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Generic Relationships and Classification of Tribe Paullinieae (Sapindaceae) with a
New Concept of Supertribe Paulliniodae
Author(s): Pedro Acevedo-Rodríguez, Kenneth J. Wurdack, M. Silvia Ferrucci, Gabriel Johnson, Pedro
Dias, Rubens G. Coelho, Genise V. Somner, Victor W. Steinmann, Elizabeth A. Zimmer, and Mark T.
Strong
Source: Systematic Botany, 42(1):96-114.
Published By: The American Society of Plant Taxonomists
URL: http://www.bioone.org/doi/full/10.1600/036364417X694926
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Systematic Botany (2017), 42(1): pp. 96–114
© Copyright 2017 by the American Society of Plant Taxonomists
DOI 10.1600/036364417X694926
Date of publication March 1, 2017
Generic Relationships and Classification of Tribe Paullinieae (Sapindaceae)
with a New Concept of Supertribe Paulliniodae
Pedro Acevedo-Rodríguez,1,6 Kenneth J. Wurdack,1 M. Silvia Ferrucci,2 Gabriel Johnson,1 Pedro Dias,3
Rubens G. Coelho,3 Genise V. Somner,4 Victor W. Steinmann,5 Elizabeth A. Zimmer,1 and Mark T. Strong1
1Department of Botany, National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, Washington,
District of Columbia, 20013-7012, U. S. A.
2Instituto de Botánica del Nordeste, C. C. 209, 3400, Corrientes, Argentina.
3Escola de Artes, Ciências e Humanidades, Universidade de São Paulo, São Paulo, SP, Brazil.
4Universidade Federal Rural do Rio de Janeiro, Departamento de Botânica, Caixa postal 74582, CEP: 23851-970 – Seropédica,
Rio de Janeiro, Brazil.
5Instituto de Ecología, A. C., Centro Regional del Bajío, A. P. 386 61600 Pátzcuaro, Michoacán, Mexico.
6Author for correspondence (acevedop@si.edu)
Communicating Editor: Michael J. Moore
Abstract–—The current study examines all genera of Sapindaceae tribe Paullinieae sensu Acevedo-Rodríguez et al. (2011). Based on molecular
phylogenetic analyses of trnL intron and ITS sequence data along with critical evaluation of morphology, supertribe Paulliniodae is newly rec-
ognized and morphologically characterized by zygomorphic flowers, thyrses with lateral cincinni, corollas of 4 petals, and alternate leaves with
a well-developed distal leaflet. Paulliniodae contains four successively nested subclades designated as tribes Athyaneae, Bridgesieae,
Thouinieae, and Paullinieae. Athyaneae contains Athyana and Diatenopteryx, and is composed of trees with exstipulate pinnately compound
leaves, and isopolar, spherical, colporate pollen grains. Bridgesieae contains the monospecific shrub genus Bridgesia with exstipulate, simple
leaves, and isopolar, spherical, tricolporate pollen grains. Thouinieae is resurrected and amended to include three genera of trees or shrubs with
exstipulate trifoliolate or unifoliolate leaves. Paullinieae is circumscribed to include only six genera (Thinouia, Lophostigma, Cardiospermum,
Paullinia, Serjania and Urvillea) of climbers or climber-derived shrubs with stipulate leaves and a pair of inflorescence tendrils. Guindilia, previ-
ously considered a member of this clade, is shown to be more distantly related and not part of supertribe Paulliniodae. The following 14 new
combinations are made to incorporate the results of our findings: Serjania biternata, Serjania cristobaliae, Serjania dissecta, Serjania
guerrerensis, Serjania macrolopha, Serjania serjanioides, Serjania sonorensis, Serjania spinosa, Serjania tortuosa, Thinouia trifoliata, Urvillea
cuchujaquense, Urvillea oliveirae, Urvillea procumbens, and Urvillea pterocarpa.
Keywords—Athyaneae, Bridgesieae, Diatenopteryx, Guindilia, molecular phylogenetics, Thouinieae.
Since the publication of the most recent taxonomic
treatment of Sapindaceae (Acevedo-Rodríguez et al. 2011),
where four subfamilies (Xanthoceroideae, Hippocastanoideae,
Dodonaeoideae, and Sapindoideae) and 142 genera were recog-
nized, four new genera (Alatococcus Acev.-Rodr., Allophylastrum
Acev.-Rodr., Balsas J. Jiménez Ram. & K. Vega, and Gereaua
[Capuron] Buerki & Callm.) have been described. Following the
description of these new genera and the results of this analysis,
we currently recognize 144 genera with ∼1,900 species within
the family. According to Acevedo-Rodríguez et al. (2011),
the Sapindaceae in the New World contains about 925 species,
of which ∼475 belong to the Paullinieae (i.e. Paullinieae +
Thouinieae, sensu Radlkofer 1890, 1931-1934). Paullinieae are
primarily Neotropical with the exception of Paullinia pinnata L.,
Cardiospermum corindum L., and C. halicacabum L., which in
addition to their Neotropical ranges, are naturally distributed in
parts of the Paleotropics (Brncic et al. 2007; Gildenhuys et al.
2015). Thouinieae is by far more diverse at the generic level in
the Neotropics than in the Paleotropics. However, at the species
level, there are many more species (∼197 species) in the Paleo-
tropics, all ofwhich belong to the genusAllophylus (Coelho 2014).
The Paullinieae was proposed by Kunth as a “section” of
Sapindaceae in 1821 (Kunth 1821) to accommodateCardiospermum
L., Paullinia L., Serjania Mill., and Urvillea Kunth. This group of
herbaceous or woody climbers with tendrils was characterized
by the presence of well-developed petal appendages, unilateral
nectaries with distinct lobes, and 3-carpellate gynoecia with
uniovular locules. In 1824, de Candolle designated Kunth’s
Paullinieae as a tribe, which was later adopted by Radlkofer
in 1890 in his tribal classification of Sapindaceae that included
14 tribes. Radlkofer further characterized Paullinieae by the
presence of stipules, and compound leaves with a fully devel-
oped distal leaflet. The presence of stipules in the Paullinieae
is unique within Sapindaceae, while the latter two characters
are shared with members of the closely related Thouinieae.
Radlkofer divided Paullinieae into the subtribes Eupaullinieae
and Thinouineae. The Eupaullinieae was essentially the same
group as the one recognized by Kunth but further characterized
by the presence of zygomorphic flowers with hood-shaped
petal appendages. Subtribe Thinouineae solely contained
Thinouia Triana & Planch., described in 1862 (Triana and
Planchon 1862), and was characterized by the presence of acti-
nomorphic flowers with marginal or bifid petal appendages
and an annular disc. Additional genera were later included
in the Eupaullinieae: Lophostigma Radlk. was described in 1897
and is characterized by the presence of short petals and
heteropolar, prolate pollen grains; Houssayanthus Hunz. was
described in 1978 (Hunziker 1978) and is characterized by
mericarps with a circumferential wing; and Chimborazoa H. T.
Beck was described in 1992 (Beck 1992) and is characterized
by wingless spherical mericarps.
Radlkofer’s system of classification of 1890 placed
Paullinieae in the vicinity of the Thouinieae, a tribe that
included the genera Guindilia Gillies ex Hook. & Arn.,
Bridgesia Bertero ex Cambess., Athyana Radlk., Diatenopteryx
Radlk., Thouinia Poit., and Allophylus L. The Thouinieae was
characterized by an arboreal or shrubby habit and zygomor-
phic flowers in lateral cincinni (or a simplification of it).
Radlkofer’s concept of Paullinieae had survived through
much of the 20th century and was only modified by
Acevedo-Rodríguez (1993) who proposed placing Thinouia
in the Cupanieae near Allosanthus Radlk. More recently,
Thinouia was reinstated in the tribe Paullinieae following
recent molecular phylogenetic analyses (Acevedo-Rodríguez,
96
unpubl. data; Acevedo-Rodríguez et al. 2011). At the same
time, Allosanthus was treated as congeneric with Thinouia as
its only differentiating character, i.e. the spicate inflorescence,
was not considered worthy of generic recognition (Acevedo-
Rodríguez et al. 2011).
Cladistic analyses of the Paullinieae and Thouinieae, based on
morphological characters, indicated a monophyletic Paullinieae
nested within a paraphyletic Thouinieae (Acevedo-Rodríguez
1993). Analyses of eight DNA sequence regions from the plastid
and nuclear genomes by Buerki et al. (2009, 2010, 2011) recov-
ered a “Paullinia group” of genera assignable to the Paullinieae
and Thouinieae. Following the conclusions suggested in
Acevedo-Rodríguez (1993) and Buerki et al. (2009), Acevedo-
Rodríguez et al. (2011) placed the genera of Thouinieae in a
newly circumscribed Paullinieae, which encompassed 12 gen-
era. That classification made sense in light of the then sparse
molecular phylogenetic taxon-sampling, but now the results of
more comprehensive analyses call for a tribal reclassification.
Our study includes genera (Balsas and Allophylastrum) assign-
able to the Paullinieae that were published after the treatment
of Sapindaceae by Acevedo-Rodríguez et al. (2011) as well as
Sapindus oligophyllus Merr. & Chun, proposed by Buerki et al.
(2009, 2010, 2011) as a member of their Paullinia group. Balsas
was described to account for a species considered closely
related to Paullinia, but which is distinguished by its exarillate
seeds and hemi-tricolporate pollen grains. Allophylastrum,
which vegetatively closely resembles Allophylus, was described
due to its actinomorphic, apetalous, solitary (or on short
racemes) flowers, and 4–5-porate pollen grains. The position of
Sapindus oligophyllus as sister to Thouinia acuminata S. Watson
(Buerki et al. 2009) was clarified by analyzing sequence data
from its type collection. In addition, the validity of Chimborazoa,
already reduced to synonymy in Serjania (Acevedo-Rodríguez
1998), was further tested in our analyses.
The objectives of our study were to analyze molecular and
morphological evidence to: 1) evaluate the current circum-
scription of tribe Paullinieae (sensu Acevedo-Rodríguez et al.
2011), 2) test the monophyly of the genera currently included
in this tribe, and 3) elucidate the relationships among the
genera once considered to belong in the Paullinieae.
Materials and Methods
Sampling—We sampled all genera of tribe Paullinieae (here recog-
nized as supertribe Paulliniodae) sensu Acevedo-Rodríguez et al. (2011),
and where possible multiple species per genus (see Appendix 1). The
outgroups selected based on the family-wide phylogenies (i.e. Buerki
et al. 2009, 2011), included 16 genera of subfamily Sapindoideae, which
represent a successive series of nested sister clades to Paullinieae. The
plastid trnL intron and nuclear ribosomal internal transcribed spacer,
ITS, were selected as molecular phylogenetic markers because they have
proven useful in Sapindaceae (e.g. Buerki et al. 2009).
Molecular Methods—DNA extractions, amplifications, and Sanger
sequencing for the 184 newly generated sequences were conducted
largely according to standard methods as outlined here. Silica-gel dried
or herbarium leaf tissue (ca. 1.0 cm2) was pulverized with glass and steel
beads in a TissueLyser (Qiagen, Hilden, Germany). DNA extractions
from the resulting tissue powder were mostly performed with the
Qiagen DNeasy Plant Mini Kit according to the manufacturer’s protocol.
The herbarium extractions of Allophylastrum, Chimborazoa, and Sapindus
oligophyllus included an overnight incubation with proteinase K, and
each sample was not co-processed (i.e. from DNA extractions through
sequencing) with any other Sapindaceae. We believe the data for each of
these is authentic and not derived from contamination, based on the
extra care taken during the extractions, expected correlation of DNA
quality and amplification success, and the unique sequences obtained.
The trnL intron was amplified and sequenced using primers “c” and “d”
(Taberlet et al. 1991), and ITS was amplified using ITS5a (Stanford et al.
2000) and ITS4 (White et al. 1990). The amplification reactions were
conducted in a final volume of 25 μl with 2.5 μl of Bioline ammonium
reaction buffer (10×), 2.0 μl of dNTP mix (10 mM), 1.25 μl of magnesium
chloride (50 mM), 1.0 μl of each primer (10 nM), 0.5 μl of bovine serum
albumin (10 mg/ml), 14.05 μl of water, 0.2 μl of Biolase DNA polymerase
(5U/μl; Bioline USA, Taunton, Massachusetts) and 2.5 μl of DNA extrac-
tion (∼20 ng/μl). Amplification conditions were 95°C for 3 min, followed
by 35 cycles of 94°C for 40 sec, 55°C for 40 sec and 72°C for 1 min 40 sec,
with a 10 min final extension at 72°C. PCR products were treated with
ExoSAP-IT (Affymetrix-USB, Santa Clara, California) prior to sequencing.
Sequencing reactions were conducted using 8 μl of a cycle sequencing
reaction mixture (including 0.8 μl BigDye Terminator v3.1 [Applied Bio-
systems, Foster City, California], 1.0 μl of 1 μM primer, 2.0 μl of 5 × buffer,
4.2 μl water) combined with 4 μl of DNA template. The cycle sequencing
conditions were 30 cycles of 95°C for 30 sec, 50°C for 30 sec and 60°C for
4 min. The cycle sequencing products were purified using Sephadex G-50
(GE Healthcare Bio-Sciences, Pittsburgh, Pennsylvania) and run on an ABI
3730xl DNA Analyzer (Applied Biosystems) at the Smithsonian. The
resulting reads were assembled and edited using Sequencher ver. 5.2.4
(Gene Codes, Ann Arbor, Michigan).
Phylogenetic Analyses—We assembled and did preliminary analyses
on a complete data set that included our new data plus additional pub-
lished trnL and/or ITS sequences for Paulliniodae (i.e. from Buerki et al.
2009, 2011; Urdampilleta et al. 2013; Gildenhuys et al. 2015). In our final
data set we included some of this published data that complemented
our taxon sampling, did not cause unnecessary taxon redundancy, and
where we could confirm the identifications. The trnL alignment was
straightforward with most indels representing tandem repeats while that
of the ITS was complex with many ambiguous regions within ITS1 and
ITS2. Alignments were generated using MAFFT ver.7 (Katoh and Standley
2013) under the Q-INS-i refinement method (alternative MAFFT iterative
refinement methods did not greatly improve the alignment) and/or using
Clustal Omega (Sievers et al. 2011). For the trnL alignment we first
inferred the secondary structure of one outgroup with the ViennaRNA
package (Lorenz et al. 2011), which was then applied as a constraint to
improve the alignment using RNAsalsa (Stocsits et al. 2009). Our
concatenated datasets included a 125-tip sampling with some taxa having
missing data in one partition (i.e. incorporating published data such as
that for Cardiospermum), had manual refinement of the alignment using a
similarity criterion, and had a manual character deletion set made by
removing matrix columns with >50% missing data. This method elimi-
nated overlapping indels with clearly noisy characters and reduced miss-
ing data, but did not remove all ambiguously aligned regions. We also
created a 99-tip sampling that minimized missing data (i.e. by removing
most tips that were missing one of the partitions and which especially
impacted Cardiospermum), was not manually refined, and used Noisy
(Dress et al. 2008) as an automated approach to remove “noisy” sites.
To further assess the monophyly of Paullinieae — in particular the effect
of previously unsampled Lophostigma and Thinouia on the backbone of that
subclade — and to assess the suspected misidentification of Sapindus
oligophyllus in Buerki et al. (2011), we manually added our data (trnL and
ITS) for those taxa to their 8-marker family-wide data set archived in
TreeBASE (http://purl.org/phylo/treebase/phylows/study/TB2:S10580).
Two new gaps (insertions relative to rest of the data set) were added to
trnL and we manually refined the ITS partition to improve alignment con-
sistency within genera of Paulliniodae and within Harpullia Roxb.,
Lepisanthes Blume, and Llagunoa Ruiz & Pav. This combined taxon sam-
pling contained 247 tips, including five new taxa and deleting their chime-
ric Haplocoelum foliosum (Hiern.) Bullock (i.e. trnL, EU721250, clusters with
the “Dodonaea group” and is likely mislabeled). Our concatenated matri-
ces, along with supplemental figures are archived in the Dryad Digital
Repository: http://dx.doi.org/10.5061/dryad.p2g6p (Acevedo-Rodriguez
et al. 2017)
We determined nucleotide substitution models for four data partitions
(i.e. ITS1, ITS2, 5.8S, and trnL) in jModelTest ver. 2.1.2 (Darriba et al. 2012)
using the Akaike information criterion (AIC; Akaike 1974). For both indi-
vidual and concatenated matrix analyses we performed parsimony, maxi-
mum likelihood (ML), and Bayesian analyses. Parsimony analyses on the
99-tip data set were performed with TNT ver.1.5 (Goloboff et al. 2000) with
a two-stage search using 100,000 replicates of TBR followed by SPR, and
keeping the best 10 trees for each replicate (maximum of 100 million trees).
Parsimony non-parametric bootstrap (Felsenstein 1985) analyses included
1 million replicates, using the same approach as in the tree search. ML
analyses of the 99-tip data set were made with RAxML ver. 8.0.0
(Stamatakis 2014) on an unpartitioned matrix and 20 simultaneous runs,
each followed by bootstrap analysis with 100,000 replicates. ML analyses
2017] ACEVEDO-RODRÍGUEZ ET AL.: SUPERTRIBE PAULLINIODAE 97
of the 125-tip Paullinieae and 247-tip Sapindaceae data set were with
GARLI ver.2.1 (Zwickl 2006) on an unpartitioned matrix; GARLI-ML boot-
strap analysis included 500 replicates. Finally, Bayesian analyses under the
GTR + I + Γ model were performed on the 99-tip data set using MrBayes
(Ronquist and Huelsenbeck 2003) with four simultaneous runs, each with
four Markov chains (three cold and one heated) for a total of 16 simulta-
neous chains including 1,000,000 generations. Phylogenetic trees were
produced using Figtree ver. 1.4.0 (Rambaut 2015), Dendroscope ver. 3
(Huson and Scornavacca 2012), and/or Mesquite ver. 3.04 (Maddison
and Maddison 2015).
Morphology—Morphological characterization of the genera is based
on the treatment of the Sapindaceae by Acevedo-Rodríguez et al. (2011),
Ferrucci (1991), and further study of collections at the U.S. National Her-
barium (US). Pollen morphology applies Erdtman’s terminology (Erdtman
1966) and the studies of van der Ham (Acevedo-Rodríguez et al. 2011),
van der Ham and Tomlik (1994), and Ferrucci and Anzótegui (1993).
Chromosome data come from Ferrucci (2000a), de Freitas et al. (2007),
Urdampilleta et al. (2013), and the Index to Plant Chromosome Numbers
(1979–). We have adopted the terms ‘anterior’ and ‘posterior’, as opposed
to traditional terminology, to refer to specific floral parts as done by
Ferrucci and Somner (2010), and Ferrucci and Urdampilleta (2011a,
2011b). Anterior is the side where the third and fifth sepals are located;
and posterior is the side on which the fourth sepal is found (Fig. 1C).
Other floral parts are described according to their relative position
between these two points of reference.
Results
Phylogenetic Analyses—Data set statistics are summarized
in Table 1 and results of our primary combined 99-tip analy-
ses are shown in Fig. 2, with additional analyses in Suppl.
Figures 1–3. Separate analyses of each locus did not reveal
any strongly supported groupings that would indicate incon-
gruence, although resolution in trnL was poor due to the low
number of informative characters. Based on this broad con-
gruence, we combined the loci for the total evidence approach
on which we base our discussion. The 99- and 125-tip analy-
ses had different approaches to data set polishing (automated
vs. manual) and software (RAxML vs. GARLI). Both topolo-
gies are highly congruent but the 99-tip sampling is better
resolved at deeper nodes and serves as the point of reference
for our discussion. The long branches we observed (Suppl.
Figure 2) in Cardiospermum integerrimum Radlk. suggest a
need for caution regarding the placement of that taxon,
although its inclusion or exclusion did not greatly change
the topology, or bootstrap values in neighboring subclades.
Inspection of the ITS matrix indicated a substitution bias that
resulted in a GC content reduction to 45% in Cardiospermum
integerrimum from an average across the rest of the data of
61% (range 58–65%). Data consistency between our sequence
and that of Urdampilleta et al. (2013) contraindicates a lab-
specific artifact. Our combined 99-tip DNA analyses show
strong support (Bayesian posterior probability (PP) = 1; ML
bootstrap percentage (MLBP) = 96) for a clade containing
most taxa placed by Acevedo-Rodríguez et al. (2011) in the
Paullinieae. This clade, here called supertribe Paulliniodae,
contains four supported monophyletic groups, which are
here classified as tribes Athyaneae, Bridgesieae, Thouinieae
and Paullinieae. Tribe Athyaneae containing Athyana and
Diatenopteryx is strongly supported (PP = 1; MLBP = 100) as
basal within Paulliniodae. Tribe Bridgesieae with a single spe-
cies (Bridgesia incisifolia Cambess.) is sister to the Thouinieae +
Paullinieae (PP = 1; MLBP = 98). Tribe Thouinieae is strongly
supported (PP = 1; MLBP = 100) as a clade including Thouinia
as sister to Allophylus plus Allophylastrum. Allophylastrum is
weakly embedded in a paraphyletic Allophylus (PP < 60;
MLBP < 50) and requires additional data to be resolved. Tribe
Paullinieae has strong support (PP = 1; MLBP = 94) and a
basal clade formed by Thinouia, successively followed by
Lophostigma and then a poorly resolved crown group of three
subclades containing Serjania, Paullinia, Urvillea, Cardiospermum,
Balsas, and Houssayanthus. Although Serjania is poorly resolved,
it is clearly paraphyletic because of deeply embedded Balsas,
Chimborazoa and Houssayanthus. Cardiospermum as currently
Fig. 1. Flowers in Paullinieae. A. zygomorphic flower (Paullinia stellata Radlk.; Acevedo-Rodríguez 14964 (US), photo by P. Acevedo). B. actinomorphic
flower (Thinouia mucronata Radlk.; photo by S. Maris Solís). C. Diagram of flower bud cross section of Serjania salzmanniana Schltdl. showing floral
orientation (72°) in relation to inflorescence axis (e) and bracteole (b); numbers mark the different sepals (modified from Radlkofer 1931–1934).
Table 1. Data set characteristics for 99 and 125-tip phylogenetic analyses.
Characteristic ITS trnL Combined total evidence
No. terminals 122/123 101/112 99/125
Aligned length, nt 680/925 441/716 1121/1641
Characters analyzed, nt 512/636 441/507 953/1143
% missing 4.0/5.2 11.2/2.6 6.9/9.4
Constant characters, nt 300/202 329/371 513/573
Variable characters, nt 380/434 112/136 440/570
Informative characters, nt 319/383 91/82 354/465
98 SYSTEMATIC BOTANY [Volume 42
Fig. 2. Bayesian 50% majority-rule consensus tree based on the combined two marker, 99-tip data set for Paulliniodae and outgroups. Bayesian
posterior probability values ≥0.50 are indicated above branches, followed by RAxML bootstrap values ≥50%. (−) = value < 0.50/50%. np = an edge
recovered in the Bayesian tree but not present with ML.
2017] ACEVEDO-RODRÍGUEZ ET AL.: SUPERTRIBE PAULLINIODAE 99
circumscribed (Ferrucci 2000b) is polyphyletic, with species
grouping with Serjania, Paullinia, and Urvillea. The core
Cardiospermum s. s. subclade (containing the type species
C. halicacabum; sampled in the 125-tip analysis; Suppl.
Figure 1) is sister to Paullinia (PP = 1; MLBP = 70). Guindilia
is among the outgroup taxa, and although support is not
strong in the 99-tip analyses as to an exact placement, it is
clearly excluded from Paulliniodae.
Our analyses of the 247-tip family-wide data set show
(Suppl. Figure 3) broad topological similarity among the
sampled Paulliniodae to our focused 2-gene results, with
two notable exceptions: (1) Bridgesia is sister to Thouinieae
(MLBP = 93) rather than sister to Thouinieae + Paullinieae,
and (2) Guindilia is sister to the rest of Paulliniodae (MLBP =
87) rather than farther out. Sapindus oligophyllus clearly groups
(MLBP = 100) with Lepisanthes, an affiliation proposed by Xia
and Gadek (2007) who transferred S. oligophyllus to Lepisanthes.
Therefore, the anomalous position of this taxon within the
Paullinia group by Buerki et al. (2009, 2010, 2013) is due to
the misidentification of their sample, which is likely a spe-
cies of Allophylus.
Discussion
Characterization of the Paulliniodae and Nested Tribes—
Our best estimate (Fig. 2) of phylogenetic relationships of
Paullinieae and its close relatives is incompletely resolved
but makes considerable progress in a group that has been
poorly sampled in prior phylogenetic studies. The examina-
tion of chromosome numbers, and important reproductive
and vegetative characters (i.e. potential morphological syn-
apomorphies) in the context of our trees reveals patterns
of character state change that deserve closer examination
(Fig. 3; Table 2). Supertribe Paulliniodae is characterized by
the following morphological synapomorphies: leaves with a
fully developed distal leaflet, thyrses with lateral cincinni,
zygomorphic flowers with 4–5 sepals, 4 petals, unilateral
Fig. 3. Hypothetical relationships of genera in supertribe Paulliniodae, backbone based on DNA sequence and chromosome analyses; relationships
within tribe Paullinieae based on morphological characters. Refer to Table 2 for synapomorphies.
100 SYSTEMATIC BOTANY [Volume 42
nectary discs, schizocarpic fruits with divaricate mericarps,
and reduced chromosome numbers (2n ≤ 30).
Tribe Athyaneae, although distinct based on molecular
data, is difficult to define with synapomorphic morphological
characters. However, the tribe can be recognized by pinnately
compound leaves in addition to the features that characterize
the Paulliniodae. Athyana and Diatenopteryx can be distin-
guished by a combination of a 3-carpellate gynoecium and an
indumentum lacking glandular hairs in Athyana, and the
2-carpellate gynoecium and indumentum with glandular hairs
in Diatenopteryx. These two genera are currently restricted to
southern South America, but according to the fossil pollen
record, Athyana once was present in North America during
the Oligocene (MacGinitie 1953).
Tribe Bridgesieae is strongly supported by molecular data
and is recognized by its simple, exstipulate leaves in addition
to the same floral characters as in Paulliniodae and by short,
axillary cymes (a single, few-flowered cincinnus) or flowers
solitary. Simple leaves and reduced cincinni are considered
morphological synapomorphies for the Bridgesieae. Monospe-
cific Bridgesia is currently restricted to the Andean region of
Chile; however, fossil pollen records indicate its presence in
North America during the Eocene (Graham 2011).
Tribe Thouinieae is characterized by trifoliolate (or trifoliolate-
derived) leaves, zygomorphic flowers, thyrses with lateral
cincinni and by the oblate to subglobose, porate pollen grains
(Fig. 4A–B). Thouinia, which is sister to Allophylus and
Allophylastrum, does not seem to have any morphological
apomorphies, but can be differentiated from the latter two
genera by its schizocarpic fruit with 3 distally winged
mericarps (Fig. 5G). The subclade containing Allophylastrum
and Allophylus is defined by fruits with coccate monocarps
(Fig. 5H–I). Although Allophylastrum is easily distinguished by
unique morphological features (see treatment below), its phy-
logenetic position is poorly resolved with respect to Allophylus
with individual trees indicating it as either sister to, or alterna-
tively embedded within, Allophylus. While our sampling of
Allophylus is broad, sequence variation is low and additional
loci are needed to resolve this point. Except for Allophylus, the
genera of Thouinieae are restricted to the New World. Thouinia
is currently known from the Greater Antilles (except Jamaica),
Mexico and northern Central America but it has been docu-
mented in pollen samples from the Eocene to the Oligocene
of North America (Muller 1981; Graham 2011). Accordingly,
Thouinieae evolved in the New World, as the Neotropical
genus Thouinia is the first diverging lineage of this clade and
possibly shared a common ancestor with Allophylus and
Allophylastrum. Hence, Allophylus evolved in the New World
and later dispersed to Africa, Madagascar, and Asia. Poorly
known Allophylastrum is restricted to northern South America,
while Allophylus has a pantropical distribution. Allophylus has
been documented as early as the middle Eocene from fossil pol-
len from the Gatuncillo Formation in Panama (Graham 1987).
Tribe Paullinieae is essentially Neotropical and the most
species diverse of the four tribes. It is characterized by the
presence of a climbing habit, stipules, and tendrils that seem
to be homologous to the lower cincinni of the inflorescence
(Darwin 1897). Floral symmetry for the most part is zygo-
morphic (Fig. 1A) with the exception of Thinouia, which has
actinomorphic flowers (Fig. 1B). Actinomorphic flowers are
plesiomorphic within the Paulliniodae and their occurrence
in the Paullinieae can be best explained as a likely reversal.
Thinouia is the first diverging lineage of this clade and
although it does not have any morphological apomorphies,
it is recognizable (in addition to the characters that define
the Paulliniodae) by the presence of actinomorphic flowers,
isopolar tricolporate pollen grains, and mericarps with distal
wings (Figs. 1B, 5A, 6F). The next inclusive clade is formed
by Lophostigma in a sister position to a clade containing
Serjania, Paullinia, Urvillea, and Cardiospermum. The presence
of heteropolar hemi-tri-syncolporate pollen grains (or its
transformation) is considered synapomorphic in this clade
(Fig. 6B–E). Lophostigma stands alone by the presence of pro-
late heteropolar 4-aperturate pollen grains and petals shorter
than the sepals (Fig. 6E). The most inclusive clade is defined
as a polytomy uniting Serjania, Paullinia, Urvillea, and
Cardiospermum. This clade is characterized by the presence
of petals that are as long as, or longer than, the sepals, and
by oblate pollen grains (Figs. 1A, 6B–D).
The greater species richness of Paullinieae has been hypothe-
sized to be the result of the ecological specializations in its
innovative climbing habit and development of zygomorphic
flowers (Buerki et al. 2013). This suggestion however, does
not explain finer differences in species richness, where
Cardiospermum, Lophostigma, and Urvillea have far fewer spe-
cies than Paullinia and Serjania. Flower zygomorphism has
evolved in all four subfamilies of Sapindaceae presumably
from ancestors with actinomorphic flowers. Although most
large genera in Sapindaceae have zygomorphic flowers, this
character alone cannot explain differences in species richness.
For example, Acer L. with about 125 species and Dodonaea
Miller with about 68 species have actinomorphic flowers. In
addition, from a total of 61 genera of Sapindaceae with zygo-
morphic flowers, only five have more than 30 species and
24 contain a single species. Thus, the poor correlation of habit
and floral symmetry with species richness in the Sapindaceae
does not seem to explain taxonomic richness in the Paullinieae.
Novel seed dispersal mechanisms in Paullinieae could
have played an important role in the evolution, specialization,
and diversification of Paullinia and also perhaps of Serjania.
Paullinia is largely a forest dweller while Serjania favors
open savannah-like formations. The presence of bird- and
Table 2. Morphological characters (synapomorphies) for clades in
supertribe Paulliniodae. Numbers correspond to synapomorphies shown
in Fig. 3.
1. Leaves with a fully developed distal leaflet; thyrses with lateral cincinni;
zygomorphic flowers with 4–5 sepals; 4 petals; unilateral nectary disc;
schizocarpic fruits with divaricate mericarps; seeds not arillate;
chromosome number 2n ≤ 30.
2. Leaves trifoliolate or trifoliolate derived; seeds basal; chromosome
number 2n ≤ 28.
3. Climbers with stipules and tendrils.
4. Pollen heteropolar.
5. Pollen oblate (compressed in polar area) with triangular outline; petals
as long as or longer than the sepals; chromosome number 2n ≤ 24.
6. Seeds in center of axis, with pseudo-hilum; fruit capsular.
7. Pollen hemi-isopolar, triporate; capsules coriaceous to woody; seeds
arillate or sarcotestal.
8. Imparipinnate leaves.
9. Leaves simple; cincinni reduced.
10. Subglobose to oblate porate pollen grains; chromosome number
2n ≤ 28.
11. Fruits with coccate monocarps; seeds covered by fleshy endocarp.
12. Actinomorphic flowers, a reversal.
13. Pollen prolate heteropolar, 4-aperturate; petals shorter than the sepals.
14. Mericarps mostly proximally winged.
15. Capsule membranous; chromosome number mostly 2n < 24.
2017] ACEVEDO-RODRÍGUEZ ET AL.: SUPERTRIBE PAULLINIODAE 101
Fig. 4. Pollen grains in super-tribe Paullinoidae. A. Thouinia striata Radlk. (Acevedo-Rodríguez 7869, US). B. Allophylastrum frutescens Acev.-Rodr.
(Schomburgk 336, W). C. Diatenopteryx sorbifolia Radlk. (Hassler 10644, US). D. Athyana weinmannifolia (Griseb.) Radlk. E. Bridgesia incisifolia Camb.
(Landrum 9824, ASU). F. Guindilia trinervis Hook & Arn. ( Joseph 4048, US).
102 SYSTEMATIC BOTANY [Volume 42
Fig. 5. Fruits in Paullinieae and Thouinieae. A. Thinouia scandens (Acevedo-Rodríguez 3697, US). B. Serjania trachygona Radlk. (Acevedo-Rodríguez
15222, US). C. Lophostima plumosum Radlk. (Acevedo-Rodríguez 6568, US). D. Urvillea triphylla Radlk. (Acevedo-Rodríguez 3711, US). E. Cardiospermum
corindum L. (Acevedo-Rodríguez 1349, US). F. Paullinia ingifolia Juss. (Acevedo-Rodríguez 13549, NY). G. Thouinia striata Radlk.; H. Allophylus sp. (Acevedo-
Rodríguez 3726, US). I. Allophylastrum frutescens Acev-Rodr. Photo credits: A–H, P. Acevedo; I, R. Perdiz.
2017] ACEVEDO-RODRÍGUEZ ET AL.: SUPERTRIBE PAULLINIODAE 103
Fig. 6. Pollen grains in super-tribe Paullinoidae. A. Allophylus sericeus (Camb.) Radlk. (Mexia 5202, US). B. Cardiospermum bahianum Ferrucci
(Harley et al. 5266, CTES). C. Paullinia carpopoda Camb. (Irwin et al. 29394, US). D. Serjania squarrosa Radlk. (Cook & Gilbert 389, US). E. Lophostigma
schunkei (Acev.-Rodr.) Acev.-Rodr. (Cerón & Cerón 4544, US); Thinouia myriantha Triana & Planch. (Tun Ortíz 2403, US).
104 SYSTEMATIC BOTANY [Volume 42
water-dispersed seeds in Paullinia seems to be an adaptation
for dispersal throughout the extensive Amazon biome, allowing
Paullinia to reach new micro-niches and eventually to diversify
into distinct species (Figs. 7A–D, 8A–B). Species richness in
Serjania, however, cannot be explained solely by its wind-
dispersed mericarps, as this feature also occurs in the much less
diverse lianoid genera Thinouia and Lophostigma (Fig. 5A, C).
Serjania may have capitalized on this dispersal mechanism
by becoming a dry habitat specialist in more open environ-
ments (Acevedo-Rodríguez 1990), while Thinouia is mostly
found in moister habitats where wind-dispersed species are
less abundant (Mori and Brown 1994), and Lophostigma is
restricted to high elevations. The poor species diversity
observed in Cardiospermum and Urvillea may be due to the
lack of effective dispersal mechanisms which otherwise would
allow these genera to reach and radiate into novel habitats. In
both genera, the seeds remain attached to the septa of the
dehisced capsules and are only liberated by gravity after the
decay of the septa (Fig. 8C). The suggestion that capsules of
Cardiospermum may be water- or wind-dispersed (Harden
2002) is highly unlikely, as it has not been documented and
because the capsule dehisces long before the fruit abscises
from the inflorescence.
Chromosome Number—Recent studies on chromosome struc-
ture, size, and number provide additional insights into the
evolution of the Paulliniodae (Ferrucci 2000a; Urdampilleta
et al. 2013; Index to Plant Chromosome Numbers 1979–). When
chromosome number is examined in the context of our trees, a
pattern emerges of reduction from 2n = 32 (Talisia Aubl. and
Matayba Aubl.) to 2n ≤ 30 in Paulliniodae (Fig. 3), with occa-
sional reports of polyploidy. This trend is evident in the
Athyaneae (Diatenopteryx) where 2n = 30 and in the closely
related Thouinieae (Allophylus) and the basal taxa of
Paullinieae (Thinouia and Lophostigma) where the number
is further reduced to 2n = 28. The most derived clade
(Cardiospermum, Paullinia, Serjania, and Urvillea) is character-
ized by 2n ≤ 24, with even further reduction to 2n ≤ 22 in
Cardiospermum and Urvillea.
Exclusion of Guindilia from Paulliniodae—Guindilia, which
heretofore has been considered a member of the Paullinieae
(Thouinieae sensu Radlkofer 1931-1934), is placed in our
99-tip phylogeny among the outgroup taxa, and clearly out-
side of the strongly supported Paulliniodae. While this
suggests that it does not belong in the supertribe, its exact
position within the tree may be an artifact of our limited
outgroup sampling. A richer phylogenetic context still
excludes Guindilia from Paulliniodae with placement as
either sister to the supertribe (i.e. our 247-tip results in
Suppl. Figure 3; also Buerki et al. 2011) or a placement fur-
ther out and roughly similar to our 99-tip results (i.e. diver-
gence dating in Buerki et al. 2013). Our data from a new
accession of Guindilia agrees with that of Buerki et al. (2011).
Morphologically, this genus differs from other Paulliniodae
by the presence of opposite, simple leaves. Although the disc
in Guindilia flowers is unilateral, it is roughly pyramidal-
shaped and two-lobed, a feature that is not present in the
Paulliniodae. We defer to assign Guindilia to any group until
its phylogenetic position is better resolved.
Origin of the Paulliniodae and Nested Tribes—Our analy-
ses do not suggest a clear affinity of the Paulliniodae with
any of the outgroup taxa. However, based on pollen morphol-
ogy, van der Ham and Tomlik (1994) suggested the parallel
evolution of Paullinieae and Thouinieae from a Cupania-like
ancestor. This hypothesis posits that the hemi-syncolporate
pollen found in Serjania, Cardiospermum, and Urvillea is nec-
essarily derived from a syncolporate or parasyncolporate
pollen type that is found in the Cupanieae. Support for this
claim is found in the sporadic presence of distal vestigial
colpi in the pollen of these three genera, and fine traces of a
parasyncolporate condition in Athyana (van der Ham and
Tomlik 1994; Acevedo-Rodríguez 2011). From the floral mor-
phology point of view, this hypothesis is plausible as some
Cupanieae (e.g. species of Guioa Cav.) have zygomorphic
flowers with unilateral nectary discs similar to those in the
Paulliniodae. The alternative hypotheses of derivation from
an ancestral group with colporate pollen such as Sapindus L.
(Acevedo-Rodríguez 1993) or Thinouia-like (Ferrucci and
Anzótegui 1993) would have to account for the unlikely
transformation of tricolporate into the hemi-tri-syncolporate
pollen present in Serjania and allied genera.
Buerki et al. (2013) offered a hypothesis for the origin of
the Paulliniodae (their “Paullinia group”) as a result of a
migration event of ancestral Sapindaceae from Australia via
Antarctica during the Middle Eocene. Although this hypoth-
esis and the proposed timing of events is not supported by
the available fossil record, it is possible that such a migratory
route existed much earlier as suggested by the wide occur-
rence of Cupaniopsis pollen (Cupanieae) during the middle
Cretaceous in Antarctica, Africa (Gabon), South America
(Brazil), and North America (Coetzee and Muller 1984; Muller
1981). Although no specific ancestor is mentioned by Buerki
et al. (2013), their consensus tree has Blomia Miranda and the
Melicocceae closer to the Paulliniodae than to the Cupanieae.
Blomia and the Melicocceae have colporate pollen grains and
could share a common ancestor with the Paulliniodae.
The constraints of the van der Ham and Tomlik (1994)
hypothesis do not preclude a common ancestor with isopolar
colporate pollen like those of Talisia, and Melicoccus P. Browne
although it would require the additional evolutionary step of
becoming syncolporate. Our analyses do not provide support
for either scenario but it would be an interesting hypothesis
to test by expanding the molecular sampling coupled with
examining the pollen of Blomia and the Melicocceae for vesti-
gial Cupanieae-like pollen characters. From a palynological
point of view, Paullinia could have been derived from a com-
mon ancestor with Cardiospermum, Serjania, and Urvillea. Its
isopolar, triporate pollen (Fig. 5C) is seen as derived from the
type found in Serjania. The presence of subisopolar pollen
grains in a few species of Paullinia is seen as a vestigial char-
acter that adds weight to this argument. In addition, the
presence of capsular fruits with thick walls and seeds with-
out sarcotesta in Balsas (herein considered a Serjania) is inter-
preted as a step in the derivation of the capsules in Paullinia
from an ancestor with schizocarpic, thin-walled fruits and
non-sarcotestal seeds.
The persistence of plesiomorphic characters such as the
trigonous-subglobose, tricolporate, striate pollen grains
(Athyaneae, Bridgesieae, Allophylus, Thinouia, and Lophostigma)
and actinomorphic flowers (Allophylastrum and Thinouia) are
indicative of mosaic-like character evolution in the Paulliniodae.
In addition, the occurrence of transitional plesiomorphic char-
acters such as the sub-zygomorphic flowers in Lophostigma
and some species of Allophylus provide further evidence for
mosaic evolution and provide possible links between genera.
For example, striate pollen and sub-zygomorphic flowers in
Lophostigma are seen as intermediate between Thinouia and
2017] ACEVEDO-RODRÍGUEZ ET AL.: SUPERTRIBE PAULLINIODAE 105
Fig. 7. Fruits in Paullinia. A. P. hyxtrix Radlk. (Acevedo-Rodríguez et al. 14408, US). B. P. obovata (Ruiz & Pav.) Pers. (Acevedo-Rodríguez et al. 14441, US).
C. P. verrucosa Radlk. (Acevedo-Rodríguez et al. 14584, US). D. P. caloptera Radlk. (Acevedo-Rodríguez et al. 14315, US).
106 SYSTEMATIC BOTANY [Volume 42
the remaining genera (Serjania, Cardiospermum, Urvillea, and
Paullinia) of Paullinieae. The presence of sub-actinomorphic
flowers within Allophylus suggests an incipient reversal (from
zygomorphic to actinomorphic flowers) and provides a con-
nection with Allophylastrum where actinomorphic flowers are
found. This notion also supports the interpretation of actino-
morphic flowers in Thinouia as a reversal. Instances of interme-
diate or incipient characters are also found in Serjania where a
few species show features (pseudo-hilum, and capsules) that
are characteristic of Cardiospermum, Urvillea, and Paullinia.
While our resolution of major subclades within supertribe
Paulliniodae is incomplete, an examination of morphological
characters with reference to the persistence of plesiomorphic
and intermediate morphological characters, suggests links
among genera and testable hypotheses of evolutionary trends.
Pollen fossils identified asAllophylus, Bridgesia,Cardiospermum,
Paullinia, Serjania, and Thouinia indicate the wide establishment
of supertribe Paulliniodae in the Americas by the late Eocene
(Gray 1960; Muller 1981; Graham 1987, 2011). Moreover, the
fact that Allophylus fossils have only been found in the Old
World in recent geological times further supports the hypothe-
sis that Allophylus evolved in the Americas and later dispersed
to Africa and other regions of the Old World.
A New Classification—The recognition of Supertribe
Paulliniodae allows for the retention of tribes that are recog-
nizable from a suite of morphological characters. Tribe
Athyaneae, although similar to the Thouinieae, contains trees
with exstipulate, pinnately compound leaves with fully devel-
oped distal leaflets. Tribe Bridgesieae contains shrubs with
simple, exstipulate leaves, and short, axillary cymes (a single
few-flowered cincinni) or solitary flowers. Tribe Thouinieae
deviates from previous classifications by excluding Athyana,
Bridgesia, Diatenopteryx, and Guindillia and contains trees or
shrubs with trifoliolate or unifoliolate, exstipulate leaves, and
zygomorphic flowers. Finally, tribe Paullinieae agrees with
previous classifications (de Candolle 1824; Radlkofer 1890),
and contains climbers or climber-derived shrubs with stipu-
late leaves, and tendrils. We have made limited taxonomic
Fig. 8. Fruits and seeds in Paullinieae. A. Seed with removed arillode showing pseudo-hilum, Paullinia verrucosa Radlk. (Acevedo-Rodríguez 14584, US).
B. Dehisced capsule, Paullinia fibrigera Radlk. (Acevedo-Rodríguez 15233, US). C. Dehisced capsule, Cardiospermum corindum L. (Acevedo-Rodríguez 4568, US).
D. Seed with pseudo-hilum, Cardiospermum corindum L., (Acevedo-Rodríguez 4568, US).
2017] ACEVEDO-RODRÍGUEZ ET AL.: SUPERTRIBE PAULLINIODAE 107
changes toward the goal of recognizing only monophyletic
genera, although problems still remain with regard to
Allophylastrum and Cardiospermum (i.e. Cardiospermum
integerrimum, C. urvilleoides). Not all of these changes are
based on direct molecular phylogenetic placement, but rather
some are inferred based on close morphological similarity to
our sampled taxa.
Taxonomic Treatment
Supertribe Paulliniodae—Lianas, vines, trees shrubs, or
hemicryptophytes. Leaves alternate, with a fully developed dis-
tal leaflet; thyrses with lateral cincinni; flowers zygomorphic,
with 4–5 sepals, 4 petals, unilateral nectary disc (or exceptionally
actinomorphic), and schizocarpic (or schizocarpic derived) fruits.
Key to the Tribes
1. Lianas, climbing shrubs, or less often erect or hemicryptophytic shrubs; stipules minute to foliaceous;
tendrils paired at base of inflorescence rachis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Paullinieae
1. Trees or erect shrubs; stipules and tendrils wanting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Leaves pinnately compound . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Athyaneae
2. Leaves trifoliolate, unifoliolate or simple . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3. Leaves trifoliolate or unifoliolate (pulvinulate at the base of blade); fruits bicoccate or schizocarpic
with non-bladder-like mericarps, apically elongated into a long (distal) wing; pollen porate . . . . . . . . . . . . . . . . . . . . . . . . . . . Thouinieae
3. Leaves simple; fruit schizocarpic, with bladder-like mericarps, transversely elongated
into a short (dorsal) wing; pollen tricolporate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Bridgesieae
Tribe Athyaneae Acev.-Rodr., tribus nova—TYPE: Athyana
Exstipulate, small trees, leaves alternate imparipinnate with
fully developed distal leaflet; flowers zygomorphic; pollen
isopolar, obtusely triangular in polar view, subspherical
in equatorial view, tricolporate, with colpi nearly reaching
the poles.
Small trees; exstipulate. Leaves alternate, imparipinnate,
distal leaflet fully developed or exceptionally rudimentary.
Inflorescences of thyrses with flowers in lateral cincinni; ped-
icel articulate (abscission zone) below the middle. Flowers
zygomorphic, structurally or functionally unisexual; calyx 4–
5-merous, sepals valvate or imbricate; corolla of 4 distinct
petals, each with an adaxial, basal, hood-shaped appendage;
disc semiannular; stamens (6–)8, filaments usually of differ-
ent lengths, anther dorsifixed; gynoecium 2- or 3-carpellate
with a single ovule per carpel.
Distribution—Two genera distributed in southern
South America.
Key to the Genera
1. Gynoecium 3-carpellate; leaf rachis winged . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Athyana
1. Gynoecium 2-carpellate; leaf rachis unwinged . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Diatenopteryx
Athyana (Griseb.) Radlk. in T. Durand, Index Gen. Phan.
73. 1887 [“1888”].—TYPE: Athyana weinmanniifolia
(Griseb.) Radlk.
Duodichogamous trees; exstipulate. Leaves imparipinnate;
leaflets (5)7–15, serrate; distal leaflet fully developed; rachis
winged. Inflorescences axillary or pseudoterminal, simple or
double thyrses; flowers on lateral, reduced cincinni (seemingly
a depauperate dichasium); pedicels articulate. Flowers zygo-
morphic; calyx actinomorphic, sepals 5, valvate, of similar
size, with the 2 anterior sepals connate at base; petals 4, as
long as the sepals, with a single basal, hood-shaped, crested
appendage; disc semiannular, lobed; stamens (7)8, filaments of
unequal lengths, anthers dorsifixed; pollen isopolar, obtusely
triangular in polar view, subspherical in equatorial view,
tricolporate, with colpi nearly reaching the poles (Fig. 4D),
finely perforate (also faintly parasyncolporate fide van der
Ham and Tomlik 1994); ovary 3-carpellate; stigma capitate.
Fruit schizocarpic, splitting into 3 samaroid mericarps with a
dorsal-distal, ascending wing; seed exarillate. A single species
found in Peru, Bolivia, Paraguay, and Argentina.
Diatenopteryx Radlk., Sitzungsber. Math.-Phys. Cl. Königl.
Bayer. Akad. Wiss. Münch. 8: 284. 1878.—TYPE:
Diatenopteryx sorbifolia Radlk.
Duodichogamous small to large trees; exstipulate. Indumentum
of simple hairs. Leaves imparipinnate or paripinnate; leaflets
dentate or serrate; distal leaflet fully developed; rachis
unwinged. Inflorescences terminal or axillary thyrses, with
flowers in lateral cincinni; pedicel articulate. Flowers zygo-
morphic, functionally unisexual; sepals 4, free, imbricate, the
anterior sepal larger; petals 4, up to four times as long as the
sepals, each with a basal hood-shaped, crested appendage;
disc semiannular, crenate; stamens (6–)8, of unequal length,
anthers dorsifixed; pollen isopolar, obtusely triangular in
polar view, subspherical in equatorial view, tricolporate, with
elongated colpi nearly reaching the poles, rugulate (Fig. 4C);
ovary 2-carpellate, v-shaped; style filiform; stigma bifid.
Fruits schizocarpic, splitting into 2 samaroid divaricate,
mericarps with a long dorsal wing; seed exarillate. Two spe-
cies from Brazil, Bolivia, Paraguay, and Argentina. 2n = 30.
Tribe Bridgesieae Acev.-Rodr., tribus nova—TYPE: Bridgesia
Exstipulate, shrubs; leaves alternate simple; flowers zygo-
morphic; pollen isopolar, subspherical in polar and equato-
rial views, tricolporate.
Characters as in Bridgesia.
Distribution—A single, monospecific genus distributed in
Chile, South America.
Bridgesia Bertero ex Cambess., Nouv. Ann. Mus. Hist. Nat.
3: 234. 1834, nom. cons., non Hook., 1831.—TYPE:
Bridgesia incisifolia Cambess.
Duodichogamous shrubs; exstipulate. Leaves simple, deeply
trilobed or serrate. Inflorescence a short, axillary cyme (a
single few-flowered cincinni) or flowers solitary; pedicels
articulate. Flowers zygomorphic; sepals 5, imbricate, lanceo-
late, nearly equal, the 2 anterior sepals partly connate; petals
108 SYSTEMATIC BOTANY [Volume 42
4, pink, with a single basal, hood-shaped crested appendage;
disc semiannular, 4-lobed; gynophore with 4 tiny lobes;
stamens 8, filaments of unequal lengths, anthers dorsifixed;
pollen isopolar, spherical in polar and equatorial view,
tricolporate, striate (Fig. 4E); ovary 3-carpellate; style filiform
with 3 stigmatic branches. Fruit schizocarpic, splitting into
3 samaroid, bladder-like, papery, divaricate mericarps with a
short dorsal wing; seed exarillate, black, with a large hilum.
A single species from Andean Chile.
Tribe Thouinieae Blume, Rumphia 3: 186. 1847.
Small trees or shrubs; exstipulate. Leaves alternate, trifo-
liolate or unifoliolate. Inflorescences of thyrses with flowers
in lateral cincinni, or less often solitary or in short racemes;
pedicel articulate (abscission zone) below the middle or
non-articulate (in Allophylastrum). Flowers zygomorphic
or less often actinomorphic, structurally or functionally
unisexual; calyx 4(5)-merous, sepals with quincuncial
imbrication; corolla of 4 distinct petals (or missing in
Allophylastrum), usually with an adaxial or marginal petal-
oid appendage; disc semiannular, 2–4 lobed, or less often
annular; stamens (6)8, filament usually of different lengths,
anther dorsifixed; gynoecium (2)3-carpellate with a single
ovule per carpel.
Distribution—All genera Neotropical, except for Allophylus
that is primarily Paleotropical.
Key to the Genera
1. Fruit schizocarpic, of 3 distally-winged mericarps . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Thouinia
1. Fruits unicoccate, bicoccate or seldom tricoccate
2. Flowers zygomorphic, petaliferous, on lateral cincinni in racemiform or paniculate thyrses; nectary disc unilateral,
semiannular, 2- to 4-lobed, or rarely annular; pedicels articulate, 1–2 times as long as the calyx; pollen 3(4)-porate,
triangular (seldom quadrangular) in polar view . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Allophylus
2. Flowers actinomorphic, apetalous, solitary, or in short axillary racemes; nectary disc cupular; pedicels non-articulate,
>4 times as long as the calyx; pollen 4- or 5-porate, 4- or 5-angled in polar view . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Allophylastrum
Thouinia Poit., Ann. Mus. Natl. Hist. Nat. 3: 70. 1804, nom.
cons., non L. f., 1782.—TYPE: Thouinia simplicifolia Poit.
Duodichogamous shrubs or small trees; exstipulate. Leaves
trifoliolate or unifoliolate. Inflorescences axillary, racemiform
thyrses with flowers in reduced lateral cincinni; pedicels artic-
ulate. Flowers zygomorphic; sepals 4, imbricate, the outer two
usually smaller; petals 4, with an adnate, ventral, 2-lobed
appendage; disc unilateral, 4-lobed; stamens 8, filaments of
equal length; pollen isopolar, obtusely triangular, quadrangu-
lar, pentagonal, or hexagonal in polar view, oblate in equatorial
view, 3–6-porate, rugulate; ovary 3-carpellate, with a single
ovule per carpel; style filiform, with 3 stigmatic branches. Fruit
schizocarpic, splitting into 3 samaroid mericarps, each bearing
a dorsal ascending wing; seeds exarillate. About 30 species
from the Greater Antilles (excluding Jamaica), Bahamas,
Mexico, and northern Central America.
Allophylus L., Sp. Pl. 348. 1753. —TYPE: Allophylus
zeylanicus L. [= Allophylus cobbe (L.) Raeusch.]
Duodichogamous, rarely dioecious, erect shrubs, trees, or
rarely scandent shrubs (in Malaysia); exstipulate. Leaves
alternate, trifoliolate or less often unifoliolate or digitately
5-foliolate (few Asian species); leaflets serrate, dentate or
entire; petioles elongated. Inflorescences axillary, racemiform
or paniculate thyrses, flowers on lateral cincinni; pedicels
articulate. Flowers zygomorphic; sepals 4(5), free, imbricate,
the outer distinctly smaller than the inner ones; petals 4, with
a single, adnate, 2-lobed, or a basal hood-shaped, non-crested
appendage, or these represented by an elongation of petal’s
margins, exceptionally wanting; disc unilateral, semiannular
or divided into 2 or 4 lobes, or exceptionally annular; stamens 8,
filaments of unequal lengths, with posterior three shorter,
anthers dorsifixed; pollen isopolar, obtusely triangular
(seldom quadrangular) in polar view, oblate in equatorial
view, 3(4)-porate (Fig. 6A) or less often brevicolporate,
rugulate, sometimes striate, reticulate or psilate (Cruz and
Melhem 1984) (pollen of A. guaraniticus has been shown also
as quadrangular in polar view and 4-porate (da Luz and
Barth 1999; in A. edulis, > 60% of pollen grains are reported
as 4-porate by Anzótegui and Ferrucci 1998; Fig. 4A); ovary
2(3)-carpellate; style with 2–3 stigmatic branches. Fruit
unicoccate (with a rudimentary coccus) or bicoccate, endo-
carp crustose, exocarp fleshy; seeds exarillate, with papery
testa. A circumtropical genus with about 255 species (Coelho
2014). 2n = 28; 56.
Allophylastrum Acev-Rodr., Phytokeys 5: 40. 2011.—TYPE:
Allophylastrum frutescens Acev.-Rodr.
Dioecious (?), small trees or shrubs; exstipulate. Leaves
trifoliolate; leaflets serrate. Flowers solitary, axillary or in
short racemes, actinomorphic, unisexual with staminate
flowers sometimes bearing a rudimentary 2-locular gynoe-
cium; pedicels elongated, non-articulate; calyx 4-merous,
sepals of similar length, in two whorls; petals wanting; disc
cupular; stamens (5)6, the filaments of nearly equal length,
connate at base; pollen isopolar, obtusely 4- or 5-angled in
polar view, subspherical in equatorial view, 4–5-porate, with
rugulate ornamentation (Fig. 4B); ovary 2-carpellate; style
with 2 stigmatic branches. Fruit unicoccate (with a rudimen-
tary coccus) or bicoccate, endocarp semi-woody, exocarp
fleshy; seeds exarillate, with papery testa. A single, poorly
collected species from Guyana and Brazil (Roraima).
Tribe Paullinieae (Kunth) DC., Prodr. 1: 601. 1824.—
TYPE: Paullinia
Lianas, vines or climbing shrubs, exceptionally erect or
hemicryptophytic shrubs, with a short, axillary shoot bearing
a distal pair of coiled tendrils; stipules minute to foliaceous.
Leaves alternate, with a well-developed distal leaflet, vari-
ously pinnate, trifoliolate, biternate, bipinnate or seldom uni-
foliolate. Inflorescences of thyrses with flowers in lateral
cincinni; pedicel usually articulate below the middle. Flowers
zygomorphic or less often actinomorphic (in Thinouia), struc-
turally or functionally unisexual; calyx 4(5)-merous, sepals
with quincuncial imbrication; corolla of 4(5) distinct petals,
with an adaxial petaloid appendage; disc unilateral, 2- or 4-
lobed, or less often annular (in Thinouia); stamens 8, filament
2017] ACEVEDO-RODRÍGUEZ ET AL.: SUPERTRIBE PAULLINIODAE 109
usually of three different lengths, anther dorsifixed; gynoe-
cium 3-carpellate with a single ovule per carpel.
Distribution—Neotropical, with a couple of species natu-
rally extending into Africa and Madagascar.
Key to the Genera*
1. Leaves trifoliolate; stipules minute; flowers actinomorphic; pollen subspherical to oblate-spherical in equatorial view . . . . . . . . . . . . . . . . . Thinouia
1. Leaves variously compound; stipules minute to foliaceous; flowers zygomorphic (sub-zygomorphic in Lophostigma);
pollen oblate, peroblate or prolate in equatorial view.
2. Petals much shorter than sepals; petal appendages about ½ the length of petals, bifid; stamens of equal lengths;
pollen striate, prolate or prolate-spherical in equatorial view, 4-hemicolporate, 2 colpi always diorate . . . . . . . . . . . . . . . . . . . . . . Lophostigma
2. Petals much longer than sepals; petal appendages as long or nearly as long as the petals, hood-shaped;
stamens of unequal length; pollen reticulate, perforate or psilate, oblate or peroblate in equatorial view.
3. Lianas, climbing shrubs or seldom erect shrubs; fruit always capsular, woody, coriaceous or crustaceous;
seed with a partial to complete arilode (sarcotesta); pollen isopolar or subisopolar, 3-porate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Paullinia
3. Lianas, climbing shrubs, herbaceous vines or less often erect shrubs or prostrate herbs; fruit schizocarpic
or if capsular, membranaceous; seeds lacking an arillode; pollen heteropolar, hemi-syncolporate.
4. Fruits schizocarpic with 3 winged mericarps or exceptionally capsular; seeds without a pseudo-hilum
or if present then trigonous . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Serjania
4. Fruits capsular, membranaceous, with seeds persistent on septa after dehiscence; seeds with a heart-shaped,
reniform, or crescent-shaped pseudo-hilum.
5. Sepals 5; nectary disc 4-lobed; anthers usually with a more or less conspicuous apical connective expansion . . . . . . . . . . . Urvillea
5. Sepals 4 or 5, when 5 nectary disc of 2 corniform lobes; anthers without an apical connective expansion . . . . . . . . . Cardiospermum
*Cardiospermum urvilloides and C. integerrimum are weakly
associated with Serjania in our analyses. However, because
they are morphologically indistinguishable from Cardiospermum
(sensu stricto), we defer creating new genera until additional
data supporting their placement are found.
Thinouia Triana & Planchon, Ann. Sci. Nat. Bot. Ser. 4, 18:
368. 1862.—TYPE: Thinouia myriantha Triana & Planchon.
Allosanthus Radlkofer in A. Engler, Pflanzenr. IV. 165 (Heft 98):
1157. 1933.
Lianas. Early stems and branches with a single vascular
cylinder; older stems occasionally with neoformed cortical
vascular cylinders. Leaves trifoliolate; stipules minute. Inflo-
rescences of umbelliform (racemiform in T. trifoliata) thyrses,
seldom bearing tendrils, axillary or aggregate into terminal
thyrsoid inflorescences with flowers in cincinni; pedicels
articulate. Flowers actinomorphic, 5-merous; calyx cup-shaped,
the sepals valvate, equal; petals 5, obovate to spatulate, with a
pair of short, marginal appendages (a prolongation of petal’s
margins); disc annular; stamens 6–8, of unequal lengths,
anthers dorsifixed; pollen isopolar, obtusely triangular in polar
view, subspherical in equatorial view, tricolporate, with elon-
gated colpi nearly reaching the poles, striate (Fig. 6F); ovary
3-carpellate; style elongated with 3 stigmatic branches. Fruit
schizocarpic, splitting into 3 mericarps (Fig. 5A), each with a
distal wing; seeds trigonous ellipsoid, or lenticular-ellipsoid,
exarillate, with a small hilum. About 10 species from Mexico,
Central America, and South America. 2n = 28 (Urdampilleta
et al. 2008a).
New Combination—
Thinouia trifoliata (Radlk.) Acev.-Rodr. & Ferrucci, comb.
nov.; Allosanthus trifoliatus Radlk. in A. Engler, Pflanzenr.
[Heft 98f] 4, Fam. 165: 1157. 1933.
Lophostigma Radlk. in Engler & Prantl, Nat. Pflanzenfam.
Nachtr. 1: 228. 1897.—TYPE: Lophostigma plumosum Radlk.
Duodichogamous woody vines. Cross section of stem with
a single vascular cylinder. Leaves trifoliolate; stipules minute.
Inflorescences axillary racemiform thyrses with a pair of ten-
drils at base of rachis and flowers in lateral cincinni. Flowers
sub-zygomorphic; sepals 5, unequal, imbricate; petals 4,
shorter than the sepals, with very short, bifid, basally adnate
appendages; disc unilateral, 4-lobed; stamens 8, with short,
equal, filaments, anthers dorsifixed (seemingly basifixed);
pollen heteropolar, subspherical or subspherical-trilobed in
polar view, prolate or prolate-spherical in equatorial view,
4-aperturate pollen heteropolar, subspherical or subspherical-
trilobed in polar view, prolate or prolate-spherical in equato-
rial view, 4-aperturate (possibly an elongated variant of the
hemi-tri-syncolporate pollen present in Thinouia), 2 colpi
always diorate, striate; ovary 3-carpellate (Fig. 6E); style
with 3 stigmatic branches. Fruit a schizocarp splitting into
3 mericarps with an elongated proximal wing (Fig. 5C);
seeds lenticular, exarillate, with a small trigonous or ellipsoid
hilum. Two species, one from Ecuador and Peru, the other
from Bolivia. 2n = 28.
Serjania Plum. ex Miller, Gard. Dic. Abrg. (ed. 4). 1754.—
TYPE: Serjania seriana L.
Houssayanthus Hunziker, Kurtziana 11: 17. 1978.
Chimborazoa H.T. Beck, Brittonia 44: 306–311. 1994.
Balsas J. Jiménez Ramírez & K. Vega, Novon 21: 197. 2011.
Duodichogamous woody or herbaceous vines, often pro-
ducing milky sap. Cross section of stem with a single or with
a central vascular cylinder and (1–2)3–10 peripheral vascular
cylinders. Leaves ternately compound (trifoliolate, biternate,
or triternate) or 5-pinnately compound; stipules generally
small, persistent, deciduous or ephemeral. Thyrse axillary and
solitary with a pair of tendrils at the base of the rachis, or dis-
tal, aggregated into terminal syn-florescenses bearing no ten-
drils. Flowers in lateral cincinni, zygomorphic; sepals 4–5,
unequal, imbricate; petals 4, with a basal, hood-shaped,
crested appendage; disc unilateral, 2- or 4-lobed; stamens 8,
filaments of unequal lengths, anthers dorsifixed; pollen
heteropolar, obtusely triangular in polar view, oblate in equa-
torial view, hemi-tri-syncolporate proximally, sometimes with
short distal demicolpi as well, perforate, reticulate, psilate or
faintly rugulate (Fig. 6D); ovary 3-carpellate; style with 3 stig-
matic branches. Fruit schizocarpic, splitting into three, winged
mericarps (Fig. 5B) [wing proximal, sometimes vestigial or
110 SYSTEMATIC BOTANY [Volume 42
lacking (e.g. S. lachnocarpa (Radlk.) Acev.-Rodr., S. cissoides
Radlk.), or less often circumferential (e.g. S. biternata,
S. dissecta and S. macrolopha)], or fruits sometimes capsular by
dissolution of septa (i.e. S. cristobaliae, S. guerrerensis, S. tortuosa);
seeds lenticular to nearly globose, exarillate, with a small
trigonous or ellipsoid hilum or sometimes with a pseudo-
hilum (e.g. S. glabrata Kunth). About 230 species native to
tropical and subtropical America. 2n = 24.
New Combinations—
Serjania biternata (Weath.) Acev.-Rodr., comb. nov.; Urvillea
biternata Weath., Proc. Amer. Acad. Arts 45: 425. 1910.
Serjania cristobaliae (Ferrucci & Urdampilleta) Ferrucci &
Steinmann, comb. nov.; Cardiospermum cristobaliae
Ferrucci & Urdampilleta, Brittonia 63: 479. 2011.
Fruits in this species are apparently dehiscent (along the
connection of the fruit wall to the partitioning wall), with
flattened, circumferential winged locules; seeds lack a
pseudo-hilum.
Serjania dissecta (S. Watson) Ferrucci & Steinmann, comb.
nov.; Urvillea dissecta S. Watson, Proc. Amer. Acad.
Arts 21: 447. 1886.
Serjania guerrerensis (Cruz Durán & K. Vega) Acev.-Rodr.,
comb. nov.; Balsas guerrerensis Cruz Durán & K. Vega,
Novon 21: 199. 2011.
Serjania macrolopha (Radlk.) Acev.-Rodr. & Ferrucci, comb.
nov.; Cardiospermum macrolophum Radlk., Sitzungsber.
Math.-Phys. Cl. Königl. Bayer. Akad. Wiss. München
8: 261. 1878.
Serjania serjanioides (Rzed. & Calderón) Acev.-Rodr., comb.
nov.; Houssayanthus serjanioides Rzed. & Calderón, Acta
Bot. Mex. 76: 91. 2006.
Serjania sonorensis (S. Watson) Ferrucci & Steinmann,
comb. nov.; Paullinia sonorensis S. Watson, Proc. Amer.
Acad. Arts 24: 45. 1889.
Serjania spinosa (Radlk.) Ferrucci & Steinmann, comb. nov.;
Cardiospermum spinosum Radlk., Contr. U. S. Natl. Herb.
1: 368. 1895.
Serjania tortuosa (Benth.) Ferrucci & Steinmann, comb.
nov.; Cardiospermum tortuosum Benth., Bot. Voy. Sulphur
1: 9. 1844.
Urvillea Kunth in Humboldt, Bonpland & Kunth, Nov.
Gen. Sp. Pl. 5: 105. 1821.—TYPE: Urvillea ulmacea Kunth
Duodichogamous, herbaceous to woody vines. Stems terete
and lenticellate, becoming trilobate at age, with a single vas-
cular cylinder, producing milky or watery sap. Leaves trifolio-
late; stipules minute, persistent or deciduous. Inflorescences
axillary, thyrses with flowers in cincinni; pedicels articulate.
Flowers zygomorphic; sepals 5, unequal, imbricate; petals 4,
spatulate, with a basal hood-shaped, crested appendage on
adaxial surface; disc unilateral, 4-lobed, receptacle enlarged
into a short androgynophore; stamens 8; pollen heteropolar,
obtusely triangular in polar view, oblate in equatorial view,
hemi-tri-syncolporate proximally, sometimes with short distal
demicolpi, perforate, indistinctly rugulate or reticulate; ovary
3-carpellate; style with 3 stigmatic branches. Fruit a 3-locular,
thin, papery, semi-inflated capsule, mericarps flattened into a
wing along dorsal margin (Fig. 5d); seeds 3 or 1, trigonous-
ellipsoid, with a heart-shaped or reniform, white pseudo-
hilum. About 21 species distributed in the United States
(Texas), Mexico, Central America and South America. 2n =
20, 22, 24, 88 (Urdampilleta et al. 2008b).
New Combinations—
Urvillea cuchujaquensis (Ferrucci & Acev.-Rodr.) Acev.-Rodr.
& Ferrucci, comb. nov.; Cardiospermum cuchujaquense
Ferrucci & Acev.-Rodr., Novon 8: 235. 1998.
Urvillea oliveirae (Ferrucci) Acev.-Rodr. & Ferrucci, comb.
nov.; Cardiospermum oliveirae Ferrucci, Bol. Soc. Argent.
Bot. 24: 116. 1985.
Urvillea procumbens (Radlk.) Acev.-Rodr. & Ferrucci, comb.
nov.; Cardiospermum procumbens Radlk., Sitzungsber.
Math.-Phys. Cl. Königl. Bayer. Akad. Wiss. München
8: 262. 1878.
Urvillea pterocarpa (Radlk.) Acev.-Rodr. & Ferrucci, comb.
nov.; Cardiospermum pterocarpum Radlk., Bull. Herb.
Boissier II, 3: 806. 1903.
Cardiospermum L., Sp. Pl. 366. 1753.—TYPE: Cardiospermum
halicacabum L.
Duodichogamous herbaceous vines. Leaves trifoliolate or
biternate; stipules usually minute and persistent. Inflores-
cences simple, axillary, racemiform or umbelliform thyrses
bearing tendrils at base of rachis, with flowers in cincinni.
Flowers zygomorphic; sepals 4(5), unequal, imbricate; petals
4, with a basal, hood-shaped, crested appendage; disc unilat-
eral, 2- or 4-lobed; stamens 8, filaments of unequal lengths,
anthers dorsifixed; pollen heteropolar, obtusely triangular in
polar view, oblate in equatorial view, tri-syncolporate proxi-
mally, perforate to reticulate (Fig. 6B); ovary 3-carpellate;
style with 3 stigmatic branches. Fruit a 3-locular septifragal-
marginicidal, inflated capsule, generally with sub-
chartaceous walls; seeds brown or black, with a small, round
to heart-shaped, light-colored area around the hilum (pseudo-
hilum sensu Pijl 1957; Fig. 8D). Six or seven species native
to the Neotropics, one of which is also native in Africa, and
2 that are now widely distributed throughout the tropics.
2n = 14, 18, 20, 22, 36.
Paullinia L., Sp. Pl. 365. 1753. —TYPE: Paullinia pinnata L.
Duodichogamous, woody vines, usually producing milky
sap. Cross section of stem with a central and 3–5 peripheral
vascular cylinders, or with a single vascular cylinder. Leaves
trifoliolate, 5-foliolate pinnate, partly bipinnate, bipinnate,
biternate, or variously dissected; stipules minute to folia-
ceous. Inflorescences axillary, solitary or fascicled thyrses,
with a pair of tendrils at base of rachis when solitary, some-
times cauliflorous and fascicled and bearing no tendrils.
Flowers zygomorphic; sepals 4–5, unequal, imbricate; petals
4, with a basal, hood-shaped, crested appendage; disc unilat-
eral, 2- or 4-lobed; stamens 8, filaments of unequal lengths,
anthers dorsifixed; pollen isopolar or subisopolar, obtusely
triangular in polar view, oblate in equatorial view, triporate,
perforate (Fig. 6C); ovary 3-carpellate; style with 3 stigmatic
branches. Fruit a 1–3-locular, septifragal-marginicidal capsule,
locules sometimes dorsally winged or exceptionally spiny;
seeds globose, oblong or ellipsoid, with a partial to nearly
complete sarcotesta, leaving a scar when removed (Figs. 7C,
2017] ACEVEDO-RODRÍGUEZ ET AL.: SUPERTRIBE PAULLINIODAE 111
8A–B). About 200 species native to the Neotropics, one
species extending into Africa and Madagascar. 2n = 24, 210
(de Freitas et al. 2007).
Placement Pending—
Guindilia Gillies ex Hook. & Arn., Hooker’s Bot. Misc. 3: 170.
1833. —TYPE: Guindilia trinervis Gillies ex Hook. & Arn.
Valenzuelia Bertero ex Cambessèdes, Nouv. Ann. Mus. Hist.
Nat. 3: 236. 1834, non Mutis, 1810.
Duodichogamous trees. Leaves simple, opposite, entire
or tridentate at apex, exstipulate. Inflorescences of axillary
cymes. Flowers zygomorphic, bisexual or functionally unisex-
ual; sepals 5, imbricate; petals 4(5), with a hood-shaped,
crested, ventral appendage; disk unilateral, 2-lobed-pyramidal;
stamens 8; pollen colporate, striate (Fig. 4F); ovary 3-carpellate,
with a single ovule per carpel; style filiform; stigma 3-lobed.
Fruit schizocarpic, splitting into (1–)3 subglobose, crustose
mericarps. Seed exarillate. Three species from southern
South America.
Acknowledgments. We would like to thank our colleagues at the
Smithsonian, Vicki Funk for helping with the cladistic analysis of
morphological characters, Rob Soreng for his advice on the use of
supra-generic names, and Alice Tangerini for her valuable help formatting
the illustrations; Peter Endress (Univ. Zürich) for his valuable discussion
on floral symmetry; and Nicholas Turland (B) for his advice on the use of
super rank names as allowed by ICN. Molecular work was supported, in
part, by the Laboratories of Analytical Biology, NMNH, Smithsonian
Institution, and by a grant from FAPESP (FAPESP 2014/18002-2; 2015/
9444-4) to the University of São Paulo.
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Appendix 1. Voucher and GenBank information for taxa included in
the phylogenetic analyses. Listed as: taxon, collection, herbarium, place of
origin, and GenBank accession numbers (ITS, trnL intron). Herbarium
acronyms follow Index Herbariorum (Thiers, continuously updated).
Accession numbers for new data begin with KX; an en-dash (–) indicates
missing data.
Allophylastrum frutescens Acev.-Rodr., Lima 812 (K), Brazil, KX584885,
KX584982. Allophylus abyssinicus (Hochst.) Radlk., Desissa & Binggeli
DD-318 (MO), Ethiopia, KX584886, KX584983. Allophylus africanus
P. Beauv., Balkwill 4206 (MO), South Africa, KX584887, KX584984.
Allophylus arboreus Choux, Wohlhauser & Stiefle 60072 (MO), Madagascar,
KX584888, KX584985. Allophylus bicruris Radlk., Barthelat 828 (MO),
Mayotte, KX584889, KX584986. Allophylus bojerianus (Cambess.) Blume,
Ratovoson 961 (MO), Madagascar, KX584890, KX584987. Allophylus
chaunostachys Gilg, Mwangoko 729 (MO), Tanzania, KX584891, KX584988.
Allophylus chirindensis Baker f., Hizza 26 (MO), Tanzania, KX584892,
KX584989. Allophylus cominia Sw., Acevedo-Rodríguez 12216 (US), Mexico,
KX584893, KX584990. Allophylus crassinervis Radlk., Acevedo-Rodríguez
s.n. (no voucher), Puerto Rico, KX584894, KX584991. Allophylus decipiens
(E. Mey.) Radlk., Phillipson 4194 (MO), South Africa, KX584895,
KX584992. Allophylus dissectus Gereau & G.E. Schatz, Phillipson 1704
(MO), Madagascar, KX584896, KX584993. Allophylus gardineri Summerh.,
Pignal 1834 (MO), Mayotte, KX584897, KX584994. Allophylus hirtellus
(Hook. f.) Radlk., Cheek 5059 (?), KX584898, KX584995. Allophylus pervillei
Blume, Hoffmann 399 (MO), Mayotte, KX584899, KX584996. Allophylus
poungouensis Pellegr., McPherson 16109 (MO), Gabon, KX584900,
KX584997. Allophylus puberulus (Cambess.) Radlk., Somner 1069 (US),
Brazil, KX584901, KX584998. Allophylus racemosus Sw., Acevedo-Rodríguez
12180 (US), Mexico, KX584902, KX584999. Allophylus rubifolius (A. Rich.)
Engl., Kuchar 23357 (MO), Tanzania, KX584903, KX585000. Allophylus
sp., Acevedo-Rodríguez 14847 (NY), Brazil, KX584904, KX585001.
Allophylus sp., Barthelat 1540 (MO), Mayotte, KX584905, KX585002.
Athyana weinmanniifolia (Griseb.) Radlk., Acevedo-Rodríguez 11166 (US),
Bolivia, KX584906, KX585003. Athyana weinmanniifolia (Griseb.) Radlk.,
Villalobos 4243 (MO), Bolivia, KX584907, KX585004. Balsas guerrerensis
Cruz Durán & K. Vega, Vega Flores 1318 (US), Mexico, KX584908,
KX585005. Blomia prisca (Standl.) Lundell, Acevedo-Rodríguez 12242 (US),
Mexico, EU720444, EU721208. Bridgesia incisifolia Cambess., Landrum
9824 (NY), Chile, KX584909, KX585006. Cardiospermum anomalum
Cambess., Urdampilleta 330 (UEC), Brazil, KX584910, ––. Cardiospermum
bahianum Ferrucci & Urdampilleta, Urdampilleta 389 (UEC), Brazil,
KX584911, ––. Cardiospermum corindum L., Harder & Bringham 3495 (MO),
Zambia, KX584912, KX585007. Cardiospermum corindum L., JLR291 (?),
KM062239, KM062345. Cardiospermum cristobaliae Ferrucci & Urdampilleta,
Urdampilleta 421 (UEC), Brazil, KX584913, ––. Cardiospermum cuchujaquense
Ferrucci & Acev.-Rodr., Van Devender 92-1012 (ARIZ), Mexico, KX584914,
KX585008. Cardiospermum grandiflorum Sw., ATBP 603 (MO), Uganda,
KX584915, KX585009. Cardiospermum grandiflorum Sw., Gildenhuys H1 (?),
Hawaii, KM062277, KM062362. Cardiospermum halicacabum L., Gildenhuys
280 (?), Argentina, KM062192, KM062341. Cardiospermum halicacabum L.,
CSM 8 (?), South Africa, KM062194, KM062296. Cardiospermum
halicacabum L., Murata 72327 (MO), Japan, KX584916, ––. Cardiospermum
heringeri Ferrucci, Urdampilleta 437 (US), Brazil, KX584917, KX585010.
Cardiospermum integerrimum Radlk., Urdampilleta 312 (UEC), Brazil,
KJ845651, ––. Cardiospermum integerrimum Radlk., Urdampilleta 312 (US),
Brazil, KX584918, KX585011. Cardiospermum oliveirae Ferrucci,
Urdampilleta 337 (UEC), Brazil, KX584919, –– Cardiospermum pechuelii
Kuntze, Gildenhuys s.n., Namibia, KM062216, KM062299. Cardiospermum
procumbens Radlk., Urdampilleta 322 (UEC), Brazil, KX584920, ––.
Cardiospermum pterocarpum Radlk., Urdampilleta 321 (US), Brazil,
KX584921, KX585012. Cardiospermum urvilleoides (Radlk.) Ferrucci,
Urdampilleta 425 (US), Brazil, KX584922, KX585013. Chimborazoa
lachnocarpa (Radlk.) H.T. Beck, Wiggens 11060 (US), Ecuador, KX584923,
KX585014. Cupania dentata DC., Acevedo-Rodríguez 12241 (US), Mexico,
KX584924, KX585015. Cupania emarginata Cambess., Somner1068 (RBR),
2017] ACEVEDO-RODRÍGUEZ ET AL.: SUPERTRIBE PAULLINIODAE 113
Brazil, KX584925, KX585016. Diatenopteryx sorbifolia Radlk., Zardini 43371
(MO), Paraguay, EU720534, EU721303. Dictyoneura obtusa Blume,
Edwards KE142 (JCT), Australia, EU720428, EU721187. Diploglottis
campbellii Cheel, Chase 2048 (K), Australia, EU720457, EU721224.
Elattostachys apetala Radlk., Munzinger 692 (MO), New Caledonia,
EU720537, EU721306. Guindilia dissecta (C. & Burk.) Hunz., Ferrucci 2928
(CTES), Argentina, KX584926, KX585017. Guioa villosa Radlk., McPherson
18040 (MO), New Caledonia, EU720544, EU721314. Haplocoelum foliosum
(Hiern.) Bullock, Edwards KE195 (JCT), Tanzania, FJ514259, FJ514265.
Haplocoelum inoploeum Radlk., Lap 117 (?), FJ514259, FJ514265.
Houssayanthus biternatus (Weath) Rzed. & Calderón, Catalán & Terán 837
(MO), Mexico, KX584927, KX585018. Houssayanthus incanus (Radlk.)
Ferrucci, Ferrucci 2710 (CTES), Argentina, KX584928, KX585019. Jagera
javanica (Blume) Kalkman, Chase 2130 (K), Bogor, EU721236, EU720468.
Lepisanthes senegalensis (Poir.) Leenh., Callmander 627 (MO), Madagascar,
EU720492, U72126. Lophostigma plumosum Radlk., Acevedo-Rodríguez 6554
(US), Bolivia, KX584929, KX585020. Macphersonia gracilis O. Hoffm.,
Rabenantoandro 1081 (MO), Madagascar, EU720550, EU721320. Matayba
guianensis Aubl., Acevedo-Rodríguez 12342 (US), French Guiana,
EU720527, EU721294. Melicoccus bijugatus Jacq., Acevedo-Rodríguez, no
voucher, Puerto Rico, EU927391, EU721207. Melicoccus lepidopetalus
Radlk., Acevedo-Rodríguez 11128 (US), Bolivia, EU720443, EU721206.
Paullinia clathrata Radlk., Acevedo-Rodríguez 14305 (US), Peru, KX584930,
KX585021. Paullinia coriacea Casar., Somner 1070 (RBR), Brazil, KX584931,
KX585022. Paullinia cuneata Radlk., Acevedo-Rodríguez 14255 (US), Peru,
KX584932, KX585023. Paullinia elegans Cambess., Acevedo-Rodríguez
14976 (US), Brazil, KX584933, KX585024. Paullinia hystrix Radlk.,
Acevedo-Rodríguez 14417 (US), Peru, KX584934, KX585025. Paullinia
imberbis Radlk., Schunke Vigo 14928 (US), Peru, KX584935, KX585026.
Paullinia olivacea Radlk., Schunke Vigo 16002 (US), Peru, KX584936,
KX585027. Paullinia pinnata L., Acevedo-Rodríguez 11088 (US), French Guiana,
KX584937, KX585028. Paullinia prevostiana Acev.-Rodr., Acevedo-Rodríguez
11113 (US), French Guiana, KX584938, KX585029. Paullinia rubiginosa
Cambess., Thomas 12995 (US), Brazil, KX584939, KX585030. Paullinia
rufescens Rich., Acevedo-Rodríguez 12350 (US), French Guiana, KX584940,
KX585031. Paullinia spicata Benth., Acevedo-Rodríguez 12344 (US), French
Guiana, KX584941, KX585032. Paullinia stellata Radlk., Acevedo-Rodríguez
14958 (US), Brazil, KX584942, KX585033. Paullinia xestophylla Radlk.,
Hoffman 5955 (US), Suriname, KX584943, KX585034. Plagioscyphus
unijugatus Capuron, Buerki 145 (NEU), Madagascar, EU720475, EU721245.
Sapindus oligophyllus Merr. & Chun, How 70627 (US), China, KX584944,
KX585035. Serjania altissima (Poepp.) Radlk., Acevedo-Rodríguez 14953 (US),
Brazil, KX584945, KX585036. Serjania ampelopsis Planch. & Lind., Acevedo-
Rodríguez 11181 (US), Bolivia, KX584946, KX585037. Serjania caracasana
(Jacq.) Willd., Acevedo-Rodríguez 15107 (US), Mexico, KX584947, KX585038.
Serjania cf. caracasana (Jacq.) Willd., Acevedo-Rodríguez 3483 (US), Guyana,
KX584948, KX585039. Serjania clematidifolia Cambess., Somner 1078 (RBR),
Brazil, KX584949, KX585040. Serjania communis Cambess., Somner 1334
(US), Brazil, KX584950, KX585041. Serjania cuspidata Cambess., Somner
1400 (US), Brazil, KX584951, KX585042. Serjania diversifolia (Jacq.) Radlk.,
Acevedo-Rodríguez 13462 (US), Puerto Rico, KX584952, ––. Serjania elongata
J.F. Macbr., Acevedo-Rodríguez 13547 (US), Brazil, KX584953, ––. Serjania
emarginata Kunth, Acevedo-Rodríguez 15135 (US), Mexico, KX584954,
KX585043. Serjania erythrocaulis Acev.-Rodr. & Somner, Acevedo-Rodríguez
3729 (US), Brazil, KX584955, KX585044. Serjania eucardia Radlk., Somner 1072
(RBR), Brazil, KX584956, KX585045. Serjania fuscifolia Radlk., Somner 1455
(RBR), Brazil, KX584957, KX585046. Serjania grandiceps Radlk., Acevedo-
Rodríguez 13704 (US), Brazil, KX584958, KX585047. Serjania grandifolia
Sagot, Acevedo-Rodríguez 11121 (US), French Guiana, KX584959, ––. Serjania
ichthyoctona Radlk., Somner 1081 (RBR), Brazil, KX584960, KX585048.
Serjania lethalis St. Hil., Roque 1860 (ALCB), Brazil, KX584961, KX585049.
Serjania lethalis St. Hil., Somner 1381 (RBR), Brazil, KX584962, KX585050.
Serjania marginata Casar., Acevedo-Rodríguez 11131 (US), Bolivia, KX584963,
KX585051. Serjania membranacea Splitg., Acevedo-Rodríguez 12329 (US),
French Guiana, KX584964, ––. Serjania mexicana (L.) Willd., Acevedo-
Rodríguez 12014 (US), Jamaica, KX584965, KX585052. Serjania mexicana (L.)
Willd., Acevedo-Rodríguez 15080 (US), Mexico, KX584966, KX585053.
Serjania paniculata Kunth, Acevedo-Rodríguez 15143 (US), Mexico, KX584967,
KX585054. Serjania perulacea Radlk., Acevedo-Rodríguez 11134 (US), Bolivia,
KX584968, KX585055. Serjania unguiculata Radlk., Acevedo-Rodríguez 15081
(US), Mexico, KX584969, KX585056. Serjania yucatanensis Standl., Acevedo-
Rodríguez 12183 (US), Mexico, KX584970, KX585057. Talisia angustifolia
Radlk., Zardini 43368 (MO), Paraguay, EU720558, EU721516. Talisia nervosa
Radlk., Pennington 628 (MO), ∼, EU720474, EU721244. Talisia obovata A.C.
Sm., Lombello 13 (MO), Brazil, EU720485, EU721255. Thinouia mucronata
Radlk., Keller 6919 (US), Argentina, KX584971, KX585058. Thinouia
myriantha Triana & Planch. Acevedo-Rodríguez 12359 (US), French Guiana, ––,
KX585059. Thinouia restingae Ferrucci & Somner, Somner 1074 (RBR),
Brazil, KX584972, KX585060. Thouinia acuminata S. Watson, Liston 633-2, ––,
EU720478, EU721249. Thouinia paucidentata Radlk., Acevedo-Rodríguez
12160 (US), Mexico, KX584973, ––. Thouinia portoricensis Radlk., Acevedo-
Rodríguez 11435 (US), Puerto Rico, KX584974, ––. Thouinia tomentosa DC.,
Acevedo-Rodríguez 12867 (US), Dominican Republic, ––, KX585061. Thouinia
villosa DC., Hall 825 (US), Mexico, KX584975, KX585062. Tristiropsis
acutangula Radlk., Chase 1358 (K), Bogor, EU720453, EU721220. Urvillea
chacoensisHunz.,Acevedo-Rodríguez 11133 (US), Bolivia, KX584976, KX585063.
Urvillea chacoensis Hunz., Keller 6834 (US), Argentina, KX584977, KX585064.
Urvillea rufescens Cambess., Somner 1073 (RBR), Brazil, KX584978, KX585065.
Urvillea ulmacea Kunth, Acevedo-Rodríguez 15145 (US), Mexico, KX584979,
KX585066. Urvillea ulmacea Kunth, Reyes-García 5585 (MO), Mexico,
KX584980, KX585067. Vouarana guianensis Aubl., Acevedo-Rodríguez 5031
(US), French Guiana, KX584981, KX585068.
114 SYSTEMATIC BOTANY [Volume 42