 mm long; seeds not observed. Brasiliae”, “prope urbem in valle Larangeiras”, April
Figures 5F, S-T; 6P-R. 1834 [seen on BR specimen], Luschnath s.n. [labelled
Distribution—Centrolobium paraense is distributed along the Martii Herb. Fl. Bras. n. 160 on specimen in K] (holotype:
Caribbean coast of Guyana, Venezuela and adjacent Colombia PR? n.v.; isotypes: BR!, K!, MO!).
and Panama, stretching into Amazonian Brazil reaching as Centrolobium minus C. Presl. var. longo-stipitata N. F. Mattos,
far south as Rio Branco in Roraima, at altitudes between 50 Loefgrenia 78: 6. 1983.—TYPE: BRAZIL. Rio de Janeiro:
and 350 m above sea level. It remains unclear if the species is “Habitat in Estado do Rio de Janeiro, Jardim Botânico”,
native to or introduced into Trinidad. Figure 1. Nov. 1969, Mattos 494 (holotype: RB n.v.).
Habitat and Phenology—Centrolobium paraense is found in Tree (7-)15–30 m tall; diameter unknown; bark lightly fis-
a wide range of habitats from being a dominant species in sured; twigs and inflorescences drying blackish brown,
the SDTF of El Sombrero-Chaguramas-Tamanaco in Guarico, glabrate. Leaves (13-)15–19(-23)-foliolate; stipules cadu-
Venezuela to the savannas of Guyana and tropical rain for- cous, not observed; leaflets 4–12(-18) × 1.5–6(-9) cm, elliptic
est in Brazil. Flowering specimens were collected in March or oblong, the base usually asymmetric, cordate, or rounded,
(Brazil), otherwise from May to September. Fruit sets from the apex cuspidate, coriaceous, both the surfaces glabrous or
February to August The species is often described as drop- with sparse curly trichomes, the lower surface with dense ses-
ping most or all of its leaves between February and April. sile peltate glands. Inflorescence axes, peduncles and calyces
Uses and Vernacular Names—“Pau Raihna” (Brazil); glabrate or with sparse rusty brown curly trichomes; bracts
“Kartang” (“Makusi”), “redwood” or “shipuradai” (“wapisi- 3.5–6.5 × 2.5–4 mm, ovate, persistent, reflexed, the apex
ana”) (Guyana); “baluster”, “cartán” or “colorado” (Venezuela); acuminate; bracteoles 2.8–3.1 × 0.6–0.9 mm, ovate, the apex
“Colorado” (Colombia); “porcupine tree” (Trinidad). acute, persistent. Flowers 17–18 mm long; pedicel 6–11 mm
Conservation Status—VU A3cd ~ vulnerable because of a long; calyx tubular, the tube ca. 8 mm long, the base obtuse,
population size reduction of ≥ 30% over the next 10 yr due to the three abaxial lobes 5–7 mm long, the apices obtuse, the
a decline in area of occupancy, extent of occurrence and/or two fused adaxial lobes ca. 7 mm long, the apex emarginate,
356 SYSTEMATIC BOTANY [Volume 34

obtuse; corolla dark yellow to orange suffused with dark red, 5. Centrolobium sclerophyllum Lima, Arq. Jard. Bot.
the venation red, the standard petal 15–16 × 11–12 mm, orbic- Rio de Janeiro 27: 182. 1985.—TYPE: BRAZIL. Espírito
ular, reflexed by anthesis, with central bright red to purple Santo: Reserva Florestal da C.V.R.D., Linhares, próximo
blotch, the wing petals 15–16 × 5–6 mm, blade ovate, auricu- a estrada 161, talhão 604, 20/11/1973, J. Spada 205 (holo-
late at the base of the upper margins and with the outer sur- type: RB !, isotypes: COL n.v., CVRD n.v., RBR n.v.).
face covered in sculpturing, the keel petals 15–16 × 5–6 mm, Tree 6–30 m tall; trunk diameter 15–70 cm, the bark lightly
blade boomerang-shaped, auriculate at the base of the upper fissured; twigs and inflorescences drying reddish brown.
margins, fused for 1/3 of the lower margins; stamens 12.5– Leaves (11-)13–17(-19)-foliolate; stipules caducous, not
13 mm long, fused basally for ¼ to ½ of their length. Samara observed; leaflets (3-)5–9(-12) × (1.5-)2–4(-5) cm, ovate, the
(10-)18–26 × 5–8 cm; seed chamber 3–3.5 cm in diameter, the base asymmetric or symmetric, cordate or rounded, the apex
spines 15–35 × 0.5–1 mm, the basal part densely indumented long-acuminate, coriaceous, the upper surface glabrous, dark
with curly trichomes ca. 1 mm long and short-stalked peltate green, the lower surface rusty brown, glabrous and with
glands, the apical part shiny rusty brown, glabrous; wing dense short-stalked peltate glands. Inflorescence axes, pedun-
chartaceous with indumentum and glands as those of the cles and calyces matted with rusty brown curly trichomes;
seed chamber; stylar spine fused to the wing for 20–30 mm, bracts 3–5 × 1.5–3.5 mm, deltate, persistent, reflexed, the
free apex ca. 10 mm long, at a 45° angle with the wing margin; apex obtuse; bracteoles 1.5–3 × 0.6–1.2 mm, ovate, the apex
stipe 15–20 mm long; seeds not observed. Figures 5D, Q-R; obtuse, persistent. Flowers 16–17 mm long; pedicel 1–2 mm
6G-I. long; calyx urceolate, the tube 6–6.5 mm long, the base trun-
Distribution—Centrolobium robustum occurs in the states of cate, the three abaxial lobes 3–4 mm long, the apices acute,
Bahia, Rio de Janeiro and São Paulo in Brazil, from 0–750 m. the two fused adaxial lobes 2–3 mm long, the apex emargin-
Figure 1. ate, acute; corolla yellow, the venation deep red, the standard
Habitat and Phenology—The species occurs in coastal rain petal 15–16 × 11–12 mm, the wing petals 14–15 × 5–6 mm, the
forest and in coastal scrub. Flowering specimens were col- blade oblong, auriculate at the base of the upper margins and
lected in November, fruiting in November, March, July, and with the outer surface covered in sculpturing, the keel pet-
August. als 14–15 × 5–6 mm, the blade half-moon-shaped, auriculate
Uses and Vernacular Names—“Araribá”, “araribá amarelo”, at the base of the upper margins, loosely adnate for 1/3 of
“iriribá” and “erarobá” (Rio de Janeiro and São Paulo; Lima the lower margins; stamens 15–16 mm long, fused basally
1985), “lei nova”, “putumuju” (Brazil in general; Rudd 1954). for ½ of their length. Samara 10–12 × 3.5–4 cm; seed chamber
Conservation Status—CR A2cd ~ critically endangered 1.5–3 cm in diameter, the spines 7–16 × 0.5–1 mm, the basal
because of a population size reduction of ≥ 80% over the last with sparse indumentum of curly trichomes ca. 1 mm long
10 yr due to a decline in area of occupancy, extent of occur- and short-stalked peltate glands, the apical part shiny rusty
rence and/or quality of habitat, and due to actual and poten- brown, glabrate; wing chartaceous, glabrate or with sparse
tial levels of exploitation. 0.2 mm long, straight trichomes; stylar spine fused to samara
Representative Specimens Examined—BRAZIL. Bahia: Itabuna, 10 wing for 8–12 mm, the free apex 3–4 mm long, at a 45–90°
Jul 1964, (fr.) Silva 58331 (NY, US). Rio de Janeiro: Estrada Dona Castorina, angle with the wing margin; stipe 20–30 mm long; seeds not
18 Nov. 1985, Lima et al. 2622 (K). São Paulo: 4 Nov 1968, Koortfor s.n. observed. Figures 5E, N-P; 6J-L.
(NY).
Distribution—The species is found in the ‘Matas de tab-
Notes—Presl (1844) distinguished Centrolobium robustum uleiro’ in southern Bahia and northern Espirito Santo. A dis-
from C. minus by its larger samaras. Lima (1985) placed, how- junct population occurs in the semiarid caatinga formations
ever, C. minus in synonymy under C. robustum, arguing that of western Bahia and northern Minas Gerais, at altitudes from
the type specimen of C. minus represents a specimen with 400–1,000 m. Figure 1.
immature fruits. Habitat and Phenology—This little-known species occurs
The differences between C. robustum and the most similar in SDTF. Flowering specimens were collected in February and
species C. microchaete are described in the notes of the latter April, fruiting in February and July.
species. Uses and Vernacular Names—“Banha-de-galinha”, “pau de
Centrolobium robustum is distinguished from C. tomentosum sangue” and “putumujú pequeno” (Bahia) and “araribá”,
by its glabrous to glabrescent leaves and inflorescences (vs. “araribá rosa” and “lei rosa” or “lei nova” (Espirito Santo).
densely indumented, also at maturity), the ovate, relatively Conservation Status—CR A2cd ~ critically endangered
small bracts and bracteoles (vs. narrowly ovate), and the because of a population size reduction of ≥ 80% over the last
samara with a stylar spine at a 45° angle with the wing margin 10 yr due to a decline in area of occupancy, extent of occur-
(vs. at a 90° angle). The species differs from C. sclerophyllum by rence and/or quality of habitat, and due to actual and poten-
the relatively large membranaceous to coriaceous leaflets (vs. tial levels of exploitation.
small rigid-coriaceous leaflets in C. sclerophyllum), the ovate Representative Specimens Examined—BRAZIL. Bahia: Bom Jesus de
bracts and bracteoles (vs. deltate), and the (10-)18–26 cm long, Lapa, 2 Jul 1983, Coradin et al. 6358 (K, NY). Espirito Santo: 23 Aug 1981,
indumented samara (vs. 10–12 cm long, glabrescent). (fr.) Lima 1635 (K). Minas Gerais: Itaobim, 3 Mar 1982 (fl.), Rizzini & Mattos
Filho 1557 (RB). Rio de Janeiro: Quissamá, Faz. São Miquel, 14 Feb 2007
It has not been possible to locate the specimen cited as
(fl.), Lima et al. 6510 (RB).
the type of C. minus var. longo-stipitata Mattos (= Mattos 494).
Notes—Centrolobium sclerophyllum is readily distinguished
The diagnosis of C. minus var. longo-stipitata specifies, how-
from the other species occurring in eastern Brazil by the urce-
ever, the fruiting stipe length to 1.8–2.5 cm which, along with
olate calyx and rigid coriaceous leaflets.
the distribution, fits well with the range as below for C. robus-
tum: 1.5–2.0 cm. The only other diagnostic feature of C. minus 6. Centrolobium tomentosum Guillem ex Benth., Hook.
var. longo-stipitata is a leaf character which is too variable to Journ. Bot. 2: 66.1840.—TYPE: BRAZIL. Distrito Federal:
be reliable. “Brasilia, Cachoeira dos Campos”, P. Claussen & B.
2009] PIRIE ET AL.: CENTROLOBIUM 357

Delessert 879 (lectotype: K!; isolectotypes: F!, GH!, K! (2 Notes—For differences between C. tomentosum and C. micro-
sheets), NY!). chaete and C. robustum, see the notes under the latter two spe-
cies. Centrolobium tomentosum does, however, bear closest
Tree 10–35 m tall, trunk diameter 10–60 cm, the bark resemblance to C. paraense. It is best distinguished by the
smooth; twigs and inflorescences light orange brown. Leaves narrowly ovate, caducous stipules, bracts and bracteoles vs.
(11-)13–17(-19)-foliolate; stipules ca. 15 × 4 mm, narrowly the longer persisting leafy stipules and the broadly ovate
ovate, caducous; leaflets 7–16(-18) × 4–8(-10) cm, oblong bracts and bracteoles of C. paraense and the large flower size
or elliptic, the base asymmetric or symmetric, cordate or (18–22 mm vs. 12–19 in C. paraense).
rounded, the apex obtuse, coriaceous or membranaceous, the
upper surface with sparse, curly trichomes, the lower mat- 7. Centrolobium yavizanum Pittier, J. Wash. Acad. Sci. 5: 439.
ted with golden curly trichomes and dense peltate glands. 1915.—TYPE: PANAMA. Darién: Yaviza, 22 Apr 1914,
Inflorescence axes, peduncles and calyces matted with dark H. Pittier 6572 (holotype: US!; isotypes: BM!, GH n.v., NY!).
brown curly trichomes; bracts 4–5 × 3–4 mm, narrowly ovate,
caducous, upright, the apex acute; bracteoles 5–7 × 2–3 mm, Tree 8–25 m tall, with buttresses up to 1.8 m; trunk dia-
oblong, the apex acute, persistent. Flowers 18–22 mm long; meter 30–40 cm; twigs and inflorescences drying black-
pedicel 3–5 mm long; calyx campanulate, the tube ca. 8–9 ish brown. Leaves 13–17-foliolate; stipules caducous, not
mm long, the base obtuse, the three abaxial lobes 5–8 mm observed; leaflets 6.5–12 × 4–5.5 cm, elliptic, chartaceous or
long, the apices obtuse, the two fused adaxial lobes 5–7 mm membranaceous, the base asymmetric or symmetric, cor-
long, the apex emarginated, obtuse; corolla yellow suffused date or rounded, the apex acuminate, both the surfaces with
by red, the venation dark red, the standard petal 15–16 × ca. sparse straight trichomes and lower surface rusty brown,
14 mm, reflexed by anthesis, the wing petals 14–15 × 5–6 mm, covered in short-stalked glands. Inflorescence axes, pedun-
blade oblong, auriculate at the base of the upper margins cles and calyces matted with dark brown curly trichomes;
and with the outer surface covered in sculpturing, the keel bracts 3–5 × 1.5–3 mm, narrowly ovate, persistent, reflexed,
petals 14–15 × 5–6 mm, blade half-moon-shaped, auriculate the apex acute; bracteoles 1.5–2.5 × 1–1.5 mm, narrowly ovate,
at the base of the upper margins, loosely adnate for 1/3 of the the apex acute, persistent. Flowers 10–12 mm long; pedicel
lower margins; stamens 15–16 mm long, fused basally for ½ 3–7 mm long; calyx tubular, the tube 5–6 mm long, the base
of their length. Samara 13–18(-23) × 6–8(-9) cm; seed chamber obtuse, the three abaxial lobes 2–5 mm long, the apices acute,
3–5 cm in diameter, the spines 9–30 × 1–1.5 mm, the basal and the two fused adaxial lobes ca. 5 mm long, the apex emar-
apical parts moderately indumented with curly trichomes ginated, acute; corolla yellow/orange with central portion of
ca. 1 mm long and long-stalked peltate glands; wing charta- standard red, the standard petal 11–12 × 9–10 mm, the wing
ceous or coriaceous, with indumentum and glands as those petals ca. 10 × 3.5 mm, the keel petals ca. 12 × 4 mm; stamens
of the seed chamber; stylar spine fused to samara wing for 10–11 mm long. Samara 7.2–16 × 3.4–5.8 cm; seed chamber
40–50 mm, the free apex ca. 20 mm long, at a 90° angle with ca. 3 cm in diameter, the spines 10–20 × 0.5–1 mm, the basal
the wing margin; stipe 10–15 mm long; seeds ca. 20 × 10 mm, part sparsely indumented with curly trichomes ca. 1 mm long
oblong, smooth, the testa glossy rusty brown. Figures 5F, S-T; and long-stalked peltate glands, the apical part rusty brown,
6S-U. shiny, glabrate; wing chartaceous, glabrate, with sparse long-
Distribution—Centrolobium tomentosum has a wide geo- stalked peltate glands; stylar spine fused to samara wing
graphic range in central and eastern Brazil from São Paulo for 3–5 mm long, the free apex 6–14 mm long, at a 45–90°
to Bahia and extending into the interior of Goiás, from 0–750 angle with the wing margin; stipe 20–30 mm long; seeds not
m. Figure 1. observed. Figures 5G, U-V; 6M-O.
Habitat and Phenology—It occurs naturally in savanna and Distribution—The species occurs in Darién province of
associated gallery forest, in varzea (floodplain) forest, and in Panama, and Bolivar, Santander, Antioquia and Boyacá
coastal rain forest mixed with restinga; and is cultivated and departments in Colombia, at sea level. Figure 1.
invasive in secondary forests. The species is deciduous, and Habitat and Phenology—Centrolobium yavizanum has been
flowering was recorded in January to March, while fruit set collected in remnant primary SDTF and in disturbed areas
takes place from August to November. such as roadside vegetation and as trees remaining in pas-
Uses and Vernacular Names—The species has beautiful tures. Flowering usually occurs from March to June, and fruit-
wood that is used in boat and canoe construction, and for ing from March to July.
furniture and carriages (Lorenzi 1992). “Araribá”, “araribá- Uses and Venacular Names—“Guayacán jobo” (Colombia).
rosa”, “aribá”, “araruva”, “ararauba”, “carijó”, “iriribá-rosa”, Conservation Status—The species has been designated
“putumuju” (Bahia), “tipiri” (Minas Gerais). ‘vulnerable’ on the IUCN red list of threatened species (Mitré
Conservation Status—VU A3cd ~ vulnerable because of a 1997), due to threats of habitat loss through logging, clear cut-
population size reduction of ≥ 30% over the next 10 yr due to ting and human settlement.
Representative Specimens Examined—COLOMBIA. Antioquia: 23 Mar
a decline in area of occupancy, extent of occurrence and/or 1987, Zarucchi et al. 4957 (K, MO, NY, US). Bolivar: Loba, Amargamiento
quality of habitat, and due to actual and potential levels of Rico, Apr 1916, Curran 483 (GH). Boyacá: Guaguaqui, 14 Jul 1917, Whitford
exploitation. & Pinzon 16A (A). Choco: Léon 550 (MO). Santander: Puerto Berrio, 30 Apr
Representative Specimens Examined—BRAZIL. Bahia: Ilheus, 1935, Haught 1688 (NY).
Centro de Pesquisas do Cacau (CEPLAC), Pennington & Carvalho 293 PANAMA. Darién: Pico Pedenjo, 15 Mar 1968, Duke 15424 (MO). Panama:
(E, K). Distrito Federal: Campus de IBDF, 28 Jul 1989, França & Melo 20331 El Llano, 1 Sep 1971, Gentry & Tyson 1731 (MO).
(NY). Espirito Santo: Linhares, 13 Nov 1993, Klitgaard et al. 27 (AAU, K, Notes—Centrolobium yavizanum is most similar to C. micro-
RB). Gioás: Corrumba de Goiás, 25 Jan 1968, Irwin et al. 19160 (K, NY). chaete (occurring in Bolivia and southern Brazil), from which
Minas Gerais: 1840, Claussen 879 (BM, F, GH, K, NY). Paraná: Arapoti, 28
Jan 1989, Hatchbach 52799 (NY). Rio de Janeiro: Rio de Janeiro, 13 Aug
it cannot readily be distinguished in flower, though the bracts
1984, Oliviera 43 (NY). São Paulo: Bofetem, 9 Apr 1971, Gottsberger & are generally larger and ovate (vs. smaller and narrowly
Gottsberger 9471 (NY). ovate) and the calyx lobes acuminate rather than acute. In
358 SYSTEMATIC BOTANY [Volume 34

fruit, it can be distinguished by the greater length of the stipe Pennington, R. T., M. Lavin, D. E. Prado, C. A. Pendry, S. K.Pell, and
(20–30 mm vs. 10–15 mm). C. A.Butterworth. 2004. Historical climate change and specia-
tion: neotropical seasonally dry forest plants show patterns of both
Tertiary and Quaternary diversification. Philosophical Transactions of
Acknowledgments. MDP thanks SYNTHESYS for financial support
the Royal Society B. Biological Sciences 359: 515–538.
to visit the Natural History Museum in London and the Royal Botanic
Pennington, R. T., G. Lewis, and J. A. Ratter. 2006. An overview of the
Gardens, Kew. DNA sequencing was carried out in the labs of the Royal
plant diversity, biogeography and conservation of neotropical savan-
Botanic Garden, Edinburgh and Utrecht University, The Netherlands. The
nas and seasonally dry forests. Pp. 1–29 in Neotropical savannas and
authors are grateful to Haroldo C. de Lima for providing the study with
seasonally dry forests, eds. R. T. Pennington, G. Lewis, and J. Ratter.
Centrolobium leaf samples, to Will Goodall Copestake for sequences, and
London: Taylor and Francis.
we thank Margaret Tebbs for the beautiful line drawings. The construc-
Pennington, R. T., D. E. Prado, and C. A. Pendry. 2000. Neotropical sea-
tive and detailed comments of two anonymous reviewers are gratefully
sonally dry forests and Quaternary vegetation changes. Journal of
acknowledged.
Biogeography 27: 261–273.
Peralvo, M., R. Sierra, K. R. Young, and C. Ulloa-Ulloa. 2007. Identification
Literature Cited of biodiversity conservation priorities using predictive modeling: an
application for the equatorial region of South America. Biodiversity
Acosta-Solis, M. 1947. Commercial possibilities of the forests of Ecuador– and Conservation 16: 2649–2675.
mainly Esmeraldas province. Tropical Woods 89: 1–47. Pittier, H. 1944. Centrolobium orinocense (Benth.) Pittier. Boletin Tecnico.
Bentham, G. 1839. Centrolobium Mart. ex Benth. Annalen des Wiener Museums Ministerio de Agricultura y Cria. Caracas 5: 123.
der Naturgeschichte 2: 95. Polhill, R. M. 1981. Dalbergieae. Pp. 233–242 in Advances in legume system-
Bentham, G. 1862. Centrolobium. Pp. 263–264 in Flora Brasiliensis 15 part atics, part 1, eds. R. M. Polhill and P. H. Raven. Richmond, Surrey:
1 fasc. 29, ed. C. F. P. v. Martius , A. W. Eichler, and I. Urban. Munich: Royal Botanic Gardens, Kew.
R. Oldenbourg. Polhill, R. M. 1994. Classification of the Leguminosae. Pp. 35–48 in
Beyra, M. A. and M. Lavin. 1999. Monograph of Pictetia (Leguminosae - Phytochemical dictionary of the Leguminosae 1, eds. F. A. Bisby,
Papillionoideae) and a review of the Aeschynomeneae. Systematic J. Buckingham, and J. B. Harbourne. London: Chapman and Hall.
Botany Monographs 56: 1–93. Posada, D. and K. A. Crandall. 1998. Modeltest: testing the model of DNA
Burnham, R. J. 1995. A new species of winged fruit from the Miocene substitution. Bioinformatics 14: 817–818.
of Ecuador: Tipuana ecuatoriana (Leguminosae). American Journal of Prado, D. E. and P. E. Gibbs. 1993. Patterns of species distributions in the
Botany 82: 1599–1607. dry seasonal forests of South America. Annals of the Missouri Botanical
Doyle, J. J. and J. L. Doyle. 1987. A rapid DNA isolation procedure for Garden 80: 902–927.
small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15. Presl, C. 1844. Botanische Bemerkungen. Abhandlungen der königlichen
Drummond, A. J., S. Y. W. Ho, M. J. Phillips, and A. Rambaut. 2006. Bohm Gesellschaft für Wissenschaft 3: 62.
Relaxed phylogenetics and dating with confidence. Public Library of Rambaut, A. and A. J. Drummond. 2003. Tracer, version 1.3. Available
Science. Biology 4: e88. doi: 10.1371/journal.pbio.0040088 from http://beast.bio.ed.ac.uk/Tracer.
Drummond, A. J. and A. Rambaut. 2007. BEAST: Bayesian evolution- Rudd, V. E. 1954. Centrolobium (Leguminosae): Validation of a specific
ary analysis by sampling trees. BMC Evolutionary Biology 7: 214. name and a brief review of the genus. Journal of the Washington
doi:10.1186/1471-2148-7-214 Academy of Sciences 44: 284–288.
Felsenstein, J. 1981. Evolutionary trees from DNA sequences: A maximum Sanderson, M. J. 2002a. Estimating absolute rates of molecular evolution
likelihood approach. Journal of Molecular Evolution 17: 368–376. and divergence times: a penalized likelihood approach. Molecular
Fitch, W. M. 1971. Toward defining the course of evolution: minimum Biology and Evolution 19: 101–109.
change for a specified tree topology. Systematic Zoology 20: 406–416. Sanderson, M. J. 2002b. r8s, version 1.50. Distributed by the author,
Huelsenbeck, J. P. and F. Ronquist. 2001. MrBayes: Bayesian inference of Section of Evolution and Ecology, University of California, Davis.
phylogenetic trees. Bioinformatics 17: 754–755. Savolainen, V., P. Cuénoud, R. Spichiger, M. D. P. Martinez, M. Crèvecoeur,
IUCN. 2001. IIRL Categories. Criteria: Version 3.1. IUCN Species Survival and J.-F. Manen. 1995. The use of herbarium specimens in DNA
Commission. phylogenetics: evaluation and improvement. Plant Systematics and
Lavin, M. 2006. Floristic and geographical stability of discontinuous sea- Evolution 197: 87–98.
sonally dry tropical forests explains patterns of plant phylogeny and Schrire, B. D., G. P. Lewis, and M. Lavin. 2005. Biogeography of the
endemism. Pp. 433–447 in Neotropical savannas and seasonally dry for- Leguminosae. Pp. 21–54 in Legumes of the world. eds. G. Lewis,
ests. eds. R. T. Pennington, G. Lewis, and J. Ratter. London: Taylor B. Schrire, B. Mackinder, and M. Lock. Richmond, Surrey: Royal
and Francis. Botanic Gardens, Kew.
Lavin, M., P. S. Herendeen, and M. F. Wojciechowski. 2005. Evolutionary Simmons, M. P. and H. Ochoterena. 2000. Gaps as characters in sequence-
rates analysis of Leguminosae implicates a rapid diversification of based phylogenetic analysis. Systematic Biology 49: 369–381.
lineages during the Tertiary. Systematic Biology 54: 575–594. Swofford, D. L. 2002. PAUP*: Phylogenetic Analysis Using Parsimony
Lavin, M., R. T. Pennington, B. B. Klitgaard, J. I. Sprent, H. C. De Lima, (*and other methods). Version 4. Sunderland: Sinauer Associates Inc.
and P. E.Gasson. 2001. The dalbergioid legumes (Fabaceae): delimita- Taberlet, P., L. Gielly, G. Pautou, and J. Bouvet. 1991. Universal primers for
tion of a pantropical monophyletic clade. American Journal of Botany amplification of the three non-coding regions of chloroplast DNA.
88: 503–533. Plant Molecular Biology 17: 1105–1109.
Lavin, M., M. Thulin, J.-N. Labat, and R. T. Pennington. 2000. Africa, Thomas, W. W. and M. R. de Vansconcellos Barbosa. 2008. Natural veg-
the odd man out: molecular biogeography of Dalbergioid Legumes etation types in the Atlantic coastal forest of northeastern Brazil.
(Fabaceae) suggests otherwise. Systematic Botany 25: 449–467. Pp. 6–20 in The Atlantic Coastal Forest of northeastern Brazil, ed. W.W.
Lima, H. C. D. 1985. Centrolobium Martius ex Bentham (Leguminosae - Thomas . Memoirs of the New York Botanical Garden vol 100. Bronx:
Papilionoideae) estudo taxonômico das espécies Brasilieras extra New York Botanical Garden.
Amazônicas. Arquivos do Jardim Botânicodo Rio de Janeiro 27:
177–191. Appendix 1. Names, vouchers and Genbank accessions for DNA sam-
Little Jr., E. L. and R. G. Dixon. 1969. Árboles comunes de la Provincia de ples used for molecular phylogenetic analyses. A code for Centrolobium
Esmeraldas. i-xii. Rome: FAO. samples (following the voucher) is used in the text and figures to discern
Lorenzi, H. 1992. Árvores Brasileiras vol. 1. Manual de indentificação e cul- samples of the same species. GenBank accession numbers are in the fol-
tivo de plantas arbóreas nativas do Brasil. Nova Odessa, Brazil: Editora lowing sequence: trnL-F, matK, ITS, replaced with — where not sampled.
Plantarum.
Lorenzi, H. 2002. Brazilian Trees 2. A guide to the identification and cultivation Centrolobium microchaete, (Mart. ex Benth.) Lima, Brazil, Paraná,
of Brazilian native trees. Nova Odessa, Brazil: Editora Plantarum. G. Hatchbach 46089 (F, NY), 769, -, EU401407, -; Centrolobium microchaete
Mitré, M. 1997. Centrolobium yavizanum. Pp. 351 in IUCN Red List of (Mart. ex Benth.) Lima, Brazil, Minas Gerais, B. B. Klitgaard 17 (AAU, K),
Threatened Species. E6, EU401419, EU401408, EU401431; Centrolobium microchaete (Mart. ex
Neill, D. 2000. Centrolobium. Pp. 97 in Libro rojo de las plantas endémicas Benth.) Lima, Bolivia, Santa Cruz, R. T. Pennington 898 (E), E1, EU401420,
del Ecuador eds. R. Valencia, N. Pitman, S. León-Yánez, and P. M. EU401409, EU401432; Centrolobium ochroxylum Rose ex Rudd, Ecuador, Los
Jørgensen. Quito: Publicaciones del Herbario QCA, Pontificia Ríos, B. B. Klitgaard 658 (AAU, K), E7, EU401421, EU401410, EU401433;
Universidad Católica del Ecuador. Centrolobium ochroxylum Rose ex Rudd, Ecuador, Loja, B. B. Klitgaard 551
2009] PIRIE ET AL.: CENTROLOBIUM 359

(AAU), E3, EU401422, EU401411, EU401434; Centrolobium ochroxylum Rose (3); Delgado 105 (2); Diaz et al. 4695 (2), 4878 (2), 5054 (2), 5410 (2), 5787 (2),
ex Rudd, Ecuador, El Oro, B. B. Klitgaard 421 (AAU, K), E5, -, -, EU401435; 6204 (2), 6289 (2), 6432 (2), 6467 (2), 6606 (2), 6714 (2); Dodson & Clendenin
Centrolobium paraense Tul., Brazil, Rio de Janeiro, Botanic Garden (cul- 11030 (2); Dodson & Thien 1293 (2); Dodson et al. 6921 (2), 8646 (2), 9651 (2),
tivated), H. C. de Lima 5688 (RB), 770, EU401423, EU401412, EU401436; 14551 (2); Ducke 332 (3), 516 (3), 35506 (3); Dugand 1126 (3); Duke 15424 (7);
Centrolobium paraense Tul., Guyana, Rapununi, Jansen-Jacobs 4192 (U), Elias 1580 (3); Fairchild 2814 (3); Forestry Department of British Guyana 138
1278, EU401424, EU401413, EU401437; Centrolobium robustum (Vell.) Mart. (3), 2160 (3), 2181 (3); Foster 9940 (3); França & Melo 20331 (6); Froes 19962
ex Benth., Brazil, Rio de Janeiro, Botanic Garden (cultivated), H. C. de Lima (1), 20171 (5), 23055 (3); Ganev 3462 (6); Gentry & Berry 15032 (3); Gentry
2506 (RB), 771, EU401425, EU401414, EU401438; Centrolobium sclerophyl- & Dodson 54849 (2); Gentry & Tyson 1731 (7); Gentry 8646 (2), 10306 (3);
lum Lima, Brazil, Bahia, Coradin 6358 (K), E24, -, EU401415, EU401439; Glaziou 2539 (6), 5715 (6), 15922 (6); Gottsberger & Gottsberger 9471 (6); Hage
Centrolobium sclerophyllum Lima, Brazil, Rio de Janeiro, Botanic Garden 1646 (6); Harris et al. 1088 (3); Hartshorn et al. 2763 (2); Hatschbach 15719 (6),
(cultivated), H. C. de Lima 1635 (K), 772, EU401426, EU401416, EU401440; 16355 (1), 16427 (6), 46038 (1), 46089 (1), 46250 (1), 52799 (6); Hatschbach
Centrolobium tomentosum Guill. ex Benth., Brazil, Rio de Janeiro, Botanic et al. 64144 (6); Hatschbach & Zelma 49536 (6); Haught 1688 (7); Helmreishen 89
Garden (cultivated), H. C. de Lima 2518 (RB), 773, -, EU401417, -; Centrolobium (6); Herbarium Guillem 592 (6); Hoffman 1048 (3); Hohenkerk 849 (3); Hopkins
tomentosum Guill. ex Benth., Brazil, Gioás, B. M. T. Walter 3343 (NY), E33, et al. 521 (3); Irwin et al. 12022 (6); 14033 (6); 15685 (6); 19160 (6); 31238 (5);
EU401427, EU401418, EU401441; Centrolobium yavizanum Pittier, Panama, Ivker s.n. (6); Jansen-Jacobs et al. 4012 (3), 4192 (3); Jardim 1370 (1), 1878 (1);
Darien, Stern 731 (NY, MO, GH), 775, EU401428, -, EU401442; Geoffroea Johansen 12 (2); Kinnup et al. 1004 (6); Kirkbride et al. 3581 (6); Klitgaard et al.
decorticans (Gillies ex Hook. & Arn.) Burkhart, USA, Arizona (seed source), 17 (1), 27 (6), 319 (2), 421 (2), 551 (2), 658 (2), 67008 (2), 99461 (2), 99487 (2);
M. Lavin 750 (MONT), -, AF270880, AF189057; Geoffroea decorticans (Gillies Koortfor s.n. (4); Koscinski & Pickel 4995 (6); Krukoff 10625 (1); Kuhlmann 3225
ex Hook. & Arn.) Burkhart, Chile, Gardner & Nees 5823 (E), AF208962, -, -; (3); 31626 (6); Kuniyoshi & Pizani 4644 (1); Lachman et al. 62 (7); Léon 550 (7);
Grazielodendron riodocense Lima, Brazil, Rio de Janeiro, Botanic Garden Lewis 1420 (3), 1697 (3), (2); Liesner & Gonzales 5419 (3), 5748 (3), 6000 (3),
(cultivated), H. C. de Lima s.n. (E), AF208952, AF270862, -; Paramachaerium 11077 (3); Liesner et al. 12654 (3); H. C. Lima 1635 (5); H. C. Lima et al. 2622
schomburgkii (Benth.) Ducke, Guyana, Kanuku Mts., Jansen-Jacobs 97 (K), (4), 3986 (1); J. Lima 790 (3); Little 6496 (2), 6557 (2), 6615 (2); Little & Dixon
AF208959, AF272062, AF204237; Platymiscium dimorphandrum Donn. Sm., 21175 (2); Louman & Oliviera 8701 (1); Madison et al. 3271 (2), 5232 (2) 5271
Mexico, J. I. Calzada 14786 (MEXU), -, -, EU401430; Platymiscium floribun- (2); Mamani & Rodriguez 515 (1); Mamani & Saucedo 616 (1), 819 (1), 875 (1);
dum Vogel, Brazil, Rio de Janeiro, B. B. Klitgaard 84 (K), -, -, EU401429; Martius 160 (4); Matthew 72812 (2), 71882 (2); Mattos et al. 333 (5); Mecenas &
Platymiscium sp., Colombia, Antioquia, R. T. Pennington 692 (E), AF208955, Cardoso 87 (6); Medri et al. 578 (6); Menacho & Jiminez 782 (1); Mendonca et al.
AF270871, -; Platymiscium stipulare Benth., Ecuador, Napo, R. T. Pennington 136 (1); Meneces & Hartshorn 2365 (1), 2375 (1); Mori et al. 9393 (6); Neill 6192
649 (E), -, AF270872, -; Platypodium elegans Vogel, Colombia, Antioquia, (2); Neill & Nuñez 10472 (2); Neill et al. 10527 (2), 11644 (2); Occhioni 16363
R. T. Pennington 688 (E), -, AF270877, -; Platypodium elegans Vogel, Brazil, (5); Oliveira 43 (6); Palacios et al. 818 (2); Peckolt s.n. or 260 (~Martius 160) (1);
Gioás, R. T. Pennington 488 (E), AF208961, -, -; Pterocarpus indicus Willd., Pedra do Cavalo 653 (1); Pendry 674 (1); R. T. Pennington & Carvalho 293 (6); R.
Phillipines, Luzon, R. T. Pennington 718 (E), AF208953, -, -; Pterocarpus indi- T. Pennington 898 (1), 916 (1); T. D. Pennington et al. 15012 (2); Pereira 11718
cus Willd., unknown locality, Henderson s.n. (NY), -, AF142691, -; Pterocarpus (6); Peter 49720 (2); Pirie & Chatrou 1 (1); Pittier 6572 (7), 6611 (3), 9736 (3),
macrocarpus Kurz, Puerto Rico, Fajardo (cultivated), M. Lavin 721 (MONT), -, 10514 (3), 11358 (3), 12240 (3); Prance et al. 9562 (3); Quevedo & Centurión 360
AF203588, AF269176; Ramorina girolae Speg., Argentina, Royal Botanic (1), 504 (1), 609 (1); Raimundo 1120 (1); Ramirez 2472 (3); Ratter et al. 5489 (3);
Gardens, Kew (cultivated), (no voucher), AF208957, AF270881, AF204236; Reidel 464 (4); Reidel & Luschnath 448 (4); Reitz 2931 (1); Reitz & Klein 1877
Tipuana tipu (Benth.) Kuntze, Argentina, Salta, M. Lavin 5796 (MONT), -, (1); Ribiero 283 (3); Rosa 3119 (3); Rosales et al. 658 (3); Rose & Rose 23370 (2);
AF270882, AF189056; Tipuana tipu (Benth.) Kuntze, Spain, Barcelona (cul- Ruiz 365 (3); Saldías 377 (1), 688 (1); Samaniego et al. 35 (2); F. S. Santos 3 (6),
tivated), R. T. Pennington s.n. (E), AF208956, -, -. 4 (5); T. S. Santos, 806 (1), 1899 (1); Schomburgk 314 (3), 590 (3); Seidel & Beck
240 (1); Sello s.n. (6); Silva 58331 (4); Silva et al. 2827 (1); Simpson & Schunke
Appendix 2. List of exsiccatae Abbott & Jardim 16395 (1); Abbott 522 (2); A. C. Smith 3207 (3); D. N. Smith et al. 14429 (1); F. D. Smith 280 (3);
16742 (1), 17279 (1); Aguilar et al. 680 (1); Aristeguieta 4710 (3), 7045 (3), 7155 Souza 2 (6); Stern et al. 731 (7), 761 (7); Steyermark 54016 (2), 61487 (3), 86772
(3); Asplund 15387 (2); Barreto 1509 (1); Beck 17203 (1); Belém et al. 954 (1); (3), 122979 (3), 123053 (3); Steyermark & Fernández 99547 (3); Steyermark
Belém & Pinheiro 2219 (1), 3392 (6); Bernardi 7386 (3); Blanco 381 (3); Brant et al. 107725 (3); Tamayo 2106 (3), 3524 (3); Thomas et al. 11906 (6); Toledo
1266 (7); Briceño & Rosales 142 (3); Bunting 17 (3), 230 (3), 5196 (3), 5211 (3), et al. 510 (1); Valverde 436 (2); I. G. Vargas C. 2450 (1), 5096 (1); I. G. Vargas C. &
5772 (3), 5773 (3) 7643 (3); Camara et al. s.n. (6); Camp 585 (2); Carabot et al. Contreras 5096 (1); I. G. Vargas C. et al. 2450 (1); J. A. Vargas 16 (2); Walter
4383 (3); Claussen s.n. (6); Coradin et al. 6342 (5), 6358 (5), 8587 (5); Corcovado et al. 3343 (6); Whitford 10 (3); Whitford & Pinzon 16A (7); Williams 11646 (3),
15921 (4); Cornejo & Bonifaz 2341 (2); Curran 483 (7); Daly 124 (2); Davis 786 11832 (3); Wilson-Browne 138 (3); Zarucchi et al. 4957 (7).