An updated account of Simaroubaceae with emphasis on American taxa

Abstract

Simaroubaceae are among the families whose circumscription radically changed over time, because phylogenetic analyses undertaken since 1995 demonstrated it was a polyphyletic group in its traditional delimitation. Currently, Simaroubaceae sensu stricto are a mostly pantropical, highly supported monophyletic group composed of 22 genera and approximately 120 species. Growing knowledge about members of the family has allowed several advances over the last couple of decades. The primary center of diversity for Simaroubaceae is in tropical America, and new contributions have been recently made regarding members of the family in the region, including descriptions of several new taxa. Hence, we undertook an updated overview of general information available for the group, with focus on American taxa of Simaroubaceae, and highlighting numerous data published after the 2011 monograph. Besides aiming to contribute to a better knowledge of a family with past controversial limits, we emphasize research topics in which the current scarcity of data demands further investigation.

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Vol.:(0123456789)
1 3
Brazilian Journal of Botany
https://doi.org/10.1007/s40415-021-00731-x
SYSTEMATICS, PHYLOGENY & FLORISTICS - REVIEW
An updated account ofSimaroubaceae withemphasis onAmerican
taxa
JoséRubensPirani1 · LucasC.Majure2 · MarceloFernandoDevecchi1
Received: 31 May 2021 / Revised: 22 July 2021 / Accepted: 24 July 2021
© Botanical Society of Sao Paulo 2021
Abstract
Simaroubaceae are among the families whose circumscription radically changed over time, because phylogenetic analyses
undertaken since 1995 demonstrated it was a polyphyletic group in its traditional delimitation. Currently, Simaroubaceae
sensu stricto are a mostly pantropical, highly supported monophyletic group composed of 22 genera and approximately 120
species. Growing knowledge about members of the family has allowed several advances over the last couple of decades.
The primary center of diversity for Simaroubaceae is in tropical America, and new contributions have been recently made
regarding members of the family in the region, including descriptions of several new taxa. Hence, we undertook an updated
overview of general information available for the group, with focus on American taxa of Simaroubaceae, and highlighting
numerous data published after the 2011 monograph. Besides aiming to contribute to a better knowledge of a family with
past controversial limits, we emphasize research topics in which the current scarcity of data demands further investigation.
Keywords Eudicots· Morphology· Rutales· Sapindales· Taxonomy
1 Introduction
Several traditional families of plants have a history
going back to the XVIIIth century, when they were first
described by botanists suchas Antoine-Laurent de Jussieu
(1748–1836), Michel Adanson (1727–1806), andAugustin-
Pyramus de Candolle (1778–1841). Along the following
centuries, great progress was gradually achieved toward
a better knowledge of the general diversity and morphol-
ogy of the components of each family. With a continuous
increase in new evidence from other sources, such as anat-
omy, palynology, chemistry, cytology and genetics, a great
improvement of the circumscription of the plant families
was achieved. Integration of data from some or all of these
sources characterizes most systems of classification pro-
duced in the nineteenth and twentieth centuries. Among the
remarkable ones are those elaborated by H. G. Adolf von
Engler (1844–1930), John Hutchinson (1884–1972), Armen
Takhtajan (1910–2009), Arthur Cronquist (1919–1992),
Robert F. Thorne (1920–2015) and Rolf M. T. Dahlgren
(1932–1987). The advent and flourishment of the Phyloge-
netic Systematics approach after ideas of Emil Hans Willi
Hennig (1913–1976) opened a new era when the use of
explicit principles to define taxa was required, especially
the search for synapomorphies to diagnose monophyl-
etic groups, as did Dahlgren etal. (1985) for families and
other taxa of the monocotyledons. The full access to DNA
sequencing from the early 1990years on allowed a rapid
construction of phylogenies, and this brought a new age of
tests of monophyly of the traditional groups.
Simaroubaceae are among the families whose circum-
scription radically changed over time, because its traditional
delimitation (Engler 1931) was showed to be an “artificial
construct” (Fernando etal. 1995). Five of the six subfamilies
recognized by Engler (1931) were excluded from the family,
while a few genera were included in it. Growing knowledge
about members of Simaroubaceae allowed several advances,
such as phylogenies based on larger sampling and number
of gene regions (Clayton etal. 2007; Devecchi etal. 2018a),
biogeographical analysis (Clayton etal. 2009), anda world-
wide taxonomic monograph (Clayton 2011).
* José Rubens Pirani
pirani@usp.br
* Marcelo Fernando Devecchi
mfdevecchi@usp.br
1 Departamento de Botânica, Instituto de Biociências,
Universidade de São Paulo, SãoPaulo, SP05508-090, Brazil
2 Florida Museum ofNatural History, University ofFlorida,
Gainesville, FL32611, USA

J.R.Pirani et al.
1 3
The primary center of diversity for Simaroubaceae is in
tropical America (e.g., Thomas 1990), and new contribu-
tions have been recently made regarding members of the
family in the region, mainly as descriptions of several new
taxa (e.g., Schrader & Davis 2011; Devecchi & Pirani 2015;
Palacios 2015; Devecchi etal. 2016, 2018b, c; Noa-Monzón
and González-Gutiérrez 2019; Majure etal. 2021a), a genus
synonymization (Euleria Urb. in Picrasma Blume, Thomas
etal. 2011), and a genus revision (Homalolepis Turcz., Devec-
chi etal. 2018b), as well as regional floras (e.g., Hahn and
Thomas 2001; Thomas and Franceschinelli 2005; Devecchi
and Pirani 2016, 2020; Devecchi etal. 2021) and broad flo-
ristic projects, such as a checklist of the vascular plants of the
Americas (Ulloa Ulloa etal. 2017), a catalogue and an illus-
trated guide to the trees of Peru (Brako and Zarucchi 1993;
Pennington etal. 2004), catalogues of Southern Cone (Zuloaga
etal. 2008), Bolivia (Pirani and Thomas 2014) and Colom-
bia (Bernal etal. 2016) and Flora do Brasil (2020), the latter
with a monographic treatment for the family (Devecchi etal.
2020). Taxonomy at thespecies level has been improved also
by detailed studies on two complex species (Simaba guianen-
sis Aubl., Thomas 1985; Homalolepis ferruginea (A.St.-Hil.)
Devecchi & Pirani, Devecchi etal. 2018d), and phenetic analy-
ses quantifying the variation of diagnostic features in related
species of Simarouba (Franceschinelli and Yamamoto 1993;
Franceschinelli etal. 1999). A general treatment in a book on
the Neotropical families of flowering plants was presented by
Thomas (2004).
On the other hand, most floras and other works on Neo-
tropical Simaroubaceae published earlier that 2000 include
surpassed descriptions and taxa that do not belong in the group
ever since (e.g., Small 1911; Fawcett and Rendle 1920; Mac-
bride 1949; Brizicky 1962; Porter 1975; Jansen-Jacobs 1979;
Pirani 1987a, b; Thomas 1990; Killeen etal. 1993; Pirani
1997). A couple of floras published after 2000 still included
genera, such as Picramnia Sw (currently in Picramniaceae,
Picramniales), as authors had to follow the general rules of
each floristic plan (Pirani 2002; Pennington etal. 2004).
Thus, this is a conducive time for undertaking an update
of general information on the group, with afocus on Ameri-
can taxa of Simaroubaceae. Our aim is to contribute to a bet-
ter knowledge of a family with past controversial limits, and
about which still there is a scarcity of data from some fields
of research, while the other needs complimentary investiga-
tion and prospects.
2 A brief historical overview, withemphasis
intaxonomy andphylogeny
Simaroubaceae was first published by De Candolle (1811)
“as Simarubeae”, including Ailanthus Desf., Brucea J.F.
Mill., Castela Turpin, Quassia L., Samadera Gaertn.,
Soulamea Lam., Simaba Aubl., and Simarouba Aubl. These
genera were previously described from 1762 to 1806, clas-
sified first within the classes Decandria and Polygamia of
Linnaeus’ classification, and were later transferred to the
“ordo” Terebinthacearum by Jussieu (1789). Circumscrip-
tion of this latter taxon remained somewhat controversial
for some decades, but subsequently the concept of Tere-
binthaceae became limited to genera currently included in
Anacardiaceae and Burseraceae (e.g., Marchand 1869), and
the definition of the family Simaroubaceae by De Candolle
(1811) prevailed.
A revisional account on the family was elaborated by
Planchon (1846), who proposed the first attempt to an inf-
rafamilial classification, placing 17 genera into four tribes:
Simaroubeae, Harrisonieae, Ailantheae, Spathelieae, based
mainly on carpel union (free or connate), number of ovules
per carpel, type of embryo and number of stamens and pet-
als. Later on, Bentham and Hooker (1862) proposed a clas-
sification recognizing only two tribes, Simaroubeae with free
carpels, and Picramnieae with asyncarpous gynoecium.
Engler (1874) in his treatment for Martius’ Flora bra-
siliensis recognized three tribes in Simaroubaceae (spelled
Simarubaceae at that time): Surianeae, Eusimarubeae and
Picramnieae, based on the structure of ovaries and styles,
and the number of ovules. In the worldwide monograph
of the family, Engler (1897, 1931) excluded the subtribe
Dictyolomeae (formerly in tribe Eusimarubeae, then trans-
ferred to Rutaceae), but largely expanded the circumscrip-
tion of Simaroubaceae, recognizing eight subtribes and
nine tribes in six subfamilies: Alvaradoideae, Irvingioideae,
Kirkioideae, Picraminoideae, Simarouboideae (the largest
one) and Surianoideae. Besides the gynoecium features
previously used, he also took into account characters of
the androecium, such as the presence or lack of scale-like
appendages at the filaments base, and leaf traits, such as the
division of the lamina. Simaroubaceae sensu Engler (1931)
became a large family comprising about 30 genera and 200
species of tropical and subtropical trees and shrubs. This
classification persisted in subsequent editions of Engler’s
Syllabus der Pfanzenfamilien (Melchior 1964, ed. 12).
Growing evidence from several sources gradually
revealed the heterogeneous nature of Simaroubaceae as
defined by Engler (1931), suchas through theanalysis of
wood anatomy (e.g., Webber 1936; Heimsch 1942), gen-
eral anatomy (Metcalfe and Chalk 1950), pollen morphol-
ogy (Erdtman 1952, 1986; Basak 1963, 1967; Moncada
and Machado 1987) and phytochemistry (e.g., Hilditch and
Williams 1964; Gibbs 1974; Waterman 1983; Simão etal.
1991). Webber (1936) and Heimsch (1942) suggested the
exclusion of some of the subfamilies, based on anatomic
evidences, as did Gibbs (1974) on chemical grounds. Even
though one or more of the subfamilies were excluded in sys-
tems of classification proposed during the second half of the

An updated account ofSimaroubaceae withemphasis onAmerican taxa
1 3
twentieth century, suchas the ones proposed by Takhtajan
(1980), Dahlgren etal. (1985), Cronquist (1981, 1988) and
Thorne (1992), the Simaroubaceae continued to encompass
considerable diversity in secondary chemistry, macro- and
micromorphology.
However, based on structural studies of the gynoecium
structure of ten genera by Ramp (1988) suggested that Sima-
roubaceae sensu lato represented a polyphyletic group. This
suggestion was later corroborated by a study of fruit anatomy
by Fernando and Quinn (1992), and eventually by the first
molecular phylogenetic analysis focusing on Simaroubaceae
(Fernando etal. 1995). Although limited to sequences of a
single gene (rbcL) of seven genera, the latter study recovered
Simaroubaceae s.l. as not monophyletic, with at least five
separate lineages. Only members of Kirkioideae and Sima-
rouboideae (except Harrisonia) clustered within the Sap-
indales clade, while those of Irvingioideae, Surianoideae,
Alvaradoideae and Picramnioideae emerged well outside
the order. The two latter currently constitute Picramniaceae,
Picramniales (see Stevens etal. 2002); Irvingioideae and
Surianoideae had been long before removed as Irvingiaceae
(currently in Malpighiales), and Surianaceae are embedded
in Fabales (see Stevens etal. 2002 onwards). Thus, Sima-
roubaceae sensu stricto was recircumscribed as a well-sup-
ported monophyletic group, composed only by the genera of
Simarouboideae, with the inclusion of Leitneria (formerly
Leitneriaceae), and the exclusion of Harrisonia, which is
nested within Rutaceae (Fernando etal. 1995). Leitneriaceae
were formerly included in Leitneriales in Engler’s Syllabus
(Melchior 1964) and also by authors, such as Takhtajan
(1980) and Cronquist (1988), within subclass Hamamelidae
on account of its reduced, naked, wind-pollinated flowers.
However, this family was treated as a member of Rutales
(= Sapindales) by Thorne (1992) and later also by Takhtajan
(1997). Kirkia as the only genus of Kirkiaceae was already
proposed by authors as Takhtajan (1980) and remains within
Sapindales (Gadek etal. 1996; Stevens etal. 2002).
Further evidences based on morphological and molecular
grounds help support Simaroubaceae s.s. as a monophyl-
etic group (Gadek etal. 1996; Clayton etal. 2007, 2009;
Muellner etal. 2007, 2016). The latest comprehensive phy-
logenetic studies of the family were conducted by Clayton
etal. (2007, 2009), based on four molecular regions and a
broad taxon sampling. A recent phylogeny based on six gene
regions from a richer sampling of neotropical taxa (Devecchi
etal. 2018a) improved the knowledge about the neotropical
lineages, and most clades from Clayton’s study (2009) were
also corroborated.
Putative synapomorphies of Simaroubaceae are the exclu-
sive triterpenoid compounds of the quassinoid type (Fer-
nando etal. 1995), five carpels united only by their styles
and separating in fruit and one ovule per locule (e.g., Ste-
venson etal. 2002; Alves etal. 2021—this issue).
Regarding the suprafamilial relationships, Simaroubaceae
form a well-supported clade with Rutaceae and Meliaceae
in Sapindales (Gadek etal. 1996; Källersjö etal. 1998;
Savolainen etal. 2000; Soltis etal. 2000; Muellner-Riehl
etal. 2016), but the sister relationship between the families
is still uncertain, with possible topologies—Rutaceae sister
to Simaroubaceae (Gadek etal. 1996), or Meliaceae sister
to Simaroubaceae (Chase etal. 1999, Muellner etal. 2007,
Muellner-Riehl etal. 2016), or Rutaceae sister to Meliaceae
(Fernando etal. 1995). Majure etal. (2021b—this issue)
resolved Simaroubaceae strongly supported as sister to Ruta-
ceae using plastome data. These three families share the
presence of unusual triterpenoids, bitter substances, which
are based on degraded forms of triterpenes and uncommon
in other Angiosperms: the limonoids in Meliaceae and Ruta-
ceae, and the quassinoids in Simaroubaceae (Kubitzki and
Gottlieb 1984; Gadek etal. 1996; Kubitzki etal. 2011). The
Simaroubaceae are related to the Rutaceae in terms of chem-
ical composition, wood anatomy, and in the free stamens
(which are mostly united in Meliaceae), but it is remarkably
distinct from Rutaceae in its absence of secretory cavities
containing aromatic oils in leaves and floral parts, and by its
uniovulate carpels, as well as by the absence of quassinoids
in Rutaceae (Fernando and Quinn 1992). The alternative
sister group relationship of Simaroubaceae and Meliaceae
is supported also by some morphological features shared by
both families, as discussed by Gama etal. (2021) and Alves
etal. (2021—this issue).
A general treatment of the family since its new circum-
scription made by Fernando and Quinn (1995) was provided
by Clayton (2011), including a complete synopsis with
identification keys and descriptions of all genera. Several
decades before, important contributions to the knowledge
of neotropical genera were provided by Arthur Cronquist,
who produced synopses of Castela (Cronquist 1944a, 1945),
Simarouba (1944b) and Simaba (1944c), and eventually a
resume of the remaining American genera (1944d). Later,
the largest genus Simaba was reviewed by Cavalcante
(1983), mostly following species circumscriptions presented
in Cronquist (1944c). Even though there were proposals to
reduce Simaba to a section of Quassia, along with other
extra-neotropical genera of subfamily Simarouboideae,
by Pierre (1896) and Nooteboom (1962), in the Americas
Simaba, Quassia, and Simarouba were maintained as dis-
tinct genera in regional floras and monographs (e.g., Cron-
quist 1944c; Porter 1973; Arrázola 1993; Cavalcante 1983;
Feuillet 1983; Thomas 1985, 1990; Pirani 1987a, b, 2015;
Hahn and Thomas 2001; Thomas and Franceschinelli 2005;
Devecchi and Pirani 2015, 2016; Devecchi etal. 2021).
Molecular phylogenies by Clayton etal. (2007, 2009) also
refuted the broad circumscription of Simaba as proposed by
Nooteboom (1962), until eventually a phylogenetic study
(Devecchi etal. 2018a) based on data of five molecular

J.R.Pirani et al.
1 3
regions, including two nuclear (ETS, ITS) and three plas-
tidial ones (psbA-trnH, rps16 and trnL-trnF) provided strong
evidence that Simaba was not monophyletic. The genus was
there reduced to include only the species of S. sect Tenui-
florae Engl., while the species belonging to the two mostly
extra-Amazonian sections (S. sect. Floribundae Engl., and
S. sect. Grandiflorae Engl.) were transferred to the reinstated
Homalolepis Turcz., which emerged closely related to Sima-
rouba (Devecchi etal. 2018a). Homalolepis is currently the
largest genus of the family and was subject of a detailed
taxonomic revision (Devecchi etal. 2018b).
Except for Castela, Simaba and Picrasma, the remaining
American genera have been maintained under the circum-
scription, such as presented in Engler’s monograph (1931)
and Cronquist’s synopses (1944a; 1944b, 1944d). Neotropi-
cal species of Picrasma were treated by Engler (1931) in a
distinct genus, Aeschrion Vell., but were synonymized under
the former by Cronquist (1944d). Holacantha A. Gray, a
genus maintained separately from Castela by Engler (1931)
and Cronquist (1944a), was synonymized with Castela by
Moran and Felger (1968) based on a putatively morpho-
logically intermediate species between the two genera.
This broader circumscription of Castela was maintained by
Thomas (1990) and Majure etal. (2021b), although Clayton
(2011) considered two distinct genera. Also, it is important
to highlight the inclusion of Leitneria, formely in Leitne-
riaceae, endemic of the southeastern USA.
Thus, the circumscription of Simaroubaceae changed
drastically over the last few decades, but currently, they are
a highly supported monophyletic group composed of 22 gen-
era and approximately 120 species (Devecchi etal. 2021).
3 General morphology, withaccounts
onspecial anatomic traits
All Simaroubaceae species are woody, ranging from large
trees, up to 60 m as in Ailanthus, to treelets, shrubs and
subshrubs, these occasionally suffrutescent with the leaves
clustered at ground level, as seen in some dwarf species of
Homalolepis from Central Brazil. The latter are geophytes,
with apparently protective structures of cauline buds, as
prophylls and cataphylls, recently investigated through
morphoanatomical and histochemical techniques (Cortez
etal. 2021—this issue). A detailed structural analysis of the
underground system of these geophytic species is presented
by Melo-de-Pinna etal. (2021—this issue).
Thorns at the branch tips or axillary are present only in
the genus Castela. This taxon also demonstrates reduced,
simple leaves and generally green, photosynthetic stems,
which are often devoid of leaves, a feature likely related to
their occurrence in deserts, southern South American Chaco
vegetation and seasonally dry tropical forests, where they
are especially diverse in the Greater Antilles (Majure etal.
2021b—see this issue).
Detailed wood anatomy is described by Webber (1936),
Record and Hess (1943) and Metcalfe and Chalk (1950,
1972). All these authors refer that the only common charac-
ters to all species studied were vessels in a diagonal and/or
radial pattern; vessel outline circular to oval; simple perfo-
ration plates; and alternate intervessel pits. Webber (1936)
and O’Donnell (1937) also observed ring porous wood in
Picrasma and Ailanthus, and semi-ring-porous in Castela.
Vessel size or diameter is among the quantitative characters
useful to help distinguish wood of these latter three genera
(O’Donell 1937). Some genera may have rays exclusively
uniseriate (Picrasma, Quassia), while others are mostly 2–4
cells wide, but up to 7 cells wide rays are found in Castela
and Simarouba, or sometimes even more than 10 cells wide
in Ailanthus (Metcalfe and Chalk 1950). Besides the thorny
habit, Castela also diverges from all other genera of the fam-
ily studied so far mainly because the greatest part of their
wood consists of libriform fibers, rather than fibers with dis-
tinctly bordered pits (Webber 1936). Additionally, the spiral
thickenings observed in vessels of Castela and Leitneria are
rare or absent in the remaining taxa.
Solitary or clustered crystals are widespread in the family,
especially the latter type, and their size and distribution seem
to bear taxonomic relevance at the generic level; clustered
crystals are particularly large in Castela (Boas 1913; Met-
calfe and Chalk 1950).
Secretory canals are often present along vascular bundles,
and secretory cells occur in the cortex and pith. Either cells
and canals contains volatile oils and resins, but in smaller
amounts compared to the related families Rutaceae and
Meliaceae (Hegnauer 1983). The presence or absence of
medullary secretory canals seems to be a feature of generic
diagnostic value (Boas 1913; Heimsch 1942; Metcalfe and
Chalk 1950).
Hairs are mostly simple, unicellular or multicellular,
sometimes glandular-capitate (Boas 1913; Metcalfe and
Chalk 1950, 1972; Macedo etal. 2005); trichomes with
secretory basal cells were found in leaves of Quassia amara
L. (Macedo etal. 2005). Taxonomic relevance of the indu-
mentum is mostly related to variations in density and size of
trichomes at thespecies level (e.g., Engler 1874; Cronquist
1944b, c; Devecchi etal. 2018b). Glandular trichomes on
leaves of Ailanthus release a secretion with anunpleasant
smell that is repulsive to insects (Bory and Clair-Maczula-
jtys 1980). Trichomes are especially common in inflores-
cence axes, bracts and floral organs (e.g., Nair and Joshi
1958; Clayton 2011).
Leaves are alternate, spirally arranged, generally crowded
at apex of branches, mostly pinnately compound, seldom
simple (Castela, Leitneria) or unifoliolate (two species
of Simaba, with petiole pulvinate at apex). Leaflets are

An updated account ofSimaroubaceae withemphasis onAmerican taxa
1 3
alternate, opposite or subopposite, and the petiole and rachis
are distinctively winged in Quassia amara and slightly so in
Picrolemma Hook. f.
Stipules are mostly lacking, though stalked extrafloral
nectaries located at the base of the petiole of young leaves
of Ailanthus are interpreted as reduced stipules by Clair-
Maczulajtys and Bory (2011). Early caducous pseudostip-
ules are reported in some Picrasma (Weberling and Leen-
houts 1966).
The margin of the leaf or leaflet lamina usually is entire,
while serrate to crenate leaflets are conspicuous in Picrasma,
toothed in Ailanthus, and sometimes with pitted, concave, or
flattish glands (Ailanthus, Homalolepis, Picrolemma, Quas-
sia, Simaba, Simarouba). The marginal glands are mainly
located at the basal tooth in Ailanthus and were anatomically
studied by Bory and Clair-Maczulajtys (1990), who con-
sidered them as foliar nectaries acting as systems allowing
for the elimination of excess sugars, probably playing an
important role in the regulation of photosynthetic activity.
The tissue structure of these marginal nectaries is similar to
that of the stalked nectaries of the petiole (Clair-Maczulajtys
and Bory 2011). In the closely related Homalolepis, Simaba
and Simarouba, there are glandular structures on the leaf
blade; these may be located at the leaflet apex (either at the
very tip of the midvein or flanking it) or elsewhere; they
are usually immersed in the mesophyll and may be found
in both surfaces or only in the adaxial one (Metcalfe and
Chalk 1950; Devecchi etal. 2018a); these variable patterns
seem to bear taxonomic significance (Devecchi etal. in
prep.; Devecchi etal. 2018a). Particularly, the apical gland
located at the tip of the midvein is very conspicuous in leaf-
lets of almost all species of Homalolepis and Simaba, while
in Simarouba there are small glands flanking both sides of
the midvein distal portion (Devecchi etal. in prep.). Such
a remarkable feature is often mentioned in descriptions of
these plants in botany manuals and floras (e.g., Engler 1874,
1931; Franceschinelli and Thomas 2000; Thomas and Franc-
eschinelli 2005; Clayton 2011; Devecchi and Pirani 2016).
Like Simarouba, species of Quassia bear laminar glands
only toward the apex, and some extra-American taxa also
have leaf glands. Apical and laminar glands seem to function
as extrafloral nectaries in young leaflets, when ants are often
seen foraging on them (Devecchi etal. 2018a).
Very peculiar sclereids, generally crossing the mesophyll,
are found in several genera of Simaroubaceae (Boas 1913;
Engler 1931). The sclereids exhibit a wide range of form
and variations in thickness of the cell wall (Metcalfe and
Chalk 1950; Saraiva etal. 2002; Macedo etal. 2005). Franc-
eschinelli and Yamamoto (1993) described variation in form
and size of the sclereids among three continental species of
Simarouba and their usefulness in distinguishing them from
each other. Although quite conspicuous, they seem to lack
enough variation among species to subsidize taxonomy in
genera, such as Simaba and Homalolepis (e.g., Alves 2015).
Flowers are arranged in inflorescences that can be axil-
lary or terminal, bracteate. The most common types found in
the family are the thyrse and the thyrsoid, which is a deter-
minate thyrse and is much more widespread in the family.
Most other inflorescence types found in a few genera can be
interpreted as modifications from the basic thyrsoid. In Pic-
rasma, there are cymoids, which are more or less rounded,
modified thyrsoids; these are sometimes greatly reduced to
1–4-flowered inflorescences (Noa-Monzón 2020, Majure
etal. 2021a), which may be treated as botryoids or dep-
auperate thyrsoids. These latter pauciflorous inflorescence
types also characterize Simaba, while Quassia amara has
botryoids usually referred to as racemes in the literature.
Inflorescences in Castela are oftenvery reduced, pauciflor-
ous fascicles, solitary or clustered in leaf axils. The peculiar
catkin-like male inflorescences of Leitneria are pendulous or
erect (Schrader & Graves 2011) and have been interpreted as
reduced thyrses by anatomical studies (Abbe and Earle 1940;
Tobe 2013). Evolution of inflorescence types within the fam-
ily is discussed in Devecchi etal. (2018a) and especially in
Alves etal. (2021—this issue).
The flowers are generally small, pedicellate (sessile in
Leitneria), actinomorphic and mostly pentamerous. Even
though the majority of core eudicots families present a sta-
ble merism with a predominance of pentamerous flowers,
taxa from many families are more prone to meristic vari-
ations (Ronse De Craene and Smets 2016), as is the case
of Simaroubaceae. The presence of flowers either tetramer-
ous or pentamerous or occasionally hexamerous in a same
species is found in some genera (e.g., Ailanthus and Hom-
alolepis), and a hexamerous to octomerous perianth became
fixed in the Holacantha clade of Castela (sensu Majure etal.
2021b—this issue). There is anatomical evidence that flow-
ers of occasional tetramerous flowers of species of Hom-
alolepis maintain traces concordant with pentamery, since
one of the four petals has two vascular traces, indicating it
originated by the fusion of two petals (Alves etal. 2017).
Theperianth underwent an extreme reduction in Leitneria
female flowers, which lack petals and have vestigial sepals,
while male flowers are naked.
The calyx is gamosepalous at the base. Petals are free,
mostly imbricate, with cases of induplicate-valvate or val-
vate corolla, commonly pale green or white and less frequent
red, pink, orange and yellow, and usually haired. Quassia
amara has distinctive reddish flowers with an elongate, tubu-
lar corolla formed by coherent petals (e.g., Clayton 2011);
flowers in Homalolepis sect. Grandiflorae may be large, with
petals surpassing 3.5cm long, and stamens coherent by the
basal appendages of the filaments (Alves etal. 2017; Devec-
chi etal. 2018a, b).

J.R.Pirani et al.
1 3
The androecium is usually described as obdiplostemon-
ous in most simaroubaceous genera. In the Americas, only
Picrasma is haplostemonous (antesepalous stamens) and
Picrolemma is obhaplostemonous (antepetalous stamens, a
rare feature in angiosperms according to Ronse De Craene
and Smets 1995). Phylogenetic analysis and ancestral charac-
ter state reconstruction reveal lability in the stamen number
within the family, with pleiostemonous and haplostemonous
flowers having evolved a couple of times, independently,
from the typically diplostemonous pattern (Clayton etal.
2007; Alves etal. 2021—this issue). The obdiplostemony of
Ailanthus was considered to have resulted from the adnation
of the traces to petals and antipetalous stamens by Nair and
Joshi (1958). The current controversy on the nature of the
(ob)diplostemonous androecium in most rosids shows the
need for more developmental studies (e.g., Ronse De Craene
and Bull-Hereñu 2016; Alves etal. 2021—this issue).
Anthers are bithecal, dorsifixed or basifixed, often ver-
satile, usually introrse, dehiscing by longitudinal slits. In
Homalolepis, the anther wall has a uniseriate epidermis and
a conspicuous endothecial layer of columnar cells with lig-
nified secondary wall thickening forming trabeculae (Alves
etal. 2017).
Twelve out of the 22 genera of the family present a
laminar, adaxial appendage on the base of the filaments,
a remarkable feature. The staminal appendages vary in
length, pubescence and form of the apex, may be erect or
curved, and are taxonomic valuable. Engler (1931) defined
tribe Simaroubeae essentially on the basis of the presence of
appendaged stamens, and the phylogeny indicates that this is
a remarkable trait of a highly supported lineage containing
11 genera, four of which occur in the Neotropics: Quassia,
Simaba, Simarouba, and Homalolepis. This lineage holds
the highest number of species in Simaroubaceae, and only
two extra-American genera probably lost these appendages
(Alves etal. 2021—this issue). The appendages may be
slightly post-genitally coherent to each other by intertwin-
ing trichomes, in Simaba and especially in species of Hom-
alolepis sect. Grandiflorae, forming a “pseudotube” (Alves
etal. 2017; Devecchi etal. 2018a, b).
Staminodes are present in female flowers of several Sima-
roubaceae genera, but only three genera have staminodes
in male flowers, two of them American: Picrolemma and
Simaba. In the former genus, staminodes alternate with pet-
als and stamens are opposite the petals. In Simaba, rudi-
mental staminodes were recently detected forming a par-
tial whorl between the base of the petals and the stamens
(Devecchi etal. 2018a).
An intrastaminal disk is found in most genera, usually
nectariferous, as seen in most representatives of Sapindales
(the disk is extrastaminal only in Sapindaceae). In some
simaroubaceous genera, a disk is inconspicuous, and in
most of them, the nectariferous tissue is placed on the entire
surface of a small to conspicuously elongated and stout
gynophore (Alves etal. 2017), as in Quassia, Simarouba,
Simaba, Homalolepis, and likely also Picrolemma. The nec-
tary tissue at the periphery of the gynophore is vascularized
only by small phloematic bundles, and the nectar is released
through stomata found in depressions or at the same level as
the epidermis (Alves etal. 2017).
The gynoecium is formed predominantly by five carpels,
sometimes less or more. Amaroria and Leitneria are the
only two genera in the family with a single carpel, and six
to eight carpels occur in the Holacantha clade of Castela
(sensu Majure etal. 2021b—this issue). Carpels are gener-
ally antepetalous and dorsally bulged above the level of the
style base (hence anacrostylous) (Alves etal. 2017). Carpels
are completely free from each other (Picrolemma), or they
may be connate for a short extent at the base of the ovaries
(e.g., Homalolepis, Simaba), but most genera have carpels
partially and weakly united only by the styles (Nair and Joshi
1958; post-genital union, Alves etal. 2017). It is important
to highlight that the vascularization of each carpel remains
independent throughout the entire gynoecium; for example,
the style is vascularized by five bundles, each corresponding
to the dorsal bundle of the carpel with vascular bundles split-
ting into smaller bundles in the stigmatic region (Alves etal.
2017). Along the free (unfused) region of the ovary, carpels
remain tightly coherent, often by means of dense intertwin-
ing trichomes. After fertilization, styles and stigmas fall
down and carpels separate from each other forming fruit-
lets. Similar gynoecia with partially, postgenitally connate
carpels are common in other families of Sapindales (e.g.,
Endress etal. 1983; Ramp 1988). The post-genital fusion of
carpels in the apices of ovaries, as observed in most genera
of Simaroubaceae, is considered as evidence of a probable
derivation from a syncarpic ancestor (Endress etal. 1983;
Alves etal.2021—this issue).
The stigma shape varies from punctiform to lobate or
with elongate stylar lobes, which are separate and divergent
in several genera. Some studied stigmas have a papillose
secretory epidermis (e.g., Alves etal. 2017).
There is a single ovule per locule, and the placentation is
marginal. The ovule is anatropous or syntropous, suspended,
or sometimes amphitropous and suberect (Picrasma), biteg-
mic and crassinucellate (Corner 1976; Alves etal. 2017). In
Homalolepis, the inner integument of the ovule overgrows
the outer and forms the micropyle (Alves etal. 2017). Pis-
tillodes are found in male flowers of most genera that are
not hermaphroditic.
Regarding the sexual systems, Simaroubaceae are her-
maphroditic, monoecious, (sub)dioecious, or polygamous,
this latter condition being the most common, with the pres-
ence of dimorphic flowers where each morphotype has rudi-
mentary organs of the opposite sex, such as staminodes or
pistillodes. Among the American genera, Castela, Leitneria,

An updated account ofSimaroubaceae withemphasis onAmerican taxa
1 3
Picrolemma and Simarouba have distinctive unisexual flow-
ers in dioecious plants, a feature traditionally used in floristic
and taxonomic works to distinguish them from related gen-
era (e.g., Engler 1931; Cronquist 1944a, b, d; Pirani 1987b;
Thomas 1990; Clayton 2011). Male flowers in these five
genera present a very reduced to vestigial pistillode, and
small, sterile staminodes are found in female flowers. Quas-
sia is hermaphroditic, with bisexual flowers known to be
self-compatible (Roubki etal. 1985).
Among the remaining genera represented in the Ameri-
cas, there are controversial references and more field and
laboratory investigations are needed. Ailanthus and Picr-
asma are usually referred to either as monoecious and dioe-
cious (Nooteboom 1962; Clayton 2011), or polygamous
(e.g., Engler 1931). However, detailed studies revealed that
flowers of Ailanthus fomerly described as bisexual are in
fact female flowers whose staminodes are similar to fertile
stamens but smaller and not releasing pollen (e.g., Nair &
Joshi 1958; Alves etal.2021—this issue). Thus, it is prob-
able that only unisexual flowers, in monoecious or dioecious
species, occur in this genus, as described by Clayton (2011).
Conversely, Picrasma is traditionally referred to as an andro-
dioecious genus with hermaphroditic and staminate flowers
on separate plants (Thomas etal. 2011, Noa-Monzón etal.
2019, Majure etal. 2021a). In Homalolepis and Simaba, the
flowers are morphologically bisexual, and the genera were
described by some authors as hermaphroditic (e.g., Caval-
cante 1983). Nevertheless, their flowers may be functionally
bisexual or unisexual, either in polygamous plants (accord-
ing to Engler 1931; Clayton 2011), or incompletely dioe-
cious (according to Cronquist 1944b). This is supported by
recent findings of scattered flowers bearing abortive ovules
in some species of these two genera (Franceschinelli and
Thomas 2000; Alves etal. 2017; Devecchi etal. 2018a,
b). Flowers that are morphologically perfect but function-
ally unisexual are reported also to some extra-American
simaroubaceous genera, as well as in many other groups of
Sapindales [e.g., Meliaceae (Styles 1972; Franceschinelli
etal. 2015), Anacardiaceae and Burseraceae (Bachelier and
Endress 2009), Sapindaceae (Avalos etal. 2019) and Ruta-
ceae (Kubitzki etal. 2011)]. Evolutionary paths of sexual
structures and systems in Simaroubaceae and related fami-
lies are discussed in Alves etal. (2021—this issue) and in
Gama etal. (2021).
The fruit in Simaroubaceae is formed by one to five
drupaceous fruitlets, each one derived from a single carpel,
one-seeded, usually with a fleshy mesocarp, and less fre-
quently woody and fibrous or dry (Leitneria). Drupaceous
fruits are likely synapomorphic for the family (Stevenson
etal. 2002; Alves etal.2021—this issue). When mature, the
fruits are cream to red or purple-blackish, with abitter taste.
Sclereids are found in the epicarp, mesocarp and endocarp
(Fernando and Quinn 1992). As is common in drupelike
fruits, the endocarp constitutes the hard portion of the peri-
carp, and it is described as a broad homogeneous layer with
irregularly arranged isodiametric sclereids (Hartl 1958; Fer-
nando and Quinn 1992). Nevertheless, the endocarp is thin
in Homalolepis, while the mesocarp has a thick, fibrous and
hard layer (Devecchi etal. 2018a, b). Globose fruitlets seem
to be conservative in the family, but more specialized types
are also found. In some Simaba, drupelets may be strongly
laterally flattened (S. obovata Spruce ex Engl. and S. ori-
nocensis Kunth), or they are lenticular (Simaba guianensis,
Castela) or lenticular and flattened (Castela sp. nov.; Majure
etal. accepted). Samaroid fruitlets as those of Ailanthus are
rare in the family.
The seed has a thin, membranaceous but hard coat,
scanty endosperm, and a straight or curved embryo with
two large plane-convex cotyledons (Corner 1976; Stevens
2001). Detailed embryological data on some of the genera
represented in the Neotropics are provided by Wiger (1935),
Mauritzon (1935) and Narayana (1957).
4 Floral biology anddispersal
Entomophily prevails in most simaroubaceousgenera, whose
flowers are often reported to be fragrant and attract a wide
range of generalist insects, including bees and moths (e.g.,
Hardesty etal. 2005; Clayton 2011; Devecchi etal. 2018a).
However, floral diversity ranges from wind-pollinated
catkin-like inflorescences in Leitneria (Cronquist 1981)
to hummingbird-pollinated tubular red flowers in Quassia
amara (Roubik etal. 1985). In the several genera with larger
appendaged stamens, the nectar is concealed beneath those
structures, which in some species of Homalolepis may even
form a long staminal pseudotube. This is probably related
to restrictions of animal visitors, but pollination system
remains to be investigated.
Numerous species of bees and wasps were observed at
populations of Castela emoryi (A. Gray) Moran & Felger, a
desert species from Northern Mexico to Arizona and Cali-
fornia; as blooming occurs during hot mid-summer time,
when few other plants produce flowers, C. emoryi is believed
to be locally essential for those foraging insects (Bell and
Herskovits 2013).
The samaroid mericarps of Ailanthus disperse over small
distances by wind. Leitneria grows in freshwater and brack-
ish swamps, and as its fruits have anair chamber between the
seed and the endocarp, they fluctuate and are water dispersed
(Clayton 2011).
As drupaceous fruits prevail in the family, with a more or
less fleshy pericarp, animal dispersion is common. Ichtyo-
chory is reported to some species of Simaba, as S. obovata
and S. orinocensis, inhabiting Amazonian seasonally flooded
forests (“mata de várzea”) or permanently flooded (“mata

J.R.Pirani et al.
1 3
de igapó”). The drupelets of these two species are laterally
flattened and float on water; they have a fleshy and edible
mesocarp and are dispersed by fishes (Gottsberger 1978;
Honda 1974).
Drupelets of Homalolepis are subglobose and can be very
large, the largest ones in H. cedron (Planch.) Devecchi &
Pirani (up to 10cm long) and H. trichilioides (A.St.-Hil.)
Devecchi & Pirani (around 4cm long); their fruit wall is
very hard, with a thick, fibrous mesocarp, and only a few
animals can crack them, so it is likely that some rodentssuch
as agoutis are dispersers (Devecchi etal. (2018a, b).
As the fruits of Castela, Picrasma and Simarouba are
small, bird-dispersed drupelets, Clayton etal. (2009) sug-
gested that north–south dispersalmay be facilitated by
the migratory patterns of fruit-eating birds. Majure etal.
(2021b—this issue) likewise provided support for this
hypothesis, showing that the modern distribution of Castela
likely is the result of multiple long-distance dispersal events.
Drupaceous fruitlets of the widespread Simarouba amara
Aubl. are known to be vertebrate-dispersed, mainly by large
birds and mammals, including chachalacas, flycatchers, mot-
mots, thrushes, howlermonkeys and tamarins (Hardesty etal.
2006), and also by fruit-eating phyllostomid bats (Kelm etal.
2008). Leaf-cutter ants have been observed to disperse the
seeds of S. amara in Panama forests (Hardesty etal. 2005),
and also of S. versicolor A.St.-Hil. in the Brazilian cerrado
(Lopes etal. 2018). Seeds of S. amara that are eaten by
monkeys are more likely to germinate than seeds that have
not (Stevenson etal. 2002), as well as seeds of S. versicolor
cleaned by ants germinate faster than seeds with tegument
and seeds with tegument removed manually (Lopes etal.
2018). However, investigation of S. amara populations in
Panama revealed that the seed dispersal effectiveness by
leaf-cutter ants “appears to be ephemeral and likely con-
tributes inconsequentially to the long-term recruitment and
distribution patterns of the species” (Hardesty 2011).
5 Palynology
Studies on pollen morphology of Simaroubaceae are rela-
tively scarce. The available palynological data are mostly
based only on light microscopy, and pollen grains are con-
sidered relatively homogeneous, mostly isopolar, tricolpo-
rate, small or medium in sized, with lalongate endoapertures.
The pollen shape varies among the genera and also between
species of a genus, from oblate, oblate-spheroidal, prolate,
prolate-spheroidal to subprolate, and the surface pattern is
mostly finely to coarsely reticulate or sometimes verrucate
(Erdtman 1952; Basak 1963, 1967; Caccavari De Filice
and Villar 1980; Zavada and Dilcher 1986; Moncada and
Machado 1987; Moura etal. 2004; Clayton 2011; Cartaxo-
Pinto etal. in prep.). Cartaxo-Pinto etal. (in prep.) present
also SEM pollen analyses and describe five distinct pollen
types based mainly on sexine sculpture.
A survey on pollen morphology of the Sapindales elabo-
rated by Gonçalves-Esteves etal. (2021—this issue) presents
data from 15 genera of Simaroubaceae, including the 10
genera represented in the Americas.
It is noteworthy to highlight that pollen morphology pro-
vides important characters for the taxonomy of the family.
For instance, pollen data supported the exclusion of Kirkia
from Simaroubaceae, erected as Kirkiaceae (Erdtman 1952,
1986), as well as they helped to refute Nooteboom’s pro-
posal (1962) to merge some genera in Quassia sl. (Basak
1967).
6 Chromosome numbers
A survey of chromosome numbers and their evolutionary
significance in Sapindales includes published and original
data on Simarubaceae taxa (Guimarães and Forni-Martins
2021—this issue). Although basic chromosome numbers of
8–13 were reported by Stevens (2001 onwards), there is a
probable range of chromosome number in Simaroubaceae
of 7–16.
Karyotypes are known only for a few genera. In Leitneria,
the basic number is X = 16 (Raven 1975), and in Castela
coccinea 2n = 26 (Bernardello etal. 1990). For Simarouba,
the basic number reports are variable: S. amara has X = 16
(Guimarães 2017), while in S. glauca there are two distinct
reports: X = 16 (Bawa 1973), and X = 15 (Baratakke and
Patil 2010). Polyploid numbers are reported in Ailanthus
altissimus with 2n = 80 (Desai 1960), and to Ailanthus integ-
rifolia with 2n = 64, which is probably an octoploid (Bennett
and Leitch 2005a, b). In Homalolepis arenaria (Devecchi
& Pirani) Devecchi & Pirani, H. bahiensis (Moric.) Devec-
chi & Pirani, H. floribunda (A.St.-Hil.) Devecchi & Pirani
and H. warmingina (Engl.) Devecchi & Pirani, chromo-
some numbers 2n = 32 were found by Romero-da-Cruz etal.
(2021—this issue), who also present additional cytogenetic
data for this genus, which allowed the inference of a caryo-
typical history for Simaroubaceae.
7 Chemistry
Plants of Simaroubaceae have long been characterized in
the literature by their bark with bitter taste, with several
medicinal uses. Such bitter principles are quassinoids,
which are triterpenoid derivatives, biosynthetically related
to the limonoids of Rutaceae and Meliaceae (Dreyer 1983;
Waterman 1983; Silva and Gottlieb 1987). Quassinoids are
present throughout vegetative tissues and are also present in
the fleshy fruits of most genera. Furthermore, the exclusive

An updated account ofSimaroubaceae withemphasis onAmerican taxa
1 3
presence of the quassinoids is a putative chemical synapo-
morphy of the family (Fernando etal. 1995; Stevens 2001).
Bitter principles widely known in Simaroubaceae
are quassin isolated from Quassia amara and Picrasma
excelsa (Sw.) Planch., glaucarubin isolated from seeds of
Simarouba glauca DC., cedrin from seeds of Homalolepis
cedron (Planch.) Devecchi & Pirani (as Simaba cedron)
(Gibbs 1974). However, a single genus, such as Picrasma,
may produce 35 different structural types (Silva and Gottlieb
1987). The common structure to these substances is the lac-
tone function and the isoprenoid structure (sesquiterpens or
diterpens), and so they are related to the limonoids typical
of Rutaceae, whose carbonskeleton is based on triterpenes
however (Gibbs 1974).
Those authors reviewed the information regarding the
chemistry of the main genera of the family. Besides the
quassinoids, secondary metabolites reported for several
genera in the family include alkaloids, mostly tryptophan-
derived, coumarins, flavonols, flavones, flavonol glycosides
and glycoflavons, and small amounts of volatile oils (e.g.,
Hegnauer 1983), and also canthinones and β-carbolines
(Simão etal. 1991). Proportions of secondary metabolites
isolated from species of Simaba and Homalolepis by Bar-
bosa etal. (2011) were identified as quassinoids (34.5%),
triterpenes (17.7%), alkaloids (16.8%) and others (31%:
coumarins, steroids, phenolic compounds, anthraquinones,
organic acid, flavonoid, essential oil and lignans).
Simão etal. (1991) suggested that a “specialization of
quassinoid skeletons is accompanied by a West to East spa-
tial radiation of the simaroubaceous lineage.” According to
them, a diversification of oxygenation and unsaturation pat-
terns, and an increase in oxidation level of the quassinoids,
are observed as one compares taxa from the Americas and
West Africa to the East African and Asian genera.
8 Biogeography andecology
Simaroubaceae are a mostly pantropical family, but include
some subtropical and temperate elements. Among the Amer-
ican genera, Castela and Picrasma include one or more sub-
tropical species, while only Leitneria is warm temperate and
Ailanthus altissimus temperate.
The primary center of diversity of Simaroubaceae (in
number of species) is found in the Neotropical region, with
over half (65) species grouped in ten genera. Other species-
rich areas are West Africa, Asia and Australasia (Clayton
2011). Brazil is home to a great diversity of Simaroubaceae,
consisting of 36 species in seven genera of which 21 are
endemic (Devecchi etal. 2020). Although forming a very
minor part of the distribution of the family, the Greater
Antilles also are a hotspot for the family, with at least 16
species occurring there, 13 of those endemics (Majure etal.
2021b—this issue). Distribution maps of the American gen-
era are depicted in Figures1, 2, 3, 4, 5, 6, 7, 8, 9.
Nine genera are monospecific or with only two species,
with restricted distribution. Among these, only Leitneria and
Quassia occur in the Americas. The largest genus is Hom-
alolepis, with 28 species, exclusively neotropical. Quassia
and Picrasma are the only American genera that also occur
disjunctly in other continents. Some remarkable disjunct pat-
terns are also present within the Americas, the most expres-
sive shown by species of Castela and Picrasma, found in
Central America and the West Indies (and occasionally in
northernmost South America), as well as in southern South
America (Figs.1g and 4f) (Thomas 1990); Castela also is
found in western North American deserts, where it likely
originated (see Majure etal. 2021b—this issue).
A few species are widespread throughout tropical Amer-
ica, as Homalolepis cedron and Simarouba amara, the latter
also with dense populations, but the former is more rare.
Most species show a more restricted distribution, and there
are some microendemics (e.g., Castela macrophylla Urb.,
Picrasma longistaminea W. Palacios, Homalolepis pumila
Devecchi and Pirani, and at least seven other species of the
later genus).
Simaroubaceae as a lineage probably diverged from the
larger families of Sapindales during the Late Cretaceous
(Clayton etal. 2009; Muellner-Riehl etal. 2016), and the
crown-group Simaroubaceae are dated to approximately 65
Ma, in the Cretaceous-Maastrichian (Clayton etal. 2009).
Although the remarkable disjunct pantropical distribution
of the family could suggest vicariance events related to
continental split, the dates of divergence of several clades
revealed that multiple recent range shifts through long-dis-
tance dispersal might have also occurred. Simaroubaceae is
likely to have a North American origin with an early history
of range expansion between major continental areas in the
Northern Hemisphere, including migration via Beringia by
ancestral taxa. Long-distance dispersal events probably took
place particularly in the Late Oligocene and later, includ-
ing dispersals across the Atlantic Ocean in both directions,
as well as between Africa and Asia, and around the Indian
Ocean basin and Pacific islands (Clayton etal. 2009).
The family is a geographically widespread and ecologi-
cally diverse, but mainly found in moist lowland tropical for-
ests, including Amazonian seasonally flooded forests (some
Simaba). They also inhabit seasonally dry (semi)deciduous
forests, subandean montane forests, highland vegetation at
the Guyana Shield, open savannas, sandy habitats as coastal
restingas in Eastern Brazil, swamp forests (only Leitneria),
and deserts and dry scrubs in northwestern Mexico and
southwestern USA (Castela). The latter genus consists of
thorny plants, and leaves are generally rudimentary in sev-
eral species. Homalolepis is remarkable for its broad habit
span, from tall, sometimes palmlike forest trees, to shrubs

J.R.Pirani et al.
1 3
and small subshrubs inhabiting South American savannas,
including eight geophytic species, which are dwarf plants
provided with a woody underground perennial axis, with
a less persistent aerial system that can be deciduous and
resprout, the leaves usually clustered at the soil surface.
This geophytic life-form seems to have evolved at least three
times independently among the members of Homalolepis
(Devecchi etal. 2018a), including distinct structural varia-
tions of the underground system as shown by Melo-de-Pinna
etal. (2021—this issue).
9 Ethnobotany/economic uses
Wood and bark of several species of Simaroubaceae yield
bitter principles—the quassinoids—traditionally employed
as therapeutic agents and thus, are used locally as medicinal
plants. According to Alves etal. (2014), the quassinoids are
“secondary metabolites responsible for a wide spectrum of
biological activities such as antitumor, antimalarial, antivi-
ral, insecticide, feeding deterrent, amebicide, antiparasitic
and herbicidal.” Other properties include antidysenterics and
antihelmintics. The main study about antimalarial properties
of the quassinoids of Homalolepis cedron (as Simaba cedron)
was elaborated by O’Neill etal. (1986). Almeida etal. (2007)
add to these the antineoplastic property. Invitro anthelmintic
activity of Picrolemma sprucei Hook.f. was demonstrated
(Nunomura etal. 2006), and the antiplasmodial activity of
the same species was due presumably to quassinoid and non-
quassinoid active components (Amorim etal. 2013). Members
of the family are included in official compendia, as Brazilian,
British, French and German pharmacopoeias, and some patent
registrations have been made (Alves etal. 2014). However,
only a few species have been studied in detail and more phy-
tochemical and pharmacological investigations are needed.
Several species produce timber of local importance for
various purposes (Record & Hess 1943), and some of them
are exported. A few species are cultivated and planted as
ornamentals, as the “Tree of Heaven” (Ailanthus altissimus
(Mill.) Swingle), the “Surinam Quassia” (Quassia amara L.)
and the “Paradise Tree” (Simarouba glauca DC.) (Brizicky
1962; Clayton 2011).
Bark extracts from species, such as Quassia amara and Pic-
rasma excelsa (Sw.) Planch., are traditionally used as flavoring
in drinks.
Fig. 1 Castela—a–f C. tweediei Planch. a Flowering twig, b male flower in lateral view, c male flower in front view, d female flower, e a fruit
with two fruitlets and a small one aborted, f longitudinal section of a fruitlet, g distribution map of the genus (a–f modified from Pirani 1997)

An updated account ofSimaroubaceae withemphasis onAmerican taxa
1 3
Fig. 2 Homalolepis—a Habit of H. arenaria, b Habit of H. pumila Devecchi & Pirani, c Leaflet of H. arenaria, d Leaflet apical gland of H.
arenaria, e Flower at anthesis of H. cedron, f Stamen in ventral and dorsal views of H. cedron, g Gynoecium on top of a long gynophore of H.
cedron, h Longitudinal and transverse section of the gynoecium of H. guajirensis Devecchi, Thomas & Pirani, i. Longitudinal section of a fruit-
let of H. guajirensis, j Distribution map of the genus (a, c, d modified from Devecchi etal. (2016), b from Devecchi etal. (2018c), e–g from
Devecchi etal. (2018b), h, i from Devecchi etal. (2018d)
Fig. 3 Leitneria floridana—a
elongate male catkins, b male
flower, c stamen, d female
flower, e fruits, f longitudinal
section of a fruitlet, g distribu-
tion map of the genus (a–f
modified from Hooker 1867)

J.R.Pirani et al.
1 3
10 Brief taxonomic account ofAmerican
taxa (native andnaturalized)
Simaroubaceae DC., nom. cons., Nouv. Bull. Sci. Soc. Phi-
lom. Paris sér.2: 209. 1811, as Simarubae. Type: Sima-
rouba Aubl., nom. cons.
Key to the native and naturalized genera occurring in
the Americas
1. Fruit with samarids (winged fruitlets); leaves pinnately
compound with a conspicuous gland at the basal lobes of
proximal leaflets ………….… 9-Ailanthus (naturalized)
1′. Fruit with drupaceous fruitlets; leaves absent, or sim-
ple, or reduced to scales, or seldom unifoliolate, when pin-
nately compound with leaflets without glandular basal lobes
… 2
2. Flowers lacking a perianth or this vestigial, surrounded
by large bracts … 3-Leitneria
Fig. 4 Picrasma—a–e—P.
excelsa: a flowering twig, b
male flower, c male flower in
longitudinal section, d female
flower, e fruit, f distribution
map of the genus (a–c modified
from Engler 1897; d, e from
Fawcett and Rendle 1920)
Fig. 5 Picrolemma sprucei—a
fruiting twig, b detail of the
hollow stem, c male flower in
lateral and front view, d female
thyrsoid, e fruit, f distribution
map of the genus (Artwork:
Klei Souza)

An updated account ofSimaroubaceae withemphasis onAmerican taxa
1 3
2. Flowers with conspicuous calyx and corolla; bracts
small, not surrounding the flowers ……. 3
3. Leaf pinnately compound, rachis winged and articu-
late …………. 6-Quassia.
3′. Leaf pinnately compound but the rachis nor winged
nor articulate, or leaves simple, or reduced to scales, or
seldom unifoliolate, or absent ………… 4.
4. Flowers isostemonous ................. 5.
4′. Flowers diplostemonous ……… 6.
5′. Twigs hollow, inhabited by ants; stamens oppo-
site to the petals; inflorescence elongate, pyramidal in
shape; styles distinct at anthesis; fruitlets ellipsoid …….
5-Picrolemma.
5. Twigs solid, not hollow, not inhabited by ants; stamens
alternate with the petals; inflorescence broad and rounded,
often (sub)corymbiform; styles united at anthesis; fruitlets
globose ………… 4-Picrasma.
6. Plants unarmed; leaves pinnately compound, seldom
scattered unifoliolate leaves present; stamens with append-
age fillaments ................ 7.
6′. Plants commonly armed with conspicuous thorns;
leaves simple or reduced to scales or absent; stamens with
unappendaged filaments ……. 1-Castela.
7. Leaflets alternate or occasionally subopposite with
laminar glands immerse at the blade adaxial surface; flowers
unisexual, style shorter than the elongate, linear, divergent
stigmas ……… 8-Simarouba.
7′. Leaflets (sub)opposite or sometimes unifoliolate with
an apical gland at the end of the midvein and laminar glands
immerse in the mesophyll; flowers bissexual (though some
may bear sterile stamens or sterile ovary in some species);
style longer than the small stigmas …………. 8
8. Leaflet laminar glands only on adaxial surface; vegeta-
tive and reproductive organs bearing only tector trichomes;
anthers with connective smooth; stigmas short-divergent
……………… 7-Simaba.
8′. Leaflet laminar glands often on both surfaces; veg-
etative and reproductive organs bearing tector and often
also glandular trichomes; anthers with connective papil-
late; stigma punctiform to slightly lobed ………………….
2-Homalolepis
1. Castela Turpin, Ann. Mus. Natl. Hist. Nat. 7: 78. 1806.
Figure1
Holacantha A Gray, Pl. Nov. Thurb. 310. 1854.
Small trees or shrubs, armed with axillary thorns or
branches terminating in multibranched thorns, leaves sim-
ple (although sometimes lobed or toothed), these some-
times reduced to scales or lacking, lacking apical and lami-
nar glands. Dioecious. Flowers in small axillary fascicles
to larger, dense axillary thrysoids. Petals 4(5–8); stamens
Fig. 6 Quassia amara—a flowering twig, b floral bud, c flower with the petals omitted, d Gynoecium, e Stamen in dorsal and ventral view, f
Fruit, g Distribution map (a–f modified from Engler 1897)

J.R.Pirani et al.
1 3
8(10–16), filaments unappendaged; carpels 4(5–8) weakly
united only at the styles, on a short gynophore, stigma
branches linear, divergent. Fruit with free, lenticular, len-
ticular-flattened or subovoid drupelets.
Sixteen species, in disjunct edaphically dry areas: in
southwestern USA and northern Mexico (including Baja
California), West Indies, northern South America includ-
ing Ecuador and Peru, the Galapagos Islands and southern
South America (Bolivia, Paraguay, Uruguay, Argentina and
southwestern Brazil). There are endemic species in most of
these areas; only one species, C. erecta, is widespread.
Revision: Cronquist (1944a, d, 1945).
Phylogenetic relationships (Clayton etal. 2007): Castela
emerged as sister to Holacantha, in a clade which also
included Picrasma. Majure etal. (2021a) and Majure etal.
(2021b—this issue) recovered Castela s.s. as sister to the
Holacantha clade, all of which were sister to the rest of
Simaroubaceae.
2. Homalolepis Turcz., Bull. Soc. Imp. Naturalistes Mos-
cou 21(1): 575. 1848.
Figure2; see also the illustrated Field Guide by Devecchi
etal. (2018e)
Trees, shrubs or dwarf geophytes. Leaves pari- or
imparipinnate, leaflets mostly opposite, occasionally with a
conspicuous apical nectariferous gland, laminar glands scat-
tered usually on both surfaces. Hermaphroditic or polyga-
mous. Flowers in (sub)terminal many-flowered thyrsoids or
thyrses. Petals (4)5(6). Stamens (8)10(12), filaments append-
aged at base; carpels (4)5 weakly united, on a conspicuous
gynophore, stigma punctiform or slightly lobed. Fruit with
1(5) free, (sub)globose to obovoid or ellipsoid drupelets.
Species of this genus were traditionally treated as Simaba
(e.g., Engler, 1874; Cronquist 1944c; Clayton 2011). A
phylogenetic analysis showed that Simaba s.l. is not mono-
phyletic and hence, Homalolepis was reinstated (Devecchi
etal. 2018a, b). As currently circumscribed, Homalolepis
comprises 28 species mainly distributed throughout tropical
South America, except for Chile and Uruguay, with most
species in open formations of Central Brazil (cerrados).
Eight species are geophytes. The widespread species H.
cedron ranges from southeastern Brazil to northern South
America and Costa Rica and El Salvador in Central Amer-
ica. Moist forests to seasonally dry forests, cerrado (savanna)
and restinga (coastal sandy formation).
Revision: Devecchi etal. (2018b).
Phylogenetic relationships: In Clayton etal. (2007,
updated by Alves etal.2021—this issue)) the sister group
relationships are: ((Simaba, Homalolepis) (Simarouba,
Fig. 7 Simaba—a Flowering twig of S. guianensis, b Leaflet with marginal laminar glands of S. guianensis, c Flower with a petal and four sta-
mens removed showing the gynoecium of S. pubicarpa Devecchi, Franceschinelli & Thomas, d Stamen in dorsal and ventral view of S. guianen-
sis, e Gynoecium of S. guianensis, f Fruiting branch of S. orinocensis, g Fruit of S. orinocensis, h Transversal section of a fruitlet of S. orinocen-
sis, i Distribution map of the genus (a modified from Thomas (1985), b from Devecchi 2017, c–e from Devecchi etal. 2021, f–h by Klei Souza)

An updated account ofSimaroubaceae withemphasis onAmerican taxa
1 3
Fig. 8 Simarouba amara—a imparipinnate leaf, b male flower, c female flower, d fruit with four fruitlets, e distribution map of the genus (a, b
modified from Devecchi & Pirani 2016, c, d from Pirani 1987b)
Fig. 9 Ailanthus altissimus—a flowering twig, b male flower, c female flower, d fruit, e distribution map (a–d modified from Takhtajan 1981)

J.R.Pirani et al.
1 3
Pierreodendron)). According to Devecchi etal. (2018a,
b), Homalolepis emerges as sister to Simarouba, in a clade
which includes also Simaba s.s.
3. Leitneria Chapm., Fl. South. U.S. 427. 1860.
Figure3
Treelets with simple leaves, lacking apical and laminar
glands. Dioecious. Flowers solitary (female) or in catkin-like
thyrsoids (male). Hermaphroditic or polygamous. Perianth
lacking (male flowers) or vestigial (female flowers), sur-
rounded by large bracts. Stamens (1)4, filaments unappend-
aged; carpel 1, stigma elongate; disk and gynophore lacking.
Fruit a narrowly ellipsoid drupe.
A genus endemic to southeastern USA, traditionally rec-
ognized as monospecific (Leitneria floridana Chapm.) until
a second species, L. pilosa Shrader & Graves was described
in 2011. Both inhabit swamp forests.
Phylogenetic relationships (Clayton etal. 2007): Leitneria
emerges as sister to a clade formed by three extra-American
genera (Brucea, Soulamea and Amaroria).
4. Picrasma Blume, Bijdr. Fl. Ned. Ind.: 247. 1825.
Figure4
Aeschrion Vell., Fl. Flum. 58. 1825.
Trees or treelets. Leaves imparipinnate, leaflets (sub)
opposite, lacking apical and laminar glands. Monoecious,
dioecious or polygamous (androdioecious). Flowers in
broad, rounded cymoids (modified thyrsoids) or reduced
cymes with 1–4 flowers. Petals (4)5. Stamens (4)5, alternate
with the petals, filaments unappendaged; carpels (2)4–5 dis-
tinct but united by the styles, on a conspicuous gynophore or
surrounded by an intrastaminal disk, stigma branches linear,
divergent. Fruit with 1–3(5) free, globose drupelets.
Eleven species, two of which occur in Asia; one spe-
cies found in southern and eastern South America, and
the remaining distributed from northern South America to
Mexico and the West Indies. There are species endemic to
Ecuador, Cuba, Dominican Republic and Mexico. Moist to
semideciduous, lowland or submontane forests, although two
species occur in seasonally dry tropical forest (Noa-Monzón
etal. 2020; Majure etal. 2021a).
Revision: Cronquist (1944d); three species described
later: P. longistaminea W. Palacios, from Ecuador, P. pauci-
flora A.Noa & P.A.González, from Cuba, and P. nanophylla
Majure & Clase, from Dominican Republic.
Phylogenetic relationships (Clayton etal. 2007): Picr-
asma emerges as sister to a clade formed by Castela + Hola-
cantha (Castela s.l.) or as sister to the rest of Simaroubaceae
after Castela s.l. (Majure etal. 2021a, 2021b—this issue).
5. Picrolemma Hook.f., Gen. Pl. 1: 312. 1862.
Figure5
Slender shrubs with hollow stems (myrmecophytes) and
imparipinnate leaves, leaflets mostly opposite without a
gland at the leaflet apex, laminar glands present only on
abaxial surface. Dioecious. Flowers in elongate, narrow
or broad pyramidal thyrsoids. Petals (4)5; stamens (4)5,
opposite to the petals and alternate with small staminodia,
filaments unappendaged; carpels (4)5, distinct, each with a
terminal style, on a conspicuous gynophore, stigma capitate.
Fruit with 1–2 free, ellipsoid drupelets.
This genus comprises two Amazonian rainforest species,
P. huberi Ducke found in Colombia, Ecuador and Peru, and
P. sprucei Hook.f. widespread throughout lowland Amazo-
nia, from Brazil, Ecuador, French Guiana, Guyana and Peru
to Venezuela.
Revision: Cronquist (1944d).
Phylogenetic relationships: According to Clayton etal.
(2007), Picrolemma emerges as sister to the large clade
formed by 11 genera, most with staminal appendages (only
two extra-American genera have unappendaged stamens).
According to Devecchi etal. (2018a), it is sister to Quassia,
with strong support.
6. Quassia L., Sp. Pl. (ed. 2) 1: 553. 1762.
Figure6
Shrubs or treelets with imparipinnate leaves, the petiole
and rachis winged; leaflets opposite, without a gland at the
leaflet apex, laminar glands present only on adaxial surface,
toward the apex. Hermaphroditic. Flowers in narrow thyr-
soids or botryoids. Petals 5; stamens 10, filaments append-
aged at base; carpels 5, weakly united by the styles, on a
short gynophore, stigma capitate or slightly lobed. Fruit with
1–2 drupelets.
Two species, one in tropical West Africa, other neotropi-
cal (Q. amara L.) from northern South America north to
Nicaragua and the West Indies. As the latter species has
been widely used as a medicinal plant, and cultivated and
naturalized, its natural distribution is difficult to determine
with confidence. It is found mainly in lowland rainforests.
Revision: Cronquist (1944d).
Phylogenetic relationships (Clayton etal. 2007, updated
by Alves etal. 2021—this issue): Quassia emerges as the
early diverging member of a clade of 11 genera mostly pro-
vided with staminal appendages (only two extra-American
genera have unappendaged stamens). According to Devecchi
etal. (2018a), it is sister to Picrolemma, with strong support.
7. Simaba Aubl., Hist. Pl. Guiane 1: 400. 1775.
Figure7
Trees or shrubs with imparipinnate or seldom unifoliolate
leaves (petiole pulvinate at apex); leaflets (sub)opposite, usu-
ally with an inconspicuous nectariferous gland present at the
apex and laminar glands scattered only on adaxial surface.
Hermaphroditic or polygamous. Flowers in depauperate
thyrsoids to botryoids. Petals (4)5(6); stamens (8–)10(–12),
filaments appendaged, vestigial staminodes; carpels (4)5,
weakly united by the styles up to the slighlty lobed stigma.
Fruit with 1–5 free, lenticular to obovoid drupelets.
In its current circumscription, Simaba s.s. comprises
about ten mostlyAmazonian species (Devecchi etal. 2018a,

An updated account ofSimaroubaceae withemphasis onAmerican taxa
1 3
b). They are concentrated at northern South America, with
only two disjunct occurrences, one in the Atlantic forest in
northeast of Brazil, and the other in the Caribbean coast of
Panama (Devecchi and Pirani, subm.). They inhabit mainly
lowland flooded and non-flooded forests, and also highland
Amazonian savanas and the Guiana Shield.
Revision: Cronquist (1944c); Cavalcante (1983).
Phylogenetic relationships: According to Devecchi etal.
(2018a, b), Simaba s.s. emerges as sister to a clade formed
by Homalolepis + Simarouba. In Clayton etal. (2007,
updated by Alves etal. 2021—this issue)) the sister group
relationships are: ((Simaba, Homalolepis)(Simarouba,
Pierreodendron)).
8. Simarouba Aubl., Hist. Pl. Guiane 2: 859. 1775.
Figure8
Trees or shrubs with leaves pari- or imparipinnate, persis-
tent; leaflets alternate or occasionally subopposite, with lam-
inar glands scattered on adaxial surface Dioecious. Flowers
in many-flowered thyrsoids. Petals (4)5; stamens (8)10, fila-
ments appendaged at base; carpels (4)5, weakly united only
by the short styles, on a short gynophore, stigmas long and
divergent. Fruit with 1–3 free, ovoid or ellipsoid drupelets.
A genus of six species, found from Florida (United
States), Mexico and the Greater Antilles to Bolivia and
southeastern Brazil. Three clearly distinct species are each
endemic to one of the Greater Antilles: Cuba, Hispaniola
and Puerto Rico; one species is found primarily in Mexico
and Central America (S. glauca); one is restricted to South
America (S. versicolor), and one is broadly distributed from
tropical South America to Guatemala and Belize (S. amara).
Revision: Cronquist (1944b).
Phylogenetic relationships: According to Clayton etal.
(2007, updated by Alves etal.2021—this issue), the rela-
tionships are: ((Simaba, Homalolepis) (Simarouba, Pierreo-
dendron)). In Devecchi etal. (2018a, b), Pierreodendron was
not sampled and the hypothesis is (Simaba (Homalolepis,
Simarouba)).
9. Ailanthus altissimus (Miller) Swingle - a nonative,
naturalized and invasive species.
Figure9.
Trees with leaves pari- or imparipinnate, deciduous;
leaflets usually (sub)opposite, with conspicuous glands at
the tip of the basal lobes of proximal leaflets. Polygamous-
dioecious. Flowers in many-flowered thyrses. Petals 5(6);
stamens (5)10(12), filaments unappendaged; carpels 5(6)
weakly united only by the styles, stigma branches peltate and
divergent. Fruit with 1–5 free, oblong samarids, each with
a flattened seed at the middle of the membranaceous wing.
Commonly known as the “Tree of Heaven”,— this species
was introduced from China in North America in 1784, where
it is cultivated but escaped and became naturalized through-
out most of the USA (from northern Florida and northward)
(Hu, 1979). It is occasionally cultivated in Southern South
America (Argentina, Bolivia, Chile and south Brazil), and
it has become naturalized in some parts of Argentina and
Chile. Plants of A. altissimus are polyploid (2n = 80, Desai,
1960) and, once established, they become very difficult to
eradicate, for they can sprout from the stumps and on any
portion of a root, and also because a female tree is a prolific
seed producer; its winged fruits spread and germinate nearby
and far away from the mother plant (e.g., Hu 1979). For
these reasons, the species is considered as a weedy tree, an
aggressive colonizer of disturbed habitats such as old fields,
forest edges, and roadsides and also invades undisturbed
habitats, suppressing growth of surrounding plants through
release of allelopathic compounds (e.g., Brizicky 1962).
Five species are currently accepted in Ailanthus, a genus
originally distributed in northeastern to southern Asia to
northern Australia (Clayton 2011).
Phylogenetic relationships: According to Clayton etal.
(2017), Devecchi etal. (2018a, b) and Majure etal. (2021b)
the genus Ailanthus emerges as sister to a clade formed by
all genera of the family except for Castela and Picrasma.
Acknowledgements We thank the following Brazilian agencies for
financial support: Coordenação de Aperfeiçoamento de Pessoal de
Nível Superior (CAPES Processo n° 88882.315503/2019-01) for a
grant to MF Devecchi; Fundação de Apoio à Pesquisa do Estado de
São Paulo (FAPESP Process 2014/18002-2 - Sapindales thematic pro-
ject); Conselho Nacional de Desenvolvimento Científico e Tecnológico
(CNPq), for a research grant to JR Pirani (307655/2015-6).
Author’s contributions Conceptualization was contributed by JRP and
MFD; formal analysis and investigation were contributed by JRP, LCM
and MFD; figures were contributed by MFD; writing—original draft
preparation, was contributed by JRP and MFD; writing—review and
editing, was contributed by JRP, LCM and MFD; funding acquisi-
tion was contributed by JRP; supervision was contributed by JRP. All
authors commented on previous versions of the manuscript, and read
and approved the final manuscript.
Declarations
Conflict of interest No potential conflict of interest was reported by
the authors.
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