ArticlePDF Available

Abstract and Figures

With ca. 2500 species, Myrteae is the largest tribe of Myrtaceae and one of the most diverse groups of flowering plants in the tropical Americas. In light of recent systematics adjustments, the present study is a review and provides new insights into floral diversity and evolution in Myrteae. General aspects of floral ontogeny and morphology for the fifty currently accepted genera plus all accepted sections within the large genera Eugenia and Myrcia are summarized based on current morphological data. The discussion provides a broader understanding of the floral diversity across the tribe, highlighting developmental modes, ecological traits, and specializations in reproductive strategies. Hypotheses to be tested in future studies are also presented and discussed.
Content may be subject to copyright.
BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access
titles in the biological, ecological, and environmental sciences published by nonprofit societies,
associations, museums, institutions, and presses.
Your use of this PDF, the BioOne Complete website, and all posted and associated content indicates
your acceptance of BioOne’s Terms of Use, available at www.bioone.org/terms-of-use.
Usage of BioOne Complete content is strictly limited to personal, educational, and non-commercial use.
Commercial inquiries or rights and permissions requests should be directed to the individual publisher
as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit
publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical
research.
A Systematic Overview of the Floral Diversity in Myrteae (Myrtaceae)
Authors: Thais N. C. Vasconcelos, Gerhard Prenner, and Eve J. Lucas
Source: Systematic Botany, 44(3) : 570-591
Published By: The American Society of Plant Taxonomists
URL: https://doi.org/10.1600/036364419X15620113920617
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Systematic Botany (2019), 44(3): pp. 570591
© Copyright 2019 by the American Society of Plant Taxonomists
DOI 10.1600/036364419X15620113920617
Date of publication August 6, 2019
A Systematic Overview of the Floral Diversity in Myrteae (Myrtaceae)
Thais N. C. Vasconcelos,
1,2,3
Gerhard Prenner,
1
and Eve J. Lucas
1
1
Jodrell Laboratory, Comparative Plant and Fungal Biology Department, Royal Botanic Gardens Kew, Richmond, Surrey, UK
2
Departamento de Botˆanica, Instituto de Biociˆencias, Universidade de S~
ao Paulo, S~
ao Paulo, Brazil
3
Author for correspondence (thais.nogales@gmail.com)
Communicating Editor: Luciano Paganucci Queiroz
AbstractWith ca. 2500 species, Myrteae is the largest tribe of Myrtaceae and one of the most diverse groups of flowering plants in the tropical
Americas. In light of recent systematics adjustments, the present study is a review and provides new insights into floral diversity and evolution in
Myrteae. General aspects of floral ontogeny and morphology for the fifty currently accepted genera plus all accepted sections within the large genera
Eugenia and Myrcia are summarized based on current morphological data. The discussion provides a broader understanding of the floral diversity
across the tribe, highlighting developmental modes, ecological traits, and specializations in reproductive strategies. Hypotheses to be tested in future
studies are also presented and discussed.
KeywordsAndroecium, evolution, gynoecium, perianth, morphology, ontogeny.
Myrtaceae are a large angiosperm family, half of the bio-
diversity (ca. 2500 species; WCSP 2018) occuring within the
monophyletic tribe Myrteae (sensu Wilson et al. 2005). Myr-
teae species are distributed in both the Paleotropics and the
Neotropics, with a more expansive diversity (ca. 2000 species)
in the latter. This tribe comprises some of the highest diversity
of tree species in South American forests and savannas
(Oliveira-Filho and Fontes 2000; Françoso et al. 2016; Beech
et al. 2017; Cardoso et al. 2017), where it has a critical ecological
role as important supplier of flowers and fruit that sustain
associated fauna throughout the year (Staggemeier et al. 2010,
2017). Consequently, recent studies have advocated Myrteae
as a useful model group for testing hypotheses of biodiversity,
ecology, evolution, and conservation in Neotropical envi-
ronments (Murray-Smith et al. 2009; Giaretta et al. 2015; Lucas
and B ¨unger 2015; Staggemeier et al. 2015).
Despite its important ecological role in some Neotropical
habitats, the systematic and evolutionary relationships of
Myrteae have been elusive due to high levels of homo-
plasy, such that characters of taxonomic relevance at the
generic level are usually difficult to identify (McVaugh 1968;
Landrum and Kawasaki 1997). Initial molecular phyloge-
netic studies (Lucas et al. 2005, 2007) showed that characters
traditionally used, such as the embryo type (Berg 18551856),
had little power to accurately explain relationships in Myrteae
and that morphologically characterized natural groups were
few and poorly understood. Given recent systematic rear-
rangements in the tribe (Lucas et al. 2007, 2018, 2019; Mazine
et al. 2016; Vasconcelos et al. 2017b), a search for characters
that diagnose monophyletic groups is highly desirable. Recent
studies (e.g. Vasconcelos et al. 2015) demonstrate that despite
its apparent homogeneous morphology, some floral traits
can help diagnose lineages within Myrteae. The periodic
reassessment of morphology in light of recent phylogenies
provides reciprocal illumination of patterns and process, and
is important for future studies of systematics, ecology, and
evolution.
This study aims to summarize data on floral morphological
diversity across Myrteae. By assembling information from the
literature, herbarium material, floral ontogeny, and field ob-
servations, the purpose is to recommend more reliable di-
agnostic characters to help diagnose genera and subtribes,
stimulate debate on form and function, and generate new
hypotheses concerning the systematics, ecology, and evolution
to be tested by future studies.
Materials and Methods
Buds and flowers of Myrteae were collected in the field and from the
living collections and herbarium material at the Royal Botanic Gardens
Kew (herbarium K, Thiers 2018). Fruits were analyzed in some cases, but
only to emphasize patterns of structures that remain from flowers. Fruits,
seeds, and embryo traits, although important in Myrteae systematics
(Landrum and Kawasaki 1997), are not the focus here. Floral morphology
for forty-three of the forty-nine currently recognized Myrteae genera was
surveyed from spirit collections and herbarium material (see Appendix 1).
No suitable material bearing flowers could be analyzed for Acca (two
species), Amomyrtella (two species), Curitiba (one species), Lithomyrtus (11
species), Myrtella (two species), or Pseudanamomis (one species), so floral
morphology in these genera is described from the literature only. All other
floral descriptions are based on herbarium specimens, spirit collections
(Appendix 1), and literature. For the largest genera (Myrcia ca. 800 species,
Lucas et al. 2018; Eugenia, ca. 1000 species, Mazine et al. 2016), specimens
representing all accepted sections also were analyzed. Herbarium speci-
mens surveyed were those identified by specialists. Buds and flowers were
boiled to re-hydrate tissues for dissection. Descriptions of anthesis are
based on comparison of buds and open flowers from herbarium specimens
and field observations during field expeditions between 2013 and 2016.
Discussions of floral ontogeny are based exclusively on specimens
preserved in ethanol 70% or FAA in the field. For SEM preparation, buds
were dissected and passed through an ethanol series through full dehy-
dratation, critical point dried using an Autosamdri-815B critical-point
dryer, mounted on stubs, platinum coated using a Quorum Q-150-T
sputter coater, and analyzed under a Hitachi cold field emission SEM
S-4700-II.
The topology presented in the section Taxonomic Treatmentis a
schematic drawing that summarizes current understanding of relation-
ships within Myrteae. No phylogenetic analysis was performed here;
the tree results merely from visual inspection of topologies presented
by different studies. It combines information found in phylogenetic in-
ferences from Lucas et al. (2005, 2007, 2011), Costa (2009), De-Carvalho
(2013), Mazine et al. (2014), B
unger et al. (2016), Santos et al. (2017), and
Vasconcelos et al. (2017b). Where the support for a relationship was low or
where results from different studies disagreed, nodes were collapsed into
polytomies.
Results
BracteolesNearly all flowers of Myrtaceae are subtended
by two bracteoles. Faria (2014) comments that Eugenia splen-
dens may be exceptional for the apparent lack of bracteoles, as
they are not visible in most collections of this species even at
very early stages of flowering. Bracteoles appear to develop
simultaneously in tetramerous species or with a small de-
velopmental gap between each bracteole in pentamerous
species (Vasconcelos et al. 2017a). At early stages of ontogeny
the bracteoles cover the bud completely, but remain relatively
small compared to the fully formed bud at late stages of
570
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
development. Bracteole morphology has systematic relevance
in some groups. In Eugenia, for instance, sections can be rec-
ognized by the presence of filiform bracteoles (i.e. Eugenia sect.
Pilothecium), whereas others have distinct caducous bracteoles
at the fruiting stage (i.e. Eugenia sect. Speciosae)(B¨unger et al.
2016; Mazine et al. 2016).
Perianth (Calyx and Corolla)The calyx and corolla usually
are treated together (e.g. Endress 1994) even though they may
have distinct evolutionary histories (Ronse De Craene 2008).
Historical taxonomic interest in perianth characters of Myrteae
dates to Linnaeus (1753), who divided Myrtus from Eugenia
based on merosity; more recent interest, especially in the calyx
(e.g. Landrum 1984, Lucas et al. 2011), reflects some common
modifications (e.g. closed calyces,see below) and its frequent
persistence at fruiting. Most floral diversity in Myrteae reflects
two types of calyx organization: pentamerous, with classic
imbricate quincuncial aestivation (i.e. two sepals outside, two
sepals inside, and one intermediate; Figs. 1Aiiv,2A);orte-
tramerous, with two pairs of sepals developing decussately
(Figs. 1Biiv, 2C). Dimerous flowers are rare, but occur in at
least one species of Blepharocalyx (B. eggersii), which lacks
ontogenetic evidence for development of a second pair of
sepals and/or petals (Figs. 1Ciiv,2D).Perianthdevelop-
ment follows a mirror-image proccess in flowers of opposite
sides in an inflorescence. In pentamerous species, perianth
parts are formed in an imperfectly sequential, spiral process,
either clockwise or counterclockwise (Fig. 1D).
Sepals are usually the same size in mature buds, but both
pentamerous and tetramerous flowers may have sepals
slightly to strongly unequal in size even at late stages. Such size
distinctions usually do not significantly change overall floral
symmetry (e.g. Fig. 2E), but are taxonomically relevant at the
species level in some groups (e.g. Sobral 2005, for Eugenia
inversa). Complete calyx fusion is homoplastic and appears
in a few to several species in different lineages (Fig. 2H, I; e.g.
Landrum 1984, in Myrceugenia; Parra-O and Bohorquez-
Osorio 2016, in Myrcianthes). This is achieved by late-
congenital fusion, a mode of development where the sepals
are initially free but tissues fuse from the base during devel-
opment. In this way, at late stages of floral development,
individual sepals are no longer recognizable and the fully
formed calyx appears to cover the bud completely. This char-
acter state is named closed calyx in the budin the Myrtaceae
literature and is common also in other tribes (e.g. Eucalypteae,
Wilson 2011; for evolutionary interpretation of this character see
Vasconcelos et al. 2017a, and Giaretta et al. 2019). The anthetic
behavior of this structure varies from being a deciduous ca-
lyptra to irregular tearing (i.e. tissues tear at random points
during anthesis; Fig. 2H) or regular tearing (i.e. tissues tear at
points where sepals are adjacent, during anthesis; Fig. 2I),
patterns with historical taxonomic relevance (McVaugh 1968;
Wilson et al. 2016; Lucas et al. 2018).
The corolla develops after the calyx (i.e. centripetal organ
formation). Petals are always alternisepalous and are usually
present in the same number as sepals. Flowers with five sepals
develop five petals in alternate positions, following the same
imbricate quincuncial aestivation pattern (Figs. 1Aiv, 2B).
Flowers with four sepals tend to have four petals that are
almost simultaneously initiated, in contrast to the decussate
pattern of the sepals (Fig. 1Bii, iv). Petals are either rounded
or elliptic and are attached to the hypanthium by a short,
thickened, and somewhat consticted base, making them fall
off easily after anthesis. There are few exceptions in corolla
arrangement among all 50 genera. The most remarkable ones
are in the tetramerous genus Octamyrtus, where a second
corolla whorl and sometimes two to four extra petals develop
(up to 12 petals in total; Scott 1978b; Craven 2006; Snow et al.
2011); and in Myrtus, where narrow petals develop into a
variable number of whorls (Mulas and Fadda 2004).
Shifts back and forth between tetramerous and pentamerous
flowers are likely to have occurred multiple times in Myrteae.
Variation between four and five perianth parts is commonly
observed at infrageneric and even at infraspecific levels (e.g.
Fig. 2F, G). The norm, however, is that the lower the taxonomic
level the more stable the merosity. Therefore, it is difficult to
estimate with precision which pattern is the plesiomophic state
for the tribe, but merosity is still an important component of
generic identification in Myrteae (e.g. keys in Landrum and
Kawasaki 1997, Sobral 2003, and Mazine et al. 2014).
Androecium and Hypanthium ExtensionThe androecium
has historically been neglected in Myrteae systematics. The al-
most invariable polystemonous flowers produce low noticeable
variation in this organ. Therefore, references to the taxonomic
relevance of the androecium are virtually absent in classical
Myrteae taxonomic literature (even in extensive reviews such
as McVaugh 1968 and Landrum and Kawasaki 1997). However,
Vasconcelos et al. (2015) show that the androecium harbors
valuable taxonomic characters, especially when considered in
concert with hypanthium development (e.g. Belsham and
Orlovich 2002, 2003; Vasconcelos et al. 2017a, 2018).
The definition of hypanthiumis inconsistent in the lit-
erature. General floral morphologists define the hypanthium
as a cup-shaped structure that involves the ovary in perigi-
neous and epigineous flowers (Weberling 1989; Endress 1994).
Weberlings hypanthium overlaps with his definition of the
floral receptacle, for which he states that the [perianth and
androecium] appear inserted on the edge of the hypanthium,
or so called receptacle(Weberling 1989, p. 20). While some
authors prefer to use the term receptacle(e.g. Ronse De
Craene and Smets 1992, 1993), most Myrtaceae literature
adopts the term hypanthiumto refer to the tissue between
perianth and gynoecium (e.g. Proença et al. 2006; Snow and
Wilson 2010; Amorim and Alves 2012; Martos et al. 2017). To
our knowledge, no study has yet explicitly tested the evolu-
tionary origin of this structure in Myrteae and we also do not
aim to solve this issue here. We will here use the same defi-
nition as in other Myrtaceae literature, referring to the hy-
panthium as a tissue between the base of the ovary and the
perianth on which the staminal rings are formed.
It is on the inner apical surface of this tissue that stamen
primordia appear and stamens of the polyandrous androe-
cium develop (Ronse De Craene and Smets 1991; Belsham and
Orlovich 2002, 2003). In this sense, it is impossible to fully
separate androecium from hypanthium when discussing floral
morphology and ontogeny of Myrteae. In Myrteae, mature
flowers present two main hypanthium types: these can be
either extend above the ovary line, forming a hypanthium cup
or tube (e.g. as in Myrcia and Siphoneugena), or terminate at the
same position as the summit of the ovary (e.g. as in Eugenia).
Development of these two patterns is similar during floral
ontogeny; the difference is mainly the extent to which stamen
primordia cover the tissue during early stages of development.
Androecium development in Myrteae starts with the ap-
pearance of two (or more) stamen primordia at the flanks of
each petal (Belsham and Orlovich 2002, 2003; Vasconcelos
et al. 2017a, 2018). Sequentially, more primordia develop
VASCONCELOS ET AL.: FLORAL DIVERSITY IN MYRTEAE 5712019]
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
forming the first staminal ring. This is contrary to other
Myrtaceae where secondary polyandry occurs and obha-
plostemonous primary stamen primordia give rise to sec-
ondary stamen primordia (e.g. Melaleuca; Carrucan and
Drinnan 2000); in Myrteae there is no clear distinction between
primary and secondary stamen primordia. After the first
staminal ring is formed, more stamen primordia initiate
centripetally. The degree to which these primordia cover the
inner hypanthial surface determines the final position of the
stamens within the flower (Vasconcelos et al. 2015, 2018).
When stamen primordia cover the entirety of the hypanthium
tissue up to the stylar base (Fig. 3Ai), stamens in the bud
appear straight and no hypanthial tube is visible (Fig. 3Aiiiv).
When the stamen primordia cover just a restricted area at the
hypanthium rim during development (Fig. 3Ci), stamens fold
into the area provided by the barehypanthium tissue,
resulting in curved stamens at anthesis and a hypanthium tube
of variable length (Fig. 3Ciiiv) (see also Vasconcelos et al.
2018). Straight vs. incurved stamens is a trait with high sys-
tematic relevance, explaining some suprageneric relationships
recovered by the molecular phylogeny of Myrteae (Lucas et al.
2007; Vasconcelos et al. 2015, 2017b). A third variation is the
Fig. 1. Patterns of perianth arrangement in Myrteae. A. Pentamerous flowers with imbricate quincuncial sepals and petals. Diagram(Ai) and ontogenetic
sequence (AiiAiv) in Myrcia guianensis (Myrcia sect. Aguava). B. Tetramerous flowers with decussate sepals and four petals that initiate simultaneously.
Floral diagram (Bi) and ontogenetic sequence (BiiBiv) in Eugenia ligustrina (Eugenia sect. Eugenia) (Bii) and Eugenia stipitata (Eugenia sect. Pilothecium) (Biii,
Biv). C. Dimerous flowers of Blepharocalyx eggersii. Floral diagram (Ci) and ontogenetic sequence (CiiCiv; two petals initiate in the axils of each sepal, but
just one is seen in Biv). D. Clockwise and anticlockwise direction of perianth development in opposite flowers of Myrcia spectabilis (Myrcia sect. Gomidesia),
highlighting the mirror-image pattern and imperfectly sequential spiraal development of perianth parts in pentamerous flowers. Dashed outlines represent
dissected structures. Brt 5bracteole; S 5sepals; P 5petals. Scale : 5 0 mm (Aii, Bii, Cii, Ciii); 100mm (Aiii, Aiv, Biii, Civ); 150 mm(Biv,D).
SYSTEMATIC BOTANY [Volume 44572
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
discontinuous androecium observed in Lenwebbia,Luma,
Myrceugenia, Temu, and some Pimenta species (Belsham and
Orlovich 2003), here interpreted as an intermediary arrange-
ment between the straight and incurved stamen types. In these
flowers, the first stamens develop from primordia below each
petal while only subsequent stamens form a continuous ring
(Fig. 3Bi; Belsham and Orlovich 2003). This discontinuous
development gives the stamens a posture that has been de-
scribed as semi-foldedin the bud (Fig. 3Biiiv; Vasconcelos
et al. 2015).
Anthers are always tetrasporangiate, consisting of four
pollen sacs that differentiate at later stages of floral devel-
opment at the distal portion of each filament. Abaxial pollen
sacs are usually smaller than adaxial ones, and latrorse de-
hiscence occurs by a simple longitudinal slit, with tearing of
the thin tissue between each pair of pollen sacs (as in most
eudicots; Endress 1994). Anthers are dorsifixed, except in Ugni
and Uromyrtus where they are somewhat basifixed (Snow and
Guymer 2001; Wilson 2011). During anthesis, or even slightly
before, tissue that connects each pair of pollen sac tears. At this
point, the walls of all four locules retract completely, giving an
opening of ca. 180 degrees for each lateral pair of pollen sacs.
Specialized connectives and dehiscence behavior can occur,
e.g. apiculate connectives in some species of Campomanesia
(Landrum 1986) and disproportionally long anthers with
slightly dislocated pollen sacs in Myrcia sect. Gomidesia (Lucas
Fig. 2. Field pictures showing diversity of perianth arrangements in Myrteae. A. Buds of Myrcia sp. (M. sect. Gomidesia) showing pentamerous flowers
with imbricate quincuncial sepals. B. Flowers of Ugni candolei, showing a similar pattern in its petals. C. Young buds of Myrceugenia alpigena, showing the
first pair of decussate sepals larger than the second pair. D. Dimerous flowers of Blepharocalyx eggersii, showing a pair of petals and a pair of
sepals. E. Unequal sepals in old flowers of Myrcia splendens (Myrcia sect. Myrcia). F. Variation of merosity in two flowers of the same inflorescence in Algrizea
minor and (G) in the same individual of Campomanesia adamantium. H. Calyx fusion in Psidum sp., showing (Hii) torn calyx after anthesis and (Hiii) a calyptra
remaining at fruiting stage. I. Partial sepal fusion in Accara elegans, showing (Iii) scars from where the sepals tore at anthesis. S 5sepals; P 5petals. Scale:
2.5 mm (Aiii, D, Iii); 5 mm (Biii, Ciii, E, F, Giii, Hiiii, Ii). All pictures by T. N. C. Vasconcelos or E. J. Lucas.
VASCONCELOS ET AL.: FLORAL DIVERSITY IN MYRTEAE 5732019]
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
et al. 2011). In the latter, possibly due to uneven growth of the
connective (Vasconcelos et al. 2017a), locule wall retraction is
not always complete, giving a poricidal aspect associated with
adaptation to buzz pollination (Proença 1992; Nic Lughadha
1998). Pollen grains are small to medium sized, usually
ranging from 14 mmto22mm (except Octamyrtus, where pollen
grains are up to 44 mm; Thornhill et al. 2012), triangular shaped
and brevicolpate, with little variation among most Myrteae
lineages (see review by Thornhill et al. 2012).
GynoeciumThe gynoecium is the most variable floral
organ in Myrteae. Characters related to the gynoecium are
present in buds, flowers, and fruits (when well dissected,
locules and aborted ovules can be seen against the ovary wall).
Traits of the gynoecium are usually infragenerically consistent
and supragenerically variable, highlighting the convenience
of this character for taxonomic diagnosis (as discussed by
Bentham 1869, and Kausel 1956). During the last decades,
several genera were described supported by characters of the
gynoecium (e.g. Accara, Landrum 1990; Chamguava, Landrum
1991; Gossia, Snow et al. 2003). Overall gynoecium morphol-
ogy also has a strong evolutionary component, as it constrains
the width of the stigma (e.g. Fig. 4), the length of the style, and
possibly the number of ovules that can be fertilized (see sec-
tions Ovule Oversupply and Herkogamy and Strategies to Avoid
Selfing below). Variation in the morphology of this structure is,
however, difficult to record. The position of the inferior ovary
and distinct patterns of ovule arrangement, placentation, and
carpel fusion are only evident when information from trans-
verse, longitudinal, and tangential sections are combined (see
Figs. 5, 6).
Early stages of gynoecium development in Myrteae are
visible by a depression that appears in the center of the de-
veloping flower, simultaneous to androecium initiation.
Carpels appear to initiate free, but fuse just after initiation (i.e.
late-congenital fusion), so that it is usually possible to rec-
ognize how many locules will be formed by the shape of the
initial depression (Figs. 4A, B, 5A, B; see also Vasconcelos et al.
2017a, 2018). Tissues around the depression swell sequentially
to form a proto-stigma. In species with multiple locules, the
depression is larger and consequently the proto-stigma is
broader, forming a stigma that is capitate or peltate, con-
trasting with a usually simple one in species with fewer locules
Fig. 3. Three main patterns of stamen formation on the hypanthium in Myrteae. A. Straight stamen developmental pathway, where stamen primordia
cover the whole hypanthial tissue. Floral diagram (Ai) and ontogenetic sequence (Aiiiv) in Eugenia bunchosiifolia (E. sect. Speciosae). B. Semi-folded stamen
pathway, where stamen primordia arise in discontinuous rings on the hypanthial tissue. Floral diagram (Bi) and ontogenetic sequence (Biiiv) in Luma
apiculata. C. Folded stamen developmental pathway, where stamen primordia are restricted to the rims of the hypanthial tissue. Floral diagram (Ci) and
ontotogenetic sequence (Ciiiv) in Myrcia subcordata (M. sect. Sympodiomyrcia). A 5androecium; G 5gynoecium; P 5petal; S 5sepal. Scale: 10 mm (F);
250 mm (Aii, Aiii, Bii, Biii, Cii, Ciii, E); 500 mm (Aiv, Biv, Civ).
SYSTEMATIC BOTANY [Volume 44574
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Fig. 4. Distortions in flower architecture caused by differences in the gynoecium development between two closely related genera. A, C, E, G. Feijoa
sellowiana;B,D,F,H.Campomanesia adamantium. A, B. Early flower development, showing a small ovary depression in (A) F. sellowiana and a (B) larger one in
C. adamantium. C, D. Longitudinal section of mature buds; note stamens slightly dislocated upwards in (D) due to the robust gynoecium. E, F. Comparison
between (E) simple stigma of F. sellowiana and (F) capitate stigma of C. adamantium. G, H. Diagram of longitudinal section in mature bud showing changes in
architecture resulting from variation in gynoecium development. A 5androecium; G 5gynoecium; P 5petal. Scale: 50 mm(A,B);250mm (C); 500 mm (D). Color
code: green 5sepals, red 5petals, yellow 5androecium, orange 5hypanthium, blue 5gynoecium.
VASCONCELOS ET AL.: FLORAL DIVERSITY IN MYRTEAE 5752019]
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Fig. 5. Diagrams of transverse sections of ovaries in Myrteae flowers, showing variation in the number of locules, number of ovule series on placenta,
and carpel fusion. A. Number of carpels usually relates to the number of locules, unless fusion is not complete (few exceptions). B. Format of depression left
on the base of the bud at early developmental stages, suggesting late-congenital fusion of carpels. C. Arrangement of ovules on placenta varies from
uniseriate to multiseriate. D. Examples of incomplete carpel closure. *Psidium ovule arrangement and placenta format is variable and may range from uni- to
multiseriate.
SYSTEMATIC BOTANY [Volume 44576
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Fig. 6. Diagrams of tangential and longitudinal sections of ovaries of Myrteae; showing variation in the number of ovule series and of placenta length.
Note that variation in number of ovule series on the placenta can only be verified in tangential sections. Examples of tangential sections (iv) showing (i)
uniseriate ovule arrangement on short placenta (Pimenta pseudocaryophyllus); (ii) biseriate ovule arrangement on medium sized placenta (Ugni candolei); (iii)
biseriate ovule arrangement on elongated placenta and incompletely fused carpels (Feijoa sellowiana); (iv) multiseriate ovule arrangement on medium sized
placenta (Chamguava shippii); (v) two ovules over a short placenta (Blepharocalyx eggersii).
VASCONCELOS ET AL.: FLORAL DIVERSITY IN MYRTEAE 5772019]
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
(Fig. 4AF). Meanwhile, during early ovary development,
each locule forms an individual chamber around the center of
the ovary. At this point, a central axis protrudes from the base
while an apical septum elongates from the apex, forming a
central septum and the locule walls (Pimentel et al. 2014). The
point where the central basal axis and apical septum meet can
be very tightly closed, or slightly to completely open, pro-
viding connection between locules in some genera (e.g. Feijoa,
Myrtus,Rhodamnia, Fig. 3D; see also Pimentel et al. 2014, and
Harthman et al. 2018).
In most genera, placentation is axial and the placenta de-
velops from the central axis or along the edges of the points
where locule walls meet at the center of the ovary. Ovules
develop attached to the placenta, and can be uniseriate (Fig. 6i;
e.g. most Decasperminae), biseriate (Fig. 6ii; e.g. some Ugninae)
or multiseriate (Fig. 6iv, e.g. most Eugeniinae and Myrtinae;
see also Fig. 5C). In Myrciinae and some Blepharocalycinae
(notably Blepharocalyx eggersii), the reduced number of ovules
per locule make this character difficult to interpret. Here we
hypothesize that the two ovules per locule found in these
groups are reductions from multiseriate arrangements with
higher number of ovules per locule, as observed in most Pli-
niinae (sister group to Myrciinae) and some individuals of
Blepharocalyx salicifolius.
The placenta is itself variable in development and format. In
subtribe Pimentinae (e.g. Feijoa,Psidium) the placenta is fre-
quently well developed, and the diminutive ovules appear
organised in crowns around the protruded tissue in tangential
dissections (Fig. 6iii). On the other hand, most species of the
Myrciinae and Eugeniinae subtribes, for instance, show poorly
developed placentas, having ovules that appear to cover the
whole placenta tissue in tangential dissections. The shape of
the placenta, a character cited as important in some studies
(Landrum 1991, 1992; Snow 2000), may be misleading because
it distorts when the number of locules changes. In other words,
species in the same genus have different placenta shapes
depending on the number of locules (as it happens in some
Campomanesia). The number of ovules per locule and number
of locules are commonly variable at lower taxonomic levels,
but some evolutionary trends can be useful to diagnose species
and genera (e.g. the common two ovules per locule in Myrcia,
Landrum and Kawasaki, 1997; and the three locules in Myrcia
sect. Aguava and M. sect. Reticulosae, Lucas et al. 2018).
In conclusion, the systematic importance of the gynoecium
includes the following characters: 1) Arrangement of ovules on
the placenta (uniseriate, biseriate, multiseriate); 2) Number of
locules; 3) Number of ovules per locule; and 4) Stigma type
(useful to separate some genera and species, but not always
consistent). These characters usually allow identification to a
genus or group of genera with reasonable confidence (see
Table 1).
TrichomesPubescence, a characteristic of most Myrteae
flowers, is typically from single-celled trichomes (Fig. 7A) that
give a silky appearance to the tissue where they grow. The
presence or absence of hairs and where they occur on the floral
surface is often taxonomically consistent and thus useful for
systematics. Examples include silky appearance of Myrcia sect.
Myrcia buds, in contrast to other Myrcia sections (Berg
18551856; Lucas et al. 2011, 2018); pubescent flowers of the
Decasperminae that distinguish them from other sympatric
Myrtaceae in the Australasian region (Ashton 2011); dibra-
chiate hairs that occur in Myrceugenia and Myrcia (Landrum
1981a, 1981b) and in some Eugenia,Ugni, and Calycolpus
species (L. Landrum pers. comm.); and hairs on the locular
walls in Eugenia sect. Pillothecium and some Pimenta (Fig. 7B;
Faria 2014). The evolutionary significance of the presence of
these trichomes is not clear, but similar indumenta are asso-
ciated with protection against predators (e.g. Breedlove and
Ehrlich 1972; Fig. 7C) and reflective properties against solar
radiation (Miller 1986).
Oil Glands and ElaiophoresMyrtaceae are renowned for
their oil glands (Evert 2006; Wilson 2011), and Myrteae flowers
are no exception. Oil glands are present in all floral tissues, but
can be particularly prominent on the anther, connective, and
style wall (Fig. 7F, G; e.g. Landrum and Kawasaki 1997; Snow
2009). These glands lack stomata or clear secretory speciali-
zation, but may present some systematic or ecological rele-
vance (suggested by Landrum and Bonilla 1996). Correlation
of this character with environmental variables is, however,
weakly supported (Vasconcelos et al. 2019). A few species
present small cavities on the surface of the floral receptacle
around the stylar base (Fig. 7D). These are at a similar position
to nectary tissue in other Myrtaceae (OBrien et al. 1996; Ronse
De Craene 2010), but lack clear secretory structures (Fig. 7E;
see also Vasconcelos et al. 2018). There is no strong support for
nectar production in Myrteae (Gressler et al. 2006); such
cavities were shown to be elaiophores in Myrtus and sug-
gested as nectary relics that are now only phenolic producers
(Ciccarelli et al. 2008). These serve to attract pollinators, and
although no evidence for scent acting as reward has ever been
documented, some Neotropical bees that visit Myrteae species
(e.g. Euglossini, Nic Lughadha and Proença 1996) are known to
be phenolic foragers (Cameron 2004).
Androdioecy: More Common Than AcknowledgedMost
Myrteae flowers are hermaphroditic, with an androecium
and a gynoecium developing as previously described. In a few
species, however, individual plants within a population bear
apparently hermaphrodite flowers while others bear only
male flowers. This trend, known as androdioecy, is fairly
common in Myrtaceae (see also Ashton 2011, for Syzygium).
Androdioecious species are present in at least seven Myrteae
genera (Pimenta, Psidium, Myrcia, Eugenia, Decaspermum,
Kanakomyrtus, and Myrtastrum; Van Wyk and Lowrey 1988;
Nic Lughadha and Proença 1996; Snow et al. 2003; Wilson
2011; Byng et al. 2016; T. Vasconcelos pers. obs.) and their
broad phylogenetic distribution indicates that this trend may
be more common than previously appreciated. Plants bearing
male flowers produce buds that have either an atrophied
gynoecium (Fig. 8) or an additional whorl of stamens at the
equivalent position to the gynoecium (T. Vasconcelos pers.
obs.). In three genera (Eugenia,Pimenta, Decaspermum), there is
evidence that the breeding system is functionally dioecious,
where the apparently hermaphrodite flowers do not produce
viable pollen (Chapman 1964; Kevan and Lack 1985; Byng
et al. 2016).
Ovule OversupplyEven though the number of ovules
varies within a genus, most genera present a standard range of
seed number. For most Eugenia and Myrcia species for ex-
ample, seed number is usually one or two regardless of the
number of ovules produced (Fig. 9A; Berg 18551856; Lucas
et al. 2007; Staggemeier et al. 2017; a similar pattern was
observed in cultivated Luma apiculata, Fig. 9B). On the other
hand, Plinia,Myrceugenia, and Myrtus produce few seeds (less
than ten, Fig. 9C) and Feijoa,Psidium, and Rhodomyrtus pro-
duce multiple seeds (frequently over 25; Landrum and
Kawasaki 1997; Wilson 2011). According to Landrum (1982),
SYSTEMATIC BOTANY [Volume 44578
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Campomanesia is also peculiar in producing several ovules but
just one seed per locule, resulting in few seeds per fruit given
the common multiloculate state in the genus. In this way, ovule
oversupply, i.e. the production of more ovules than will be
fertilized (Rosenheim et al. 2016), occurs at different levels
throughout Myrteae. Taxa that are single or few-seeded are
concentrated in the largest lineages (i.e. Eugeniinae, Myrcii-
nae, Pliniinae), regardless of the number of ovules produced.
Constraining the number of ovules that can be fertilized may
have given an advantage to certain lineages, allowing the
Table 1. Floral formulae and diagnostic characters in Myrteae subtribes (floral formulae after Prenner et al. 2010). * Floral formulae andstigma types in
Myrtella and Lithomyrtus are based on Wilson (2011). ** Calyptrogenia,Hottea, and Pseudanamomis are not represented due to their nested phylogenetic
placement and future synonymization in Eugenia.
Clade Genus Floral formulae Ovule arrangement
on placenta Stigma Position of stamens
in the bud
Decasperminae Archirhodomyrtus aK5* C5* A*
ˆ
G(23)VxUniseriate Capitate Straight
Austromyrtus aK5* C5* A*
ˆ
G(2)Vx1020 Apparently biseriate Simple Straight
Decaspermum _a K45* C45*A*
ˆ
G(5)Vx10 Uniseriate Capitate Straight
Gossia aK45*C45*A*
ˆ
G(2)Vx520 Multiseriate Simple Straight
Kanakomyrtus _a K45* C45* A*
ˆ
G(24)VxUniseriate Capitate (lobed) Straight to
semi-curved
Lithomyrtus* aK5* C45* A*
ˆ
G(2)Vx2 (not seen) Simple or capitate (not seen)
Myrtella* aK5* C5* A*
ˆ
G(23)Vx412 (not seen) Simple or capitate (not seen)
Octamyrtus aK4* C4*14*12A1520*
ˆ
G(3)VxUniseriate Capitate Straight
Pilidiostigma aK45*C45*A*
ˆ
G(13)Vp-VxUniseriate Capitate Straight
Rhodamnia aK45* C45* A*
ˆ
G(23)Vp1020 Uni- or biseriate Simple or capitate Straight
Rhodomyrtus aK5* C5* A*
ˆ
G(3)VxUniseriate Capitate Straight
Uromyrtus aK5* C5* A*
ˆ
G(3)Vx1020 Uniseriate Simple Straight
General ground plan aK45*C45*A*
ˆ
G(23)Vx5-Uniseriate Simple or capitate Straight
Blepharocalyinae Blepharocalyx eggersii aK(2)*C2*A*
ˆ
G(2)Vx48 Multiseriate Simple Strongly incurved
Blepharocalyx
salicifolius
aK4*C4*A*
ˆ
G(2)Vx416 Multiseriate Simple Strongly incurved
General ground plan aK(2)-4*C24*A*
ˆ
G(2) Vx416 Multiseriate Simple Strongly incurved
Eugeniinae ** Eugenia _aK4(4)*C4*A*
ˆ
G(2)Vx4-Multiseriate Simple Straight
Myrcianthes aK5(5)*C5*A*
ˆ
G(2)VxMultiseriate Simple Straight
General ground plan aK4*C4*A*
ˆ
G(2)Vx4-Multiseriate Simple Straight
Luminae Luma aK4*C4*A*
ˆ
G(2)VxUniseriate Simple Semi-curved
Myrceugenia aK4(4)*C4*A*
ˆ
G(2)VxUniseriate Simple semi-curved
Nothomyrcia aK4*C4*A*
ˆ
G(2)VxUniseriate Simple semi-curved
Temu aK4*C4*A*
ˆ
G(2) VxUniseriate Simple semi-curved
General ground plan aK4*C4*A*
ˆ
G(2) VxUniseriate Simple semi-curved
Myrciinae Myrcia aK5(5)*C5*A*
ˆ
G(23) Vx46 Multiseriate Simple Strongly incurved
General ground plan aK5(5)*C5*A*
ˆ
G(23) Vx46 Multiseriate Simple Strongly incurved
Ugninae Lenwebbia aK4*C4*A*
ˆ
G(3) VxUniseriate Simple Semi-curved
Lophomyrtus aK4*C4*A*
ˆ
G(23) VxUniseriate Simple Semi-curved
Myrteola aK45*C45*A1030*
ˆ
G(23) VxUniseriate Simple Straight
Neomyrtus aK5*C5*A*
ˆ
G(2) VpBiseriate Simple Straight
Ugni aK5*C5*A2030*
ˆ
G(3) VxBiseriate Simple Straight
General ground plan aK45*C45*A20-*
ˆ
G(23) VxUni- or Biseriate Simple Straight or
Semi-curved
Myrtinae Accara aK(4)*C4*A*
ˆ
G(4) VxBi- or Multiseriate Simple Straight
Calycolpus aK5(5)* C5* A*
ˆ
G(46) VxMultiseriate Simple to slightly
capitate
Straight
Chamguava aK(4)* C4* A*
ˆ
G(2) VxMultiseriate Simple Straight
Myrtus aK5* C5* A*
ˆ
G(3) VxMultiseriate Simple Straight
General ground plan aK45* C45* A*
ˆ
G(24) VxMultiseriate Simple Straight
Pimentinae Acca* aK4* C4* A*
ˆ
G(2) Vx(not seen) Simple (not seen)
Campomanesia aK5(5)* C5* A*
ˆ
G(218)Vx Uniseriate Capitate Straight
Curitiba aK4* C4* A*
ˆ
G(2)VxUniseriate Simple Straight
Feijoa aK5* C45* A1530*
ˆ
G(4)VxBiseriate Simple Straight
Legrandia aK4* C4* A*
ˆ
G(23)VxUniseriate Simple Straight
Mosiera aK4* C4* A*
ˆ
G(23)VxMultiseriate Capitate Straight
Myrrhinium aK4*C4*A48:
0
ˆ
G(2)Vx715 Uniseriate Simple Straight
Pimenta _a K45* C45* A*
ˆ
G(2)Vx 18 Uniseriate Simple Semi-curved
Psidium _aK45(45)*C45*A*
ˆ
G(25)VxMultiseriate Capitate Straight
General ground plan aK45* C45* A*
ˆ
G(2)VxUni- or Multiseriate Simple or Capitate Straight
Pliniinae Algrizea aK5* C5* A*
ˆ
G(2)Vx36 Multiseriate Simple Strongly incurved
Myrciaria aK4* C4* A*
ˆ
G(2)Vx46 Multiseriate Simple Strongly incurved
Neomitranthes aK(4)* C4
r
*A*
ˆ
G(2)Vx48 Multiseriate Simple Strongly incurved
Plinia aK4(4)* C4* A*
ˆ
G(2)Vx610 Multiseriate Simple Strongly incurved
Siphoneugena aK4(4)* C4 * A*
ˆ
G(2)Vx48 Multiseriate Simple Strongly incurved
General ground plan aK4(4)* C4* A*
ˆ
G(2)Vx48 Multiseriate Simple Strongly incurved
VASCONCELOS ET AL.: FLORAL DIVERSITY IN MYRTEAE 5792019]
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
development of larger seeds that are better adapted to certain
environments (e.g. rainforests; Foster 1986), conferring a
strategy of shift from quantity to quality (Schupp 1993).
Herkogamy and Strategies to Avoid SelfingGenera and
groups of genera present different strategies to avoid selfing.
In species with folded stamens, the style elongates earlier
than the stamens, thus presenting discrete protogyny that may
help avoid self-pollination (Fig. 10A; most Myrteae are self-
incompatible, Nic Lughadha and Proença 1996). Species with
straight stamens usually have both stamens and style at ap-
proximately the same height after anthesis, with pollen ready
for collection as soon as the flower opens, increasing the
chances of self-pollination (see discussion in Vasconcelos et al.
2015). Some species of Eugenia and Psidium avoid self polli-
nation by presenting style gigantism, where the style stands
twice as high as the anthers during anthesis (see Vasconcelos
et al. 2018, for Eugenia). This strategy may be linked with
higher diversity in these groups (Vasconcelos et al. 2017b),
with further evidence from similar trends in other plant groups
(de Vos et al. 2014). Heterostyly is not evident in any species,
but cannot be ruled out until more extensive surveys are
carried out.
Common Pollination StrategiesMost Myrteae share a
similar pollination strategy. Anthesis commonly occurs just
before sunrise and is concentrated in the months between
September and December (i.e. spring in the southern hemi-
sphere, Staggemeier et al. 2010), although it may extend
considerably beyond that depending on local conditions.
Flowers of Myrteae offer pollen as the main or sole reward
(Gressler et al. 2006) and are visited by a range of insects, with
bees considered the most general and effective pollinators
(Nic Lughadha and Proença 1996; Gressler et al. 2006). Most
flowers can be loosely classified into two subcategories based
on display. The first is a stamen-dependent display (also called
brush blossom, Johnson and Briggs 1984), where stamens
are the main component of floral visual attraction (Fig. 10C).
In this case, the perianth reflexes backwards when the
flower opens and is thought to play a less important role than
the stamens in pollinator attraction. The second trend is a
petaloid display, wherein the larger non-reflexed petals rep-
resent the most conspicuous visual attraction (Fig. 10D), and
in which filaments are commonly shorter than in more
stamen-dependent displays. Many intermediates are observed,
but even closely related taxa may represent extremes in this
continuum (e.g. the petaloid Calycolpus vs. the more stamen-
dependent Myrtus, both in subtribe Myrtinae). A similar var-
iation between stamen-dependent and petaloid display also
is observed in other Neotropical pollen-flowers, such as
Solanaceae and Melastomataceae (Buchmann and Cane 1989;
Kriebel and Zumbado 2014), and may be related to sub-
syndromes of pollen-gathering bee pollination.
Uncommon Pollination StrategiesPollination by verte-
brates is rare in Myrteae, but exists in at least two genera. The
bird pollinated Myrrhinium and Feijoa show similar floral
strategies: decreased numbers of stamens, increased filament
length, red colored display, and thick-sweet petals (Fig. 10B),
the latter being the main reward for pollinators (Roitman
et al. 1997). Reduced number of stamens is especially ex-
treme in Myrrhinium, where just four to six stamens de-
velop (Landrum 1986). The fact that Feijoa and Myrrhinium
Fig. 7. Trichomes, elaiophores, and anther glands in Myrteae flowers. A. Single celled trichomes (hairs) developing on external calyx and hypanthium
surface of a Myrcia splendens (M. sect. Myrcia) bud. B. Similar trichomes growing on the inner surface of the locule wall in Eugenia itajurensis (E. sect.
Pilothecium). C. Termite inside a pubescent bud of Myrcia sect. Gomidesia. D, E. Elaiophores in (D) Pimenta dioica (indicated by arrows) and in (E) Rhodamnia
cinerea. F, G. Anther oil gland in (F) Rhodomyrtus tomentosa and (G) Myrcia rubella (M. sect. Aulomyrcia) (arrow). G 5gynoecium. Scale: 25 mm(A);50mm
(D, E); 250 mm (B, F, G); 3 mm (C).
SYSTEMATIC BOTANY [Volume 44580
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
represent species-poor clades (one species each) suggests
that specialization towards bird pollination has not been
advantageous for Myrteae diversification. It is important
to reiterate that Myrteae flowers usually do not produce
nectar, and thus cannot benefit from the most successful bird
pollinators in the Neotropics, the hummingbirds, as have
other diverse and sympatric bird pollinated groups such as
Bignonieae (Alcantara and Lohmann 2010) and Costus (Kay
et al. 2005; see also Rocca and Sazima 2010). Other unusual
floral displays that resemble pollination syndromes asso-
ciated to birds, bats, or flightless vertebrates are observed in
the Decasperminae (e.g. long stamens and petals forming a
tube in Octamyrtus; White 1951; Craven 2006) and Eugenia
from the Pacific and Madagascar regions (Eugenia sect.
Jossinia; e.g. long stamens and petals forming a tube in E. bullata
and thick bracteoles subtending flowers in E. ambanizanensis).
Observations in the field that can confirm such specializations
are, however, not available for these taxa yet.
Taxonomic Treatment
Recent phylogenetic studies, coupled with monographs and
revisions, indicate high levels of homoplasy in many floral
traits (e.g. merosity, fused calyx, trichomes, locule, and ovule
number). Observation of a single organ is usually systemati-
cally irrelevant; combinations of traits, however, can identify
a genus or a group of genera with fair confidence (Table 1).
The overall floral pattern found in each subtribe is described
below.
Blepharocalycinae, Myrciinae, and PliniinaeThe subtribe
Blepharocalycinae, consisting of Blepharocalyx as the sole ge-
nus, historically has been considered closely related to the
Fig. 8. Androdioecy in Decaspermum. Flower on the left has aborted gynoecium (staminate flower), while in the flower on the right gynoecium and
androecium are formed (hermaphrodite). Scale bar 510 mm.
VASCONCELOS ET AL.: FLORAL DIVERSITY IN MYRTEAE 5812019]
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Fig. 9. Distinct degrees of ovule oversupply in fruits of similar size. Distinct lineages present from a few to several aborted ovules in the mature
fruit. A. Myrcia spectabilis (M. sect. Gomidesia), showing three aborted ovules and one seed. B. Luma apiculata, showing several aborted ovules and one
seed. C. Myrtus communis, showing several aborted ovules and several seeds. Scale bar 5ca. 5 mm.
SYSTEMATIC BOTANY [Volume 44582
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Pimentinae and Myrtinae genera, based mainly on embryo
morphology (Landrum 1986). In terms of floral architecture,
however, Blepharocalycinae flowers are similar to those of the
Myrciinae and Pliniinae genera (Fig. 11BD). Floral characters
shared by all three subtribes include strongly incurved sta-
mens (Vasconcelos et al. 2015), the multiseriate ovule ar-
rangement on the placenta (visible when ovule number is
above two per locule), and a low number of ovules per ovary
(Lucas et al. 2007). The locules are usually two, or less com-
monly, three. Within the Pliniinae and Myrciinae genera, the
flowers are highly homogeneous, such that variation that
diagnoses infrageneric groups in the large genus Myrcia comes
from traits such as hairs, calyx fusion, relative hypanthium
projection above the ovary, and thickness of the staminal ring
(Lucas et al. 2018). Pliniinae and Myrciinae always appear as
sister groups in phylogenetic analyses, with high statistical
support from bootstrap and posterior probability. Different
studies indicate Blepharocalycinae in different positions
within Myrteae (see also Murillo-A et al. 2013), and its phy-
logenetic position within the tribe remains unresolved (Lucas
et al. 2007, 2019; Vasconcelos et al. 2017b).
DecasperminaeDecasperminae is the only subtribe in
Myrteae restricted to the Australasian and Pacific geographic
regions (Lucas et al. 2007; Vasconcelos et al. 2017b). Its flowers
commonly present a pinkish display (Fig. 11GI), distinct from
the usually white corollas of Neotropical subtribes. Possibly
due to its older age and broad geographical distribution
(Vasconcelos et al. 2017b), few morphological characters are
exclusive and constant enough to be defined as diagnostic in
the group. In general, pentamery is the most common perianth
arrangement, although tetramerous flowers are found in
Octamyrtus,Rhodamnia, some species of Decaspermum and
Pilidiostigma (Snow 2004), and in the New Caledonian species
Rhodomyrtus andromedoides Pancher ex Guillaumin (Scott
Fig. 10. Diversity of floral display strategies in Myrteae. A. Protogyny in Luma apiculata. B. Red showy flowers of the bird-pollinated Feijoa
sellowiana. C. Brush-blossom display in Eugenia bunchosiifolia (E. sect. Speciosae). D. Petaloid display in Ugni candolei. Scale bar 5ca. 10 mm.
VASCONCELOS ET AL.: FLORAL DIVERSITY IN MYRTEAE 5832019]
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Fig. 11. Simplified phylogeny of Myrteae (i), field pictures (ii), and floral diagrams (iii) of selected species. Topology is a summary of total molecular
evidence (nuclear and plastidial) found by Lucas et al. (2005, 2007, 2011); Costa (2009); De-Carvalho (2013); Mazine et al. (2014); B¨unger et al. (2016), Santos
et al. (2017) and Vasconcelos et al. (2017b). Represented clades are those with strong PP (.0.95) and bootstrap (.70) support by the majority of studies.
Poorly supported relationships are collapsed into polytomies. Numbers between brackets represent estimated species diversity per tip. (A) Luma apiculata;
(B) Myrcia linearifolia (M. sect. Myrcia);(C)Myrciaria floribunda;(D)Blepharocalyx salicifolius;(E)Accara elegans; (F) Myrtus communis;(G)Rhodomyrtus
tomentosa;(H)Decaspermum vitis-idea; (I) Rhodamnia cinerea.*Lithomyrtus and Myrtella are still to be phylogenetically placed within Decasperminae. Color
code in floral diagrams: green 5sepals, red 5petals, yellow 5androecium, orange = hypanthium, blue 5gynoecium.
SYSTEMATIC BOTANY [Volume 44584
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
1978b, 1979; Snow 2000). The fused calyx, a common feature
found in flowersof Neotropical Myrteae, appears to be absent in
subtribe Decasperminae. Staminal primordia are spread over
the entire hypanthium, resulting in straight stamens in the bud
(Vasconcelos et al. 2015). Locule number is variable, but the
most common pattern is trilocular. The unilocular ovary of
Rhodamnia (Scott 1979) appears derived from incomplete fusion
of the bi- or tricarpelar ovary (Figs. 5D, 11I), resulting in a
parietal arrangement. Ovule organization on the placenta is
mostly uniseriate, giving a lamelliform aspect to the placenta in
bilocular species (terminology used by Snow et al. 2003). Gossia
is unusual in the sense that it presents a multiseriate arrange-
ment of ovules over the placenta (Snow et al. 2003).
The clade formed by Rhodomyrtus (a polyphyletic genus; see
Snow et al. 2011), Octamyrtus,Kanakomyrtus,Pilidiostigma, and
Archirhodomyrtus (KARPOclade, supported by PP .0.95
and bootstrap .90, Snow et al. 2011; Vasconcelos et al. 2017b)
has several shared floral modifications. These include a thin,
partial to nearly complete membranous partition between
most or all ovules (named a pseudo-septum; Scott 1978b,
1978c) and peltate stigmas. Flowers of Octamyrtus are similar
to those of Rhodomyrtus in general morphology, the main
difference being an additional whorl of longer petals that gives
its display a characteristic tubular appearance (Craven et al.
2016), and the stamens and style often projecting well above
the tips of the corolla. Although still to be sampled in phy-
logenetic studies, Myrtella and Lithomyrtus have clear traits of
Decasperminae and thus are treated as such here and in Lucas
et al. (2019). These two genera present a non-elongated hy-
panthium, bi- to tetralocular ovaries, and uniseriate ovule
arrangement on the placenta (Scott 1978a, 1979; Snow and
Guymer 1999). The lack of a capitate/peltate stigma and
pseudo-septum between ovules suggest that their position will
be other than within the KARPO clade.
EugeniinaeEugeniinae includes Myrcianthes,Eugenia, and
several small genera that are nested in the latter according to
molecular evidence (Mazine et al. 2014; Byng et al. 2016;
Vasconcelos et al. 2017b). Some of these have recently un-
dergone synonymization (e.g. Calycorectes,Monimiastrum,
Hexachlamys, Meteoromyrtus) or are in the process of it
(Calyptrogenia,Pseudanamomis,Hottea). Whereas Myrcianthes
is a relatively small genus mostly from the Andean region
(Grifo 1992), Eugenia, in its broader circumscription, is the
largest and most widespread genus of Myrteae, with ca. 1000
species distributed throughout the Neotropics, New Caledo-
nia, Madagascar, Continental Africa, and India (Van der
Merwe et al. 2005; Mazine et al. 2014, 2016; Byng et al. 2016;
Wilson and Heslewood 2016). Myrcianthes generally is pen-
tamerous, whereas most Eugenia are tetramerous (with the
notable exception of E. sect. Hexachlamys, Mazine et al. 2016).
In both genera staminal primordia cover the whole hypan-
thium during flower development, resulting in straight sta-
mens in the bud in most cases (Vasconcelos et al. 2015, 2018).
Species formely treated in Monimiastrum have stamens cov-
ering the whole inner layer of their highly elongated hypan-
thia, resulting in somewhat curved stamens that are
exceptional in Eugenia (see Scott 1980; Snow 2008; Giaretta
et al. 2019). Ovaries are mostly bilocular, with a small central
placenta attached to a single point in the septum (Landrum
and Kawasaki 1997). Ovule arrangement over the placenta for
the great majority is multiseriate.
Floral morphology is homogeneous throughout the vast
majority of the ca. 1000 species of Eugenia (Figs. 12A, B) and,
traditionally, morphological characters that separate sections
within the genus are related to non-floral aspects (e.g. seeds
and inflorescences; Mazine et al. 2014, 2016). However, some
floral variation may have systematic relevance. These include
presence of trichomes and their location (Faria 2014), the
length of the style (Vasconcelos et al. 2018), and calyx modi-
fications (aspect and fusion; B ¨unger et al. 2016; Giaretta et al.
2019). Section Pilothecium, for example, can be identified by the
presence of hairs in the ovary (a character shared with some
genera of Pimentinae; Faria 2014), whereas most members of
Eugenia sect. Umbellatae have styles that are twice as long as the
stamens, compared to styles of similar size to stamens in other
clades (Vasconcelos et al. 2018). Furthermore, sect. Phyllocalyx is
recognizable by the leafy aspects of sepals, which are mor-
phologically similar to their bracteoles (Berg 18551856; B ¨unger
et al. 2016). Some fundamental differences in the gynoecium
were observed in two lineages arising from the deepest nodes of
Eugenia.Eugenia sects. Pseudeugenia and Pilothecium are ex-
ceptional in having apparent uniseriate arrangement of ovules
over the placenta in some species (e.g. Eugenia stipitata,
T. Vasconcelos pers. obs.) and frequently more than two locules
(Faria 2014; Mazine et al. 2016), resembling some genera in the
sister group Pimentinae (e.g. Campomanesia).
LuminaeLuminae includes four genera of distinct mor-
phology and taxonomic history. Myrceugenia, the largest of
them with ca. 50 recognized species (WCSP 2018), has histor-
ically been associated with Myrciinae based on embryo char-
acters (McVaugh 1968), but it grouped with Luma, Temu, and
Nothomyrcia in recent phylogenetic studies (Lucas et al. 2007;
Murillo-A and Ruiz 2011; Murillo-A et al. 2012; Vasconcelos
et al. 2017a). The genera share common floral traits, including
tetramery, discontinuous staminalrings giving stamens a semi-
folded posture prior to anthesis, and twofour locular ovaries
with uniseriate ovule organization (Fig. 11A). The style is
usually long and folds on top of the anthers in the bud.
MyrtinaeThe close relationship between the only Medi-
terranean Myrtaceae, the genus Myrtus, and a group of
Neotropical genera has been recently clarified (see Vascon-
celos et al. 2017b). These four genera (Myrtus,Calycolpus,
Accara, and Chamguava) form the recircumscribed subtribe
Myrtinae and share multiseriate ovule organization over
subpeltate but elongated placentas, in contrast to other sym-
patric Myrteae genera with multiseriate ovules attached to a
minute placenta (e.g. Eugenia; Landrum 1990, 1991; Landrum
and Kawasaki 1997). The perianth is pentamerous in Myrtus
(Fig. 11F) and Calycolpus, but tetramerous in Accara (Fig. 11E)
and Chamguava.Myrtus frequently has an additional but re-
duced whorl of petals (Mulas and Fadda 2004; T. Vasconcelos
pers. obs.).
PimentinaeThe genera of Pimentinae present, along with
Decasperminae, the broadest flower diversity in Myrteae.
Flowers are either tetramerous or pentamerous, but variation
is common even at the species level (e.g. in Psidium guajava,
Campomanesia adamantium; see Fig. 2G). Locularity ranges from
bilocular to multilocular, sometimes reaching 18 locules in
some Campomanesia (Landrum 1986), but locularity also is
commonly variable at lower taxonomic levels. Stamens are
mostly straight in the bud, with the exception of Pimenta,
where the stamen primordia developing in a discontinuous
ring result in a semi-folded posture in the bud (Vasconcelos
et al. 2015; Fig. 3B). Stigmas can be capitate, which sometimes
is a good character to separate Pimentinae from other sym-
patric Myrteae (Bentham 1869). Psidium,Myrrhinium, and
VASCONCELOS ET AL.: FLORAL DIVERSITY IN MYRTEAE 5852019]
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Fig. 12. Simplified phylogeny of Myrteae (i), field pictures (ii) and floral diagrams (iii) of selected species. Topology is a summary of total molecular evidence
(nuclear and plastidial) found by Lucas et al. (2005, 2007, 2011); Costa (2009); De-Carvalho (2013); Mazine et al. (2014); B
unger et al. (2016), Santos et al. (2017) and
Vasconcelos et al. (2017b). Represented clades are those with strong PP (.0.95) and bootstrap (.70) support by the majority of studies. Poorly supported relationships
are collapsed into polytomies. Numbers between brackets represent estimated species diversity. (A) Eugenia bimarginata (E.sect.Umbellatae); (B) Eugenia stipitata (E.sect.
Pilothecium); (C) Psidium guajava;(D)Myrrhinium atropurpureum;(E)Campomaneia adamantium;(F)Feijoa sellowiana;(G)Ugni candolei. Color code in floral diagrams:
green 5sepals, red 5petals, yellow 5androecium, orange 5hypanthium, blue 5gynoecium. Photo in (D) by I. R. Costa.
SYSTEMATIC BOTANY [Volume 44586
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Mosiera form a strongly supported clade (Vasconcelos et al.
2017b) but differ in some fundamental aspects of flower or-
ganization. Mosiera and most Psidium (e.g. Psidium guajava,
P. guineense; Fig. 12C) have a multiseriate ovule arrangement
on the placenta, and locules that can be only partially fused
(Landrum 1992). Myrrhinium presents an apparent uniseriate
ovule arrangement, a strong reduction in number of stamens
(Landrum and Kawasaki 1997), and structures resembling
staminodes on the base of the hypanthium that may represent
aborted filaments (crosses in floral diagram, Fig. 12D). Flowers
of Feijoa are distinct from the other Pimentinae and Myrteae by
their hairy anthers (unique amongst the genera) and distinct
multilocular ovaries wherein the central axis is not fused,
giving the impression of a unilocular chamber (Fig. 12F;
Dettori and Di Gaetano 1991).
UgninaeUgninae is the smallest subtribe treated here. It
represents ca. 15 species distributed in five small genera (Lucas
et al. 2007; Wilson 2011; Vasconcelos et al. 2017b). Merosity is
useful for generic delimitation: Ugni and Neomyrtus are pen-
tamerous while Myrteola,Lophomyrtus, and Lenwebbia are
mostly tetramerous (Landrum 1988a, 1988b; Snow et al. 2003).
Stamens are mostly straight in the bud (Vasconcelos et al.
2015). Ovaries are either bi-or tri-locular and ovule arrange-
ment is uni- or bi-seriate, never multiseriate. Ugni has an
overall distinct floral morphology from other Ugninae genera,
with a campanulate corolla formed by relatively large petals,
which occur on strongly reflexed pedicels, resembling some
Ericaceae and members of Uromyrtus (Fig. 12G; Wilson 2011);
the red anthers are sagitate and longitudinally covered in oil
glands. Lenwebbia has an unusual androecium morphology.
The staminal base is slightly fused and the discontinuous rings
are similar to those of the Luminae, giving the stamens a semi-
folded aspect in the bud (Vasconcelos et al. 2015). Myrteola,a
genus with distribution in Patagonia and the Falkland Islands,
presents small flowers with few, small stamens but a relatively
high number of ovules, increasing the ovule/pollen ratio that
may characterize a selection-induced evolutionary change in
breeding system (Cruden 1977). Neomyrtus and Lophomyrtus,
the only Myrteae genera native to New Zealand, form a clade
in the phylogeny (Lucas et al. 2007). In overall flower aspect,
however, Neomyrtus has some similarities to Ugni (larger
glandulous anthers, biseriate ovules on the placenta), while
Lophomyrtus (Belsham and Orlovich 2002) resembles Lenwebbia
(stamens with a somewhat semi-folded posture in the bud,
uniseriate ovules on the placenta).
Incertae SedisAccording the new subtribe circumscrip-
tion of Lucas et al. (2019), three genera are considered incertae
sedis (unplaced) in Myrteae: Amormytus,Myrtastrum, and
Amormyrtella. The first two have been included in previous
phylogenetic studies, but uncertain placement challenges their
inclusion in a particular subtribe (Lucas et al. 2005, 2007;
Vasconcelos et al. 2017b; Murillo-A et al. 2012). The last one is
yet to be included in molecular analysis so its phylogenetic
position is unknown. Myrtastrum, a mono-specific genus en-
demic to New Caledonia, has an unusual floral structure
relative to other extant Myrteae. The stigma is capitate, but the
style is shorter than the anthers (protoandry), a pattern not
observed elsewhere in the tribe. Petals are shorter than sepals,
restricting the degree to which the corolla reflexes (T. Vas-
concelos pers. obs.). The gynoecium is three locular with in-
complete fusion and ovule arrangement and has been
described as biseriate (Scott 1979), but seems to be in fact
uniseriate. Amomyrtella, a genus from the Andes, is described
as a taxon of morphologically distinct flowers (Landrum and
Morocho 2011), with anthers up to 2 mm and trilocular ovaries
with biseriate ovule arrangement on placenta. Even though
such descriptions are similar to those of some Ugninae
(e.g. Ugni), preliminary results from ITS sequencing provide
evidence that Amomyrtella will be placed within Pimentinae
(T. Vasconcelos, unpublished data).
Discussion
The general floral ground plan of subtribes in Myrteae does
not differ significantly and is similar to that of other tribes of
Myrtaceae (Wilson 2011), but combinations of floral traits are
somewhat diagnostic of subtribes. In terms of systematic
relevance, the general sequence in order of floral character
stability from higher to lower taxonomic levels is: androecium
structure (stamen primordia distribution over the hypanthium
and their posture in the pre-anthetic bud), gynoecium struc-
ture (origin of placenta and ovule arrangement), and lastly
perianth structure (number of parts and degree of fusion).
In groups with uniform traits such as Myrteae, careful
morphological studies that reveal discrete changes responsible
for flexibility of reproductive strategies are the most relevant
for evolutionary understanding. In Myrteae, these include
subtle herkogamic effects, changes from brush-blossom to a
petaloid display (and vice versa) and poorly understood
changes in the evolution of floral features that affect both
phases of reproduction (i.e. pollination and seed dispersal),
such as androdioecy and ovule oversupply (i.e. changes in the
gynoecium seem to constrain the number of ovules that can
form seeds). Variation in flower size and number per in-
florescence, total number of ovules per flower, and number
and size of anthers (a proxy for pollen investment) also are
likely to affect diversification rates in different ways and
should be studied in conjunction with phylogenies in future
research. The gynoecium, a hidden and difficult structure to
analyze, appears to be especially meaningful in the evolution
and systematics of Myrteae. Ovary development appears to
influence the number of seeds, the development of the em-
bryos, and to balance self vs. cross-pollination (by strong style
elongation in some groups) and pollen competition (Mulcahy
and Mulcahy 1987). More studies of ovary structure and
evaluation of its role in these processes will be profitable.
Furthermore, fine changes in one floral whorl lead to spatial
changes that affect the development of the next whorl (e.g.
Fig. 4), showing the importance of considering the whole
flower system in conjunction as a single unit under natural
selection.
Acknowledgments
We are grateful to all taxonomists that helped with field expeditions,
collection of samples and discussion of floral features in Myrteae, par-
ticularly to R. Aguilar, B. S. Amorim, L. Barrab´e, D. Bogarin, K. Campbell,
J. E. Q. Faria, A. Giaretta, D. F. Lima, B. Peguero, C. E. B. Proença,
P. O. Rosa, D. Santamaria-Aguilar, M. F. Santos and J. Soewarto. We are
indebted to P. Endress, L. R. Landrum, L. P. Queiroz, N. Snow and
A. Wingler who read earlier versions of this manuscript and provided
helpful comments and suggestions. This research was funded by CAPES
(SwB number 7512-13-9) and the Emily Holmes Memorial Scholarship.
Author Contributions
All authors contributed with designing the research, collecting the data,
and writing of the manuscript.
VASCONCELOS ET AL.: FLORAL DIVERSITY IN MYRTEAE 5872019]
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Literature Cited
Alcantara, S. and L. G. Lohmann. 2010. Evolution of floral morphology and
pollination system in Bignonieae (Bignoniaceae). American Journal of
Botany 97: 782796.
Amorim, B. S. and M. Alves. 2012. A new species of Eugenia (Myrteae,
Myrtaceae) from the Brazilian Atlantic forest. Systematic Botany 37:
694698.
Ashton, P. 2011. Myrtaceae in Tree Flora of Sabah and Sarawak, vol. 7,
eds. E. Soepadmo, L. G. Saw, R. C. K. Chung, R. Kiew. Forest Research
Institute Malaysia.
Beech, E., M. Rivers, S. Oldfield, and P. P. Smith. 2017. GlobalTreeSearch:
The first complete global database of tree species and country dis-
tributions. Journal of Sustainable Forestry 36: 454489.
Belsham, S. R. and D. A. Orlovich. 2002. Development of the hypanthium
and androecium in New Zealand Myrtoideae (Myrtaceae). New
Zealand Journal of Botany 40: 687695.
Belsham, S. R. and D. A. Orlovich. 2003. Development of the hypanthium
and androecium in South American Myrtoideae (Myrtaceae). New
Zealand Journal of Botany 41: 161169.
Bentham, G. 1869. Notes on Myrtaceae. Botanical Journal of the Linnean
Society 10: 101166.
Berg, O. 18551856. Revisio Myrtacearum Americae. Linnaea 27: 1472.
Breedlove, D. E. and P. R. Ehrlich. 1972. Coevolution: Patterns of legume
predation by a lycaenid butterfly. Oecologia 10: 99104.
Buchmann, S. L. and J. H. Cane. 1989. Bees assess pollen returns while
sonicating Solanum flowers. Oecologia 81: 289294.
unger, M. O., F. F. Mazine, F. Forest, M. Leandro, J. Stehmann, and
E. J. Lucas. 2016. The evolutionary history of Eugenia sect. Phyllocalyx
(Myrtaceae) corroborates historically stable areas in the southern
Atlantic forests. Annals of Botany 118: 12091223.
Byng, J. W., F. Barthelat, N. Snow, and B. Bernadini. 2016. Revision of
Eugenia and Syzygium (Myrtaceae) from the Comoros archipelago.
Phytotaxa 252: 163184.
Cameron, S. A. 2004. Phylogeny and biology of neotropical orchid bees
(Euglossini). Annual Review of Entomology 49: 377404.
Cardoso, D., T. S ¨arkinen, S. Alexander, A. M. Amorim, V. Bittrich, M. Celis,
D. C. Douglas, P. Fiaschi, V. A. Funk, L. L. Giacomin, R. Goldenberg,
G. Heiden, J. Iganci, C. L. Kelloff, S. Knapp, H. C. Lima,
A. F. P. Machado, R. M. Santos, R. Mello-Silva, F. A. Michelangeli,
J. Mitchell, P. Moonlight, P. L. R. de Moraes, S. A. Mori, T. S. Nunes,
T. D. Pennington, J. R. Pirani, G. T. Prance, L. P. de Queiroz, A. Rapini,
R. Riina, C. A. V. Rincon, N. Roque, G. Shimizu, M. Sobral,
J. R. Stehmann, W. D. Stevens, C. M. Taylor, M. Trov ´o,
C. van den Berg, H. van der Werff, P. L. Viana, C. E. Zartman, and
R. C. Forzza. 2017. Amazon plant diversity revealed by a taxonom-
ically verified species list. Proceedings of the National Academy of Sciences
USA 114: 1069510700.
Carrucan, A. E. and A. N. Drinnan. 2000. The ontogenetic basis for floral
diversity in the Baeckea sub-group (Myrtaceae). Kew Bulletin 55:
593613.
Chapman, G. P. 1964. Some aspects of dioecism in pimento (allspice).
Annals of Botany 28: 451458.
Ciccarelli, D., F. Garbari, and A. M. Pagni. 2008. The flower of Myrtus
communis (Myrtaceae): Secretory structures, unicellular papillae, and
their ecological role. Flora-Morphology, Distribution.Functional Ecology
of Plants 203: 8593.
Costa, I. R. 2009. Estudos Evolutivos em Myrtaceae: Aspectos Citotaxon ˆomicos e
Filogen´eticos em Myrteae, Enfatizando Psidium eGˆeneros Relacionados.
Ph.D. thesis. Universidade de Campinas.
Craven, L. A. 2006. Myrtaceae of Papua. Pp. 429434 in The Ecology of Papua,
eds. A. J. Marshall and B. M. Beehler. Singapore: Periplus Editions.
Craven, L. A., S. Sunarti, D. Mudiana, and T. Yulistyarini. 2016. Identifi-
cation key to the indigeneous Indonesian genera of Myrtaceae. Flo-
ribunda 2: 8994.
Cruden, R. W. 1977. Pollen-ovule ratios: A conservative indicator of
breeding systems in flowering plants. Evolution 31: 3246.
De-Carvalho, P. S. 2013. Ecologia e Relaç~
oes Filogen´eticas de Blepharocalyx
salicifolius (Kunth) O.Berg (Myrtaceae). Ph.D. thesis. Universidade de
Brasilia.
Dettori, M. T. and R. Di Gaetano. 1991. Feijoa sellowiana: Floral biology.
Advances in Horticultural Science 5: 1114.
de Vos, J. M., C. E. Hughes, G. M. Schneeweiss, B. R. Moore, and E. Conti.
2014. Heterostyly accelerates diversification via reduced extinction in
primroses. Proceedings. Biological Sciences 281: 20140075.
Endress, P. K. 1994. Diversity and Evolutionary Biology of Tropical Flowers.
Cambridge, UK: Cambridge University Press.
Evert, R. F. 2006. Esaus Plant Anatomy: Meristems, Cells, and Tissues of the
Plant Body: Their Structure, Function, and Development. Hoboken: John
Wiley and Sons.
Faria, J. E. Q. 2014. Revis~
ao Taxonˆomica e Filogenia de Eugenia sect. Pilo-
thecium (Kiaersk.) D. Legrand (Myrtaceae). Ph.D. thesis. Brazil: Uni-
versidade de Brasilia.
Foster, S. A. 1986. On the adaptive value of large seeds for tropical moist
forest trees: a review and synthesis. Botanical Review 52: 260299.
Françoso, R. D., R. F. Haidar, and R. B. Machado. 2016. Tree species of
South America central savanna: Endemism, marginal areas and the
relationship with other biomes. Acta Botanica Bras´
ılica 30: 7886.
Giaretta, A., L. F. T. de Menezes, and A. L. Peixoto. 2015. Diversity of
Myrtaceae in the southeastern Atlantic forest of Brazil as a tool for
conservation. Brazilian Journal of Botany 38: 175185.
Giaretta, A., T. N. C. Vasconcelos, F. F. Mazine, J. E. Q. Faria, R. Flores,
Holst, P. T. Sano, P. T. and E. Lucas. 2019. Calyx (con)fusion in the
hyper-diverse genus Eugenia (Myrtaceae): Parallel evolution of un-
usual flower patterns. Molecular Phylogenetics and Evolution https://
doi.org/10.1016/j.ympev.2019.106553.
Gressler, E., M. A. Pizo, and L. P. C. Morellato. 2006. Polinizaç~
ao e dis-
pers~
ao de sementes em Myrtaceae do Brasil. Brazilian Journal of Botany
29: 509530.
Grifo, F. T. 1992. A Revision of Myrcianthes Berg (Myrtaceae). Ph.D. thesis.
Ithaca, New York: Cornell University.
Harthman, V. C., L. A. de Souza, and E. J. Lucas. 2018. Characters of the
inferior ovary of Myrteae (Myrtaceae) and their implication in the
evolutionary history of the tribe. Australian Systematic Botany 31:
252261.
Johnson, L. A. S. and B. G. Briggs. 1984. Myrtales and Myrtaceae A
phylogenetic analysis. Annals of the Missouri Botanical Garden 71:
700756.
Kausel, E. 1956. Beitrag zur Systematik der Myrtaceen. Stockholm: Almqvist &
Wiksell.
Kay, K. M., P. A. Reeves, R. G. Olmstead, and D. W. Schemske. 2005. Rapid
speciation and the evolution of hummingbird pollination in Neo-
tropical Costus subgenus Costus (Costaceae): Evidence from nrDNA
ITS and ETS sequences. American Journal of Botany 92: 18991910.
Kevan, P. G. and A. J. Lack. 1985. Pollination in a cryptically dioecious plant
Decaspermum parviflorum (Lam.) AJ Scott (Myrtaceae) by pollen-
collecting bees in Sulawesi, Indonesia. Biological Journal of the Linnean
Society. Linnean Society of London 25: 319330.
Kriebel, R. and M. A. Zumbado. 2014. New reports of generalist insect
visitation to flowers of species of Miconia (Miconieae: Melastomataceae)
and their evolutionary implications. Brittonia 66: 396404.
Landrum, L. R. 1981a. A monograph of the genus Myrceugenia (Myrtaceae).
Flora Neotropica 29. New York: New York Botanical Garden.
Landrum, L. R. 1981b. The phylogeny and geography of Myrceugenia
(Myrtaceae). Brittonia 33: 105129.
Landrum, L. R. 1982. The development of the fruits and seeds of Cam-
pomanesia (Myrtaceae). Brittonia 34: 220224.
Landrum, L. R. 1984. Taxonomic implications of the discovery of calyptrate
species of Myrceugenia (Myrtaceae). Brittonia 36: 161166.
Landrum, L. R. 1986. Campomanesia, Pimenta, Blepharocalyx, Legrandia, Acca,
Myrrhinium,andLuma (Myrtaceae). Flora Neotropica 45. New York:
New York Botanical Garden.
Landrum, L. R. 1988a. The myrtle family (Myrtaceae) in Chile. Proceedings
of the California Academy of Sciences 45: 277317.
Landrum, L. R. 1988b. Systematics of Myrteola (Myrtaceae). Systematic
Botany 13: 120132.
Landrum, L. R. 1990. Accara: A new genus of Myrtaceae, Myrtinae from
Brazil. Systematic Botany 15: 221225.
Landrum, L. R. 1991. Chamguava: a new genus of Myrtaceae (Myrtinae)
from Mesoamerica. Systematic Botany 16: 2129.
Landrum, L. R. 1992. Mosiera (Myrtaceae) in Mexico and Mesoamerica.
Novon 2: 2629.
Landrum, L. R. and J. Bonilla. 1996. Anther glandularity in the American
Myrtinae (Myrtaceae). Madro~
no 43: 5868.
Landrum, L. R. and M. K. Kawasaki. 1997. The genera of Myrtaceae in
Brazil: An illustrated synoptic treatment and identification keys.
Brittonia 49: 508536.
Landrum, L. R. and V. Morocho. 2011. A new combination based on
Myrcianthes irregularis (Myrtaceae) a new genus for Ecuador. Journal
of the Botanical Research Institute of Texas 5: 105107.
Linnaeus, C. V. 1753. Species Plantarum. Stockholm: Laurentii Salvii,
Holmiae.
SYSTEMATIC BOTANY [Volume 44588
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Lucas, E. J. and M. O. B ¨unger. 2015. Myrtaceae in the Atlantic forest: Their
role as a modelgroup. Biodiversity and Conservation 24: 21652180.
Lucas, E. J., S. R. Belsham, E. M. Nic Lughadha, D. A. Orlovich,
C. M. Sakuragui, M. W. Chase, and P. G. Wilson. 2005. Phylogenetic
patterns in the fleshy-fruited Myrtaceae: Preliminary molecular evi-
dence. Plant Systematics and Evolution 251: 3551.
Lucas, E. J., S. A. Harris, F. F. Mazine, S. R. Belsham, E. M. Nic Lughadha,
A. Telford, P. E. Gasson, and M. W. Chase. 2007. Suprageneric
phylogenetics of Myrteae, the generically richest tribe in Myrtaceae
(Myrtales). Taxon 56: 11051128.
Lucas, E. J., K. Matsumoto, S. A. Harris, E. M. Nic Lughadha, B. Bernardini,
and M. W. Chase. 2011. Phylogenetics, morphology, and evolution of
the large genus Myrcia s.l. (Myrtaceae). International Journal of Plant
Sciences 172: 915934.
Lucas, E. J., B. S. Amorim, D. F. Lima, A. R. Lima-Lourenço,
E. Nic Lughadha, C. E. B. Proença, A. S. Rosario, L. L. Santos,
M. F. Santos, M. C. Souza, V. G. Staggemeier, T. N. C. Vasconcelos,
and M. Sobral. 2018. A new infra-generic classification of the species-
rich Neotropical genus Myrcia sl. Kew Bulletin 73: 9.
Lucas, E. J., B. Holst, M. Sobral, F. F. Mazine, E. M. Nic Lughadha,
C. E. B. Proença, I. R. Costa, and T. N. C. Vasconcelos. 2019. A new
subtribal classification of tribe Myrteae (Myrtaceae). Systematic Botany
44: 560569.
Martos, L., A. T. O. F. Galan, L. A. D. Souza, and K. S. M. Mour~
ao. 2017. The
flower anatomy of five species of Myrteae and its contribution to the
taxonomy of Myrtaceae. Acta Botanica Bras´
ılica 31: 4250.
Mazine, F. F., V. C. Souza, M. Sobral, F. Forest, and E. J. Lucas. 2014. A
preliminary phylogenetic analysis of Eugenia (Myrtaceae: Myrteae),
with a focus on Neotropical species. Kew Bulletin 69: 9497.
Mazine, F. F., M. O. B ¨unger, J. E. Q. Faria, E. J. Lucas, and V. C. Souza. 2016.
Sections in Eugenia (Myrteae, Myrtaceae): Nomenclatural notes and a
key. Phytotaxa 289: 225236.
McVaugh, R. 1968. The genera of American Myrtaceae: An interim report.
Taxon 17: 354418.
Miller, G. A. 1986. Pubescence, floral temperature and fecundity in species
of Puya (Bromeliaceae) in the Ecuadorian Andes. Oecologia 70:
155160.
Mulcahy, D. L. and G. B. Mulcahy. 1987. The effects of pollen competition.
American Scientist 75: 4450.
Mulas, M. and A. Fadda. 2004. First observations on biology and organ
morphology of myrtle (Myrtus communis L.) flower. Agricoltura
Mediterranea 134: 223235.
Murillo-A, J. and E. Ruiz. 2011. Revalidaci ´on de Nothomyrcia (Myrtaceae),
un g´enero end´emico del Archipi´elago de Juan Fern ´andez. Gayana.
Bot´anica 68(2): 129134.
Murillo-A, J., E. Ruiz-P, L. R. Landrum, T. F. Stuessy, and M. H. J. Barfuss.
2012. Phylogenetic relationships in Myrceugenia (Myrtaceae) based on
plastid and nuclear DNA sequences. Molecular Phylogenetics and
Evolution 62: 764776.
Murillo-A, J., T. F. Stuessy, and E. Ruiz. 2013. Phylogenetic relationships
among Myrceugenia, Blepharocalyx,andLuma (Myrtaceae) based on
paired-sites models and the secondary structures of ITS and ETS
sequences. Plant Systematics and Evolution 299: 713729.
Murray-Smith, C., N. A. Brummitt, A. T. Oliveira-Filho, S. Bachman,
J. Moat, E. M. Nic Lughadha, and E. J. Lucas. 2009. Plant diversity
hotspots in the Atlantic coastal forests of Brazil. Conservation Biology
23(1): 151163.
Nic Lughadha, E. 1998. Preferential outcrossing in Gomidesia (Myrtaceae) is
maintained by a post-zygotic mechanism. Pp 363379 in Reproductive
Biology, eds. S. J. Owens and P. J. Rudall. Richmond, UK: Royal Botanic
Gardens Kew.
Nic Lughadha, E. and C. Proença. 1996. A survey of the reproductive
biology of the Myrtoideae (Myrtaceae). Annals of the Missouri Botanical
Garden 83: 480503.
OBrien, S. P., B. R. Loveys, and W. J. R. Grant. 1996. Ultrastructure and
function of floral nectaries of Chamelaucium uncinatum (Myrtaceae).
Annals of Botany 78: 189196.
Oliveira-Filho, A. T. and M. A. L. Fontes. 2000. Patterns of floristic dif-
ferentiation among atlantic forests in southeastern Brazil and the
influence of climate. Biotropica 32: 793810.
Parra-O, C. and A. F. Bohorquez-Osorio. 2016. Effectiveness of DNA
barcoding markers in the description of a new and unusual calyptrate
species of Myrcianthes (Myrtaceae). Phytotaxa 284: 203210.
Pimentel, R. R., A. D. Nat´alia, P. Barreira, D. P. Spala, N. B. Cardim,
M. C. Souza, B. S´a-Haiad, S. R. Machado, J. F. Rocha, and
L. D. R. Santiago-Fernandes. 2014. Development and evolution of the
gynoecium in Myrteae (Myrtaceae). Australian Journal of Botany 62:
335346.
Prenner, G., R. M. Bateman, and P. J. Rudall. 2010. Floral formulae updated
for routine inclusion in formal taxonomic descriptions. Taxon 59:
241250.
Proença, C. E. B. 1992. Buzz-pollination older and more wide-spread than
we think? Journal of Tropical Ecology 8: 115120.
Proença, C. E. B., E. M. Nic Lughadha, E. J. Lucas, and E. M. Woodgyer.
2006. Algrizea (Myrteae, Myrtaceae): A new genus from the highlands
of Brazil. Systematic Botany 31: 320326.
Rocca, M. A. and M. Sazima. 2010. Beyond hummingbird-flowers: The
other side of ornithophily in the Neotropics. Oecologia Australis 14:
6799.
Roitman, G., N. H. Montaldo, and D. Medan. 1997. Pollination biology of
Myrrhinium atropurpureum (Myrtaceae): Sweet, fleshy petals attract
frugivorous birds. Biotropica 29: 162168.
Ronse De Craene, L. P. 2008. Homology and evolution of petals in the core
eudicots. Systematic Botany 33: 301325.
Ronse De Craene, L. P. 2010. Floral Diagrams: An Aid to Understanding Flower
Morphology and Evolution. Cambridge, UK: Cambridge University Press.
Ronse De Craene, L. P. and E. F. Smets. 1991. The impact of receptacular
growth on polyandry in the Myrtales. Botanical Journal of the Linnean
Society 105: 257269.
Ronse De Craene, L. P. and E. F. Smets. 1992. Complex polyandry in the
Magnoliatae: definition, distribution and systematic value. Nordic
Journal of Botany 12: 621649.
Ronse De Craene, L. P. and E. F. Smets. 1993. The distribution and sys-
tematic relevance of the androecial character polymery. Botanical
Journal of the Linnean Society 113: 285350.
Rosenheim, J. A., S. J. Schreiber, and N. M. Williams. 2016. Does an
oversupplyof ovules cause pollen limitation? The New Phytologist
210: 324332.
Santos, M. F., E. J. Lucas, P. T. Sano, S. Buerki, V. G. Staggemeier, and
F. Forest. 2017. Biogeographical patterns of Myrcia s.l. (Myrtaceae) and
their correlation with geological and climatic history in the Neo-
tropics. Molecular Phylogenetics and Evolution 108: 3448.
Scott, A. J. 1978a. A new species of Myrtella (Myrtaceae) from Australia
and a synopsis of the genus. Kew Bulletin 33: 299302.
Scott, A. J. 1978b. A revision of Octamyrtus (Myrtaceae). Kew Bulletin 33:
303309.
Scott, A. J. 1978c. A revision of Rhodomyrtus (Myrtaceae). Kew Bulletin 33:
311329.
Scott, A. J. 1979. A revision of Rhodamnia (Myrtaceae). Kew Bulletin 33:
429459.
Scott, A. J. 1980. Notes on Myrtaceae in the Mascarenes with some re-
combinations for taxa from Aldabra, Malaya, New Caledonia. Kew
Bulletin 34: 473498.
Schupp, E. W. 1993. Quantity, quality and the effectiveness of seed dis-
persal by animals. Vegetatio 107/108: 1529.
Snow, N. 2000. Systematic conspectus of Australasian Myrtinae (Myrta-
ceae). Kew Bulletin 55: 647654.
Snow, N. 2004. Systematics of Pilidiostigma (Myrtaceae). Systematic Botany
29: 393406.
Snow, N. 2008. Studies of Malagasy Eugenia (Myrtaceae) I: Two new
species from the Masoala Peninsula and generic transfers from
Monimiastrum.Systematic Botany 33: 343348.
Snow, N. 2009. Kanakomyrtus (Myrtaceae): A new endemic genus from
New Caledonia with linear stigma lobes and baccate fruits. Systematic
Botany 34: 330344.
Snow, N. and G. P. Guymer. 1999. Systematic and cladistic studies of
Myrtella F. Muell. and Lithomyrtus F. Muell. (Myrtaceae). Austrobaileya
5: 173208.
Snow, N. and G. P. Guymer. 2001. Revision of Australian species of
Uromyrtus (Myrtaceae) and two new combinations for New Cale-
donia. Systematic Botany 26: 733742.
Snow, N. and P. G. Wilson. 2010. New species of Eugenia and Gossia
(Myrtaceae: Myrteae) from Papua New Guinea. Telopea 12: 453461.
Snow, N., G. P. Guymer, and G. Sawvel. 2003. Systematics of Austromyrtus,
Lenwebbia, and the Australian species of Gossia (Myrtaceae). Systematic
Botany Monographs 65: 195.
Snow, N., J. McFadden, T. M. Evans, A. M. Salywon, M. F. Wojciechowski,
and P. G. Wilson. 2011. Morphological and molecular evidence of
polyphyly in Rhodomyrtus (Myrtaceae: Myrteae). Systematic Botany
36: 390404.
Sobral, M. 2003. A Fam´
ılia Myrtaceae no Rio Grande do Sul. Sao Leopoldo,
Brazil: Editora Unisinos.
VASCONCELOS ET AL.: FLORAL DIVERSITY IN MYRTEAE 5892019]
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
Sobral, M. 2005. Eugenia inversa (Myrtaceae), a new species from Esp´
ırito
Santo, Brazil. SIDA, Contributions to Botany 21(3): 14651469.
Staggemeier, V. G., J. A. F. Diniz-Filho, and L. P. C. Morellato. 2010. The
shared influence of phylogeny and ecology on the reproductive
patterns of Myrteae (Myrtaceae). Journal of Ecology 98: 14091421.
Staggemeier, V. G., J. A. F. Diniz-Filho, F. Forest, and E. J. Lucas. 2015.
Phylogenetic analysis in Myrcia section Aulomyrcia and inferences on
plant diversity in the Atlantic rainforest. Annals of Botany 115: 747761.
Staggemeier, V. G., E. Cazetta, and L. P. C. Morellato. 2017. Hyper-
dominance in fruit production in the Brazilian Atlantic rain forest: The
functional role of plants in sustaining frugivores. Biotropica 49: 7182.
Thiers, B. 2018. Index Herbariorum: A global directory of public herbaria
and associated staff. New York Botanical Gardens Virtual Herbar-
ium. http://sweetgum.nybg.org/ih.
Thornhill, A. H., G. S. Hope, L. A. Craven, and M. D. Crisp. 2012. Pollen
morphology of the Myrtaceae. Part 4: Tribes Kanieae, Myrteae and
Tristanieae. Australian Journal of Botany 60: 260289.
Van der Merwe, M. M., A. E. Van Wyk, and A. M. Botha. 2005. Molecular
phylogenetic analysis of Eugenia L. (Myrtaceae), with emphasis on
southern African taxa. Plant Systematics and Evolution 251: 2134.
Van Wyk, A. E. and T. K. Lowrey. 1988. Studies on the reproductive bi-
ology of Eugenia L. (Myrtaceae) in Southern Africa. Pp 1014 in Modern
systematic studies in African botany. Proceedings of the Eleventh Plenary
Meeting of the Association for the Taxonomic study of the Flora of Tropical
Africa, eds. P. Goldblatt and P. P. Lowry II. St. Louis: Missouri Bo-
tanical Garden.
Vasconcelos, T. N. C., G. Prenner, M. O. B ¨unger, P. S. De-Car valho,
A. Wingler, and E. J. Lucas. 2015. Systematic and evolutionary im-
plications of stamen position in Myrteae (Myrtaceae). Botanical Journal
of the Linnean Society 179: 388402.
Vasconcelos, T. N. C., G. Prenner, M. F. Santos, A. Wingler, and E. J. Lucas.
2017a. Links between parallel evolution and systematic complexity in
angiospermsA case study of floral development in Myrcia sl
(Myrtaceae). Perspectives in Plant Ecology, Evolution and Systematics
24: 1124.
Vasconcelos,T.N.C.,C.E.Proença,B.Ahmad,D.Santamari-Aguilar,
R. Aguilar, B. S. Amorim, K. Campbell, I. R. Costa, P. S. De-Carvalho,
J.E.Q.Faria,A.Giaretta,P.W.Kooij,D.F.Lima,F.F.Mazine,B.Peguero,
G.Prenner,M.F.Santos,J.Soewarto,A.Wingler,andE.J.Lucas.2017b.
Myrteae phylogeny, calibration, biogeography and diversification pat-
terns: Increased understanding in the most species rich tribe of Myrta-
ceae. Molecular Phylogenetics and Evolution 109: 113137.
Vasconcelos, T. N. C., E. J. Lucas, J. E. Q. Faria, and G. Prenner. 2018. Floral
heterochrony promotes flexibility of reproductive strategies in the
morphologically homogeneous genus Eugenia (Myrtaceae). Annals of
Botany 121: 161: 174.
Vasconcelos, T. N. C., M. Chartier, A. Martins, G. Prenner, A. Wingler,
J. Sch¨onenberger, and E. Lucas. 2019. Floral uniformity through
evolutionary time in a species-rich tree lineage. The New Phytologist
221: 15971608.
WCSP. 2018. World checklist of selected plant families. Facilitated by the
Royal Botanic Gardens, Kew. http://apps.kew.org/wcsp/.
Weberling, F. 1989. Morphology of Flowers and Inflorescences. Cambridge,
UK: Cambridge University Press.
White, C. T. 1951. Some noteworthy Myrtaceae from the Moluccas, New
Guinea, and the Solomon Islands. Journal of the Arnold Arboretum
32: 139149.
Wilson, C. E., F. Forest, D. S. Devey, and E. J. Lucas. 2016. Phylogenetic
relationships in Calyptranthes (Myrtaceae) with particular emphasis on
its monophyly relative to Myrcia s.l. Systematic Botany 41: 378386.
Wilson, P. G. 2011. Myrtaceae. Pp 212271 in The Families and Genera of
Vascular Plants, vol. 10, ed. K. Kubitzki. Netherlands: Springer.
Wilson, P. G. and M. M. Heslewood. 2016. Phylogenetic position of
Meteoromyrtus (Myrtaceae). Telopea 19: 4555.
Wilson, P. G., M. M. OBrien, M. M. Heslewood, and C. J. Quinn. 2005.
Relationships within Myrtaceae sensu lato based on a matK phy-
logeny. Plant Systematics and Evolution 251: 319.
Appendix 1. List of analyzed specimens. All vouchers deposited in
herbarium K. Species name and authorship according to the WCSP (2018).
Brazilian states are abbreviated as: AM 5Amazonas, BA 5Bahia, DF 5
Distrito Federal, ES 5Espirito Santo, GO 5Goi ´as, MG 5Minas Gerais,
PE 5Pernambuco, PR 5Paran´a, RJ 5Rio de Janeiro, RR 5Roraima, SP 5
S~
ao Paulo, TO 5Tocantins.
Blepharocalycinae: Blepharocalyx eggersii (Kiaersk.) Landrum, B W.
Nelson 923, Brazil (AM); Blepharocalyx eggersii (Kiaersk.) Landrum,
T.Vasconcelos 458, Brazil (BA); Blepharocalyx salicifolius (Kunth) O.Berg,
J.A. Ratter 5984, Brazil (MS); Blepharocalyx salicifolius (Kunth) O.Berg, J.E.Q
Faria 4050, Brazil (DF); Blepharocalyx salicifolius (Kunth) O.Berg, T.R.S. Silva
13494, Brazil (MG). Decasperminae: Archirhodomyrtus beckleri (F.Muell.)
A.J.Scott, B. Gray 1548, Australia (Queensland); Archirhodomyrtus turbinata
(Schltr.) Burret, J. Soewarto HB 11, New Caledonia; Archirhodomyrtus
turbinata (Schltr.) Burret, PS Green 1258, New Caledonia; Austromyrtus
dulcis (C.T.White) L.S.Sm., S. Belsham M77, Australia (Queensland);
Decaspermum parviflorum (Lam.) A.J.Scott, T. Vasconcelos 728, Malayisia
(Sabah); Decaspermum parviflorum (Lam.) A.J.Scott, T. Vasconcelos 730,
Malayisia (Sabah); Decaspermum vitis-idaea Stapf, T. Vasconcelos 729,
Malayisia (Sabah); Gossia bidwillii (Benth.) N.Snow & Guymer, L.S. Smith
4516a, Australia (Queensland); Kanakomyrtus longipetiolata N.Snow, H.S.
Mackee 32732, New Caledonia; Octamyrtus arfancensis Kaneh. & Hatus. ex
C.T.White, P. Van Royen 7925, New Guinea; Octamyrtus pleiopetala Diels,
D.R. Pleyte 209, New Guinea, ; Octamyrtus sp., Johns 9885, New Guinea;
Pilidiostigma tropicum L.S.Sm., PiF 27636, Australia (Queensland); Pili-
diostigma tropicum L.S.Sm., S.F. Kajewski 1265, Australia (Queensland);
Rhodamnia cinerea Jack, T.Vasconcelos 672, Singapore; Rhodamnia dumeto-
rum (DC.) Merr. & L.M.Perry, Schanzer I. et al. 148c, Australia; Rhodomyrtus
tomentosa (Aiton) Hassk., Amin and Francis SAN116159, NA (from the US
spirit collection); Rhodomyrtus tomentosa (Aiton) Hassk., Eyde 4/79, NA
(from the MO spirit collection); Rhodomyrtus tomentosa (Aiton) Hassk.,
T. Vasconcelos 678, Singapore; Rhodomyrtus tomentosa (Aiton) Hassk.,
T. Vasconcelos 726, Malayisia (Sabah); Uromyrtus archboldiana (Merr. &
L.M.Perry) A.J.Scott, P. Puradyatmika 7425, New Guinea; Uromyrtus
emarginata (Pancher ex Baker f.) Burret, T. Vasconcelos 605, New Caledonia;
Uromyrtus emarginata (Pancher ex Baker f.) Burret, T. Vasconcelos 628, New
Caledonia. Eugeniinae: Myrcianthes fragrans (Sw.) McVaugh, T.Vascon-
celos 535, Costa Rica; Myrcianthes fragrans (Sw.) McVaugh, R. Chacon350,
NA; Myrcianthes pungens (O.Berg) D.Legrand, J.E.Q. Faria 4277, Brazil (DF);
Calycorectes acutatus (Miq.) Toledo, T. Vasconcelos 506, Brazil (DF); Caly-
corectes bergii Sandwith, J.G. Myers 5955, French Guiana; Eugenia ligustrina
(Sw.) Willd., Hamilton M.A. 570, British Virgin Islands; Eugenia ligustrina
(Sw.) Willd., T.Vasconcelos 570, Dominican Republic; Eugenia uniflora L.,
T. Vasconcelos s.n., RBG Kew living collection (native to Brazil); Eugenia
splendens O.Berg, J.E.Q.Faria 4196, Brazil (BA); Hexachlamys edulis (O.Berg)
Kausel & D.Legrand, T.M. Pedersen 2756, Brazil (SP); Eugenia bullata
Pancher ex Guillaumin, T.Vasconcelos 608, New Caledonia; Eugenia
malangensis (O.Hoffm.) Nied., Brenan 7962, South Africa; Eugenia malan-
gensis (O.Hoffm.) Nied., Brenan 8024, South Africa; Eugenia malangensis
(O.Hoffm.) Nied., Greenway 8129, South Africa; Eugenia malangensis
(O.Hoffm.) Nied., Robson 342, South Africa; Eugenia paludosa Pancher ex
Brongn. & Gris, T.Vasconcelos 646, New Caledonia,; Eugenia roseopetiolata
N.Snow & Cable, T. Vasconcelos s.n., RBG Kew living collection (native to
Madagascar); Eugenia involucrata DC., J.E.Q. Faria 4047, Brazil (DF);
Eugenia involucrata DC., T.Vasconcelos 256, Brazil (DF); Eugenia involucrata
DC., T.Vasconcelos 734, Brazil (DF); Eugenia itajurensis Cambess., J.E.Q.
Faria 4250, Brazil (BA); Eugenia klotzschiana O.Berg, Heringer et al. 1975,
Brazil (GO); Eugenia pohliana DC., J.E.Q. Faria 4184, Brazil (BA); Eugenia
stipitata McVaugh, T.Vasconcelos 677, Singapore (cultivated, native to
Brazilian Amazon); Eugenia victoriana Cuatrec., T.Vasconcelos 717, Sin-
gapore (cultivated, native to Colombia); Eugenia azurensis O.Berg, J.E.Q.
Faria 4186, Brazil (BA); Eugenia azurensis O.Berg, T.Vasconcelos 433,
Brazil (BA); Eugenia pyriformis Cambess., L.M. Borges 1090, Brazil (RJ);
Eugenia pyriformis Cambess., Reitz & Klein 11341, Brazil (RJ); Eugenia
angustissima O.Berg, D.F. Lima 489, Brazil (GO); Eugenia biflora (L.) DC.,
T.Vasconcelos 589, Dominican Republic; Eugenia longiracemosa Kiaersk.,
T.Vasconcelos 310, Brazil (AM); Eugenia paracatuana O.Berg, P.O. Rosa
1399, Brazil (GO); Eugenia bunchosiifolia Nied., T. Vasconcelos 466, Brazil
(ES); Calyptrogenia cuspidata Alain, E. Lucas 1125, Dominican Republic;
Eugenia aff. schunkei McVaugh, A. Giaretta 1419, Brazil (AM); Eugenia
bahiensis DC., J.E.Q. Faria 4229, Brazil (BA); Eugenia coffeifolia DC. Vel.
Eugenia adenocalyx DC., A. Giaretta 1441, Brazil (RR); Eugenia pluriflora DC.,
Hatschbach 19022, Brazil (PR); Eugenia protenta McVaugh, T. Vasconcelos
350, Brazil (AM); Eugenia punicifolia (Kunth) DC., J.E.Q. Faria 4051, Brazil
(DF); Eugenia punicifolia (Kunth) DC., J.E.Q. Faria 4237, Brazil (ES); Eugenia
punicifolia (Kunth) DC., T. Vasconcelos 284, Brazil (GO); Eugenia punicifolia
(Kunth) DC., T. Vasconcelos 475, Brazil (MG); Eugenia stictosepala Kiaersk.,
J.E.Q. Faria 4269, Brazil (ES); Hottea ekmanii (Urb.) Borhidi, E. L. Ekman
2502c, Dominican Republic; Incertae sedis: Amomyrtus luma (Molina)
D. Legrand & Kausel, RBGE 1996- 1065, RBG Edimburg living collection
(native to Chile); Myrtastrum rufopunctatum (Pancher ex Brongn. & Gris)
Burret, M.W. Callmander 796, New Caledonia. Luminae: Blepharocalyx
SYSTEMATIC BOTANY [Volume 44590
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
cruckshanksii (Hook. & Arn.) Nied, M.F. Gardner 4193, Chile; Luma apiculata
(DC.) Burret, T. Vasconcelos s.n., RBG Kew living collection (native to
Chile); Myrceugenia alpigena (DC.) Landrum, J.E.Q. Faria 4264, Brazil (MG);
Myrceugenia alpigena (DC.) Landrum, T. Vasconcelos 489, Brazil (MG);
Myrceugenia bananalensis Gomes-Bezerra & Landrum, J.E.Q. Faria 4048,
Brazil (DF); Myrceugenia bananalensis Gomes-Bezerra & Landrum, J.E.Q.
Faria 4049, Brazil (DF); Myrceugenia planipes (Hook. & Arn.)
O.Berg, E. J. Lucas s.n., RBG Kew living collection (native to Chile).
Myrciinae: Myrcia guianensis (Aubl.) DC., D.F. Lima 463, Brazil (MG);
Myrcia laxiflora Cambess., E. Lucas 1221, Brazil (BA); Myrcia nivea Cam-
bess., D.F. Lima 492, Brazil (GO); Myrcia sp., D.F. Lima 483, Brazil
(MG); Calyptranthes multiflora Poepp. ex O.Berg, A. Giaretta 1429, Brazil
(AM); Calyptranthes multiflora Poepp. ex O.Berg, A. Giaretta 1431,
Brazil (AM); Calyptranthes multiflora Poepp. ex O.Berg, T. Vasconcelos 379,
Brazil (AM); Marlierea excoriata Mart., T. Vasconcelos 493, Brazil (MG);
Marlierea glabra Cambess., J.E.Q. Faria 4246, Brazil (ES); Marlierea neu-
wiedeana (O.Berg) Nied., T. Vasconcelos 467, Brazil (ES); Marlierea
umbraticola (Kunth) O.Berg, T. Vasconcelos 311, Brazil (AM); Myrcia
amazonica DC., T. Vasconcelos 591, Brazil (SP); Myrcia hirtiflora DC.,
T. Vasconcelos 440, Brazil (BA); Myrcia rubella Cambess., D.F. Lima 495,
Brazil (GO); Myrcia strigipes Mart., J.E.Q. Faria 6303, Brazil (RJ); Calyp-
tranthes aff. blanchetiana O.Berg, E. Lucas 1208, Brazil (BA); Calyptranthes
brasiliensis Spreng., J.E.Q. Faria 4244, Brazil (BA); Calyptranthes grammica
(Spreng.) D.Legrand, T.Vasconcelos 483, Brazil (MG); Calyptranthes lucida
Mart. ex DC., T.Vasconcelos 259, Brazil (DF); Calyptranthes pallens Griseb.,
T.Vasconcelos 534, Costa Rica; Calyptranthes thomasiana O.Berg, T.Vas-
concelos s.n., RBG Kew living collection (native to British Virgin Islands);
Mitranthes clarendonensis (Proctor) Proctor, T.Vasconcelos 510, Jamaica;
Mitranthes ottonis O.Berg, E. Otto 272, Jamaica; Myrcia multipunctata
Mazine, J.E.Q. Faria 4236, Brazil (ES); Myrcia multipunctata Mazine,
T.Vasconcelos 801, Brazil (MG); Myrcia fenzliana O.Berg, E. Nic-Lughada
H50637, Brazil (BA); Myrcia sp.1, T. Vasconcelos 500, Brazil (MG); Myrcia
spectabilis DC., E. Lucas 1210, Brazil (BA); Myrcia spectabilis DC., E. Lucas
1214, Brazil (BA); Myrcia aff. eriopus DC., E. Lucas 1205, Brazil (BA); Myrcia
cardiaca O.Berg, T.Vasconcelos 274, Brazil (GO); Myrcia linearifolia Cam-
bess., P.O. Rosa 1402, Brazil (GO); Myrcia paivae O.Berg, T.Vasconcelos 298,
Brazil (AM); Myrcia paivae O.Berg, T.Vasconcelos 516, Costa Rica; Myrcia
splendens (Sw.) DC., G.C. Herrera 9932, NA; Myrcia splendens (Sw.) DC.,
T.Vasconcelos 250, Brazil (DF); Myrcia splendens (Sw.) DC., T.Vasconcelos
587, Dominican Republic; Myrcia splendens (Sw.) DC., T.Vasconcelos 753,
Brazil (ES); Myrcia sylvatica (G.Mey.) DC., E. Lucas 1222, Brazil (BA); Myrcia
pubipetala Miq., E. Lucas 477, Brazil (SP); Myrcia amplexicaulis (Vell.)
Hook.f., E. Lucas 1207, Brazil (BA); Myrcia mucugensis Sobral, JEQ Faria
4197, Brazil (BA); Myrcia mucugensis Sobral, T. Vasconcelos 441, Brazil
(BA); Myrcia subcordata DC., JEQ Faria 4257, Brazil (ES); Myrcia trimera
Sobral, E. Lucas 1219, Brazil (BA); Myrcia truncada Sobral, E. Lucas 1216,
Brazil (BA); Myrcia laruotteana Cambess., J.E.Q. Faria 4046, Brazil (DF);
Myrcia tomentosa (Aubl.) DC., P.O. Rosa 1379, Brazil (DF); Myrcia tomentosa
(Aubl.) DC., T.Vasconcelos 262, Brazil (DF). Myrtinae: Accara elegans (DC.)
Landrum, T.Vasconcelos 485, Brazil (MG); Accara elegans (DC.) Landrum,
T.Vasconcelos 490, Brazil (MG); Calycolpus goetheanus (Mart. ex DC.)
O.Berg, T.Vasconcelos 332, Brazil (AM); Chamguava schippii (Standl.)
Landrum, D.Aguilar 9833, Costa Rica; Chamguava schippii (Standl.)
Landrum, P.H. Gentle 8354, Costa Rica; Myrtus communis L., E. Lucas 211,
RBG Kew living collection (native to Mediterranean region); Myrtus
communis L., T. Vasconcelos s.n., RBG Kew living collection (native to
Mediterranean region). Pliniinae: Algrizea macrochlamys (DC.) Proença &
NicLugh, E. Melo 4496, Brazil (BA); Algrizea minor Sobral, Faria & Proença,
J.E.Q. Faria 4157, Brazil (BA); Myrciaria aff. glazioviana (Kiaersk.)
G.M.Barroso ex Sobral, T.Vasconcelos 413, Brazil (BA); Myrciaria floribunda
(H.West ex Willd.) O.Berg, R.M. Harley 54895, Brazil (BA); Myrciaria flo-
ribunda (H.West ex Willd.) O.Berg,, T.Vasconcelos 380, Brazil (AM);
Myrciaria glanduliflora (Kiaersk.) Mattos & D.Legrand, T.Vasconcelos 479,
Brazil (BA); Neomitranthes cordifolia (D.Legrand) D.Legrand, M.C. Souza
550, Brazil (RJ); Neomitranthes obscura (DC.) N.Silveira, A.M. Carvalho 816,
Brazil (SP); Plinia cauliflora (Mart.) Kausel, T.Vasconcelos 388, Brazil (DF)
(cultivated); Plinia nana Sobral, A. Stadnik 348, Brazil (MG); Siphoneugena
delicata Sobral & Proença, T.Vasconcelos 760, Brazil (ES); Siphoneugena
densiflora O.Berg, G. Martinelii 11939, NA. Pimentinae: Feijoa sellowiana
(O.Berg) O.Berg, Spirit collection 14462, RBG Kew living collection (native
to southern Brazil); Feijoa sellowiana (O.Berg) O.Berg, T.Vasconcelos s.n.,
RBG Kew living collection (native to southern Brazil); Capomanesia ada-
mantium (Cambess.) O.Berg, T. Vasconcelos 273, Brazil (DF); Campomanesia
adamantium (Cambess.) O.Berg, T.Vasconcelos 293, Brazil (GO); Campo-
manesia adamantium (Cambess.) O.Berg, T.Vasconcelos 474, Brazil (GO);
Campomanesia guazumifolia (Cambess.) O.Berg, A Lobao 1372, Brazil
(SP); Campomanesia simulans M.L.Kawas., T.Vasconcelos 472, Brazil
(MG); Campomanesia velutina, T.Vasconcelos 507, Brazil (DF); Legrandia
concinna (Phil.) Kausel, Germain s.n., Chile; Mosiera longipes (O.Berg)
Small, M.A. Hamilton 630, Sadle 186 Turks and Caicos Islands; Myr-
rhinium atropurpureum Schott, C. Farney 2265, Brazil (RJ); Myrrhinium
atropurpureum Schott, G. Hatchbachi 61056, Brazil (RJ); Myrrhinium
atropurpureum Schott,M.Souzas.n.,Brazil(RJ);Pimenta berciliae T. Vasc.
&B.Peguero,T.Vasconcelos578, Dominican Republic; Pimenta dioica (L.)
Merr., T.Vasconcelos 534, Costa Rica; Pimenta pseudocaryophyllus
(Gomes) Landrum, A.P. Duarte 8722, Brazil (SP); Pimenta pseudocar-
yophyllus (Gomes) Landrum, E. Lucas 193, Brazil (SP); Pimenta pseudo-
caryophyllus (Gomes) Landrum, H.C. de Lima 3453, Brazil (SP); Pimenta
pseudocaryophyllus (Gomes) Landrum, H.S. Irwin 19844, Brazil (GO);
Pimenta pseudocaryophyllus (Gomes)Landrum,T.Vasconcelos403,Brazil
(MG); Pimenta racemosa (Mill.) J.W.Moore, F. Axelrod 7796, Dominican
Republic; Psidium acranthum Urb., T.Vasconcelos 579, Dominican Re-
public; Psidium brownianum Mart. ex DC., T.Vasconcelos 465, Brazil (BA);
Psidium firmum O.Berg, T.Vasconcelos 290, Brazil (GO); Psidium frie-
drichsthalianum (O.Berg) Nied., T.Vasconcelos 522, Costa Rica; Psidium
guajava L., T.Vasconcelos 389, Brazil (DF) (cultivated); Psidium guajava L.,
T.Vasconcelos 585, Dominican Republic (cultivated); Psidium guineense
Sw., B.S.Amorim 1913, Brazil (PE); Psidium guineense Sw., T.Vasconcelos
279, Brazil (GO); Psidium laruotteanum Cambess, J.E.Q. Faria 4276, Brazil
(GO); Psidium myrsinites DC., T.Vasconcelos 503, Brazil (GO); Psidium
myrtoides O.Berg, T.Vasconcelos 402, Brazil (SP); Psidium oligospermum
Mart.exDC.,F.Franca5431,Brazil(BA);Psidium oligospermum Mart. ex
DC., F.F.Mazine 1346, Brazil (ES); Psidium riparium Mart. ex DC., J.E.Q.
Faria 4107, Brazil (TO); Psidium rufum Mart. ex DC., J.E.Q. Faria 4271,
Brazil (MG); Ugniinae: Lenwebbia prominens N.Snow & Guymer, G.P. Guymer
AQ424641, Australia (Queensland); Lenwebbia prominens N.Snow & Guymer,
L. Bird AQ424632, Australia (Queensland); Lophomyrtus obcordata (Raoul)
Burret, Cult Lord Headfort (Kew id:16201), New Zealand; Lophomyrtus obcordata
(Raoul) Burret, Melville 5751, New Zealand; Lophomyrtus obcordata (Raoul)
Burret, Spirit collection 10291, New Zealand; Myrteola nummularia (Lam.)
O.Berg, G.T.Prance 28535, Falklands; Myrteola nummularia (Lam.) O.Berg, M.F.
Gardner 3579, Falklands; Neomyrtus pedunculata (Hook.f.) Allan, B.H.Macmillan
76/102, New Zealand; Neomyrtus pedunculata (Hook.f.) Allan, Colens 1714,
New Zealand; Ugni candolei (Barn´eoud) O.Berg, T.Vasconcelos s.n., RBG Kew
living collection (native to Chile); Ugni myricoides (Kunth) O.Berg, T.Vasconcelos
533, Costa Rica.
VASCONCELOS ET AL.: FLORAL DIVERSITY IN MYRTEAE 5912019]
Downloaded From: https://bioone.org/journals/Systematic-Botany on 12 Aug 2019
Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP)
... The newly resolved phylogenetic position of Neomyrtus will necessitate a reappraisal of taxon circumscriptions and will likely impact morphological character mapping and inference of pleisiomorphic and synapomorphic character states as previously understood (e.g. Lucas et al. 2007;Retamales 2017;Vasconcelos et al. 2019). Specific matters to reconsider include (1) identification of synapomorphies for Neomyrtus + Myrtastrum and the distinguishing characters and circumscription of each genus, and (2) synapomorphies for Lenwebbia + Lophomyrtus and their generic circumscriptions. ...
... The placement of Neomyrtus in Ugninae Vasconcelos et al. 2019) is not too surprising as Neomyrtus and Ugni share a number of characters, including 5 sepals, 5 petals, biseriate ovules on the placenta, straight stamens in bud, and larger glandulous anthers. These characters, and others, now need to be reconsidered in relation to the newly established relationship between Neomyrtus and Myrtastrum, especially if these genera are to be recognised as a new subtribe. ...
... For example, the misidentified Belsham M42 (OTA 57310) was used by Belsham and Orlovich (2002) to describe hypanthium and androecium development in N. pedunculata, but the specimen on which their study is based is now considered to be L. obcordata. Further, Burret (1941), Allan (1961), and Lucas et al. (2007) describe the Neomyrtus gynoecium as unilocular, but Vasconcelos et al. (2019) and our examination of herbarium specimens shows it is bilocular with a distinct septum (CHR 531002, MJA Simpson 8413; CHR 285438, BPJ Molloy s.n.; CHR 619881, AF Mark s.n.). It appears that when one or more ovules in one locule are fertilised they suppress the development of ovules in the other locule, giving the appearance of being unilocular; further examination of locule number and placentation is required. ...
Article
Neomyrtus is a New Zealand endemic monotypic genus that has been assigned to the Myrtaceae tribe Myrteae. Previous phylogenetic studies using the five genetic markers ITS, ETS, matK, psbA-trnH, and rpl16 have placed the single species Neomyrtus pedunculata in a clade with the New Zealand endemic Lophomyrtus (subtribe Ugninae), comprising the two species L. bullata and L. obcordata. Examination of the single herbarium voucher (OTA 57310) representing the plant material from which the DNA for the five phylogenetic markers was obtained revealed that it had been misidentified as Neomyrtus pedunculata and that it actually belongs to Lophomyrtus obcordata. We conducted a reanalysis of previously published data with new sequences from Neomyrtus and also undertook an analysis of 85 kbp of plastid protein coding genes from available Myrteae plastid genomes. These new phylogenetic analyses place Neomyrtus as sister to the New Caledonian endemic genus Myrtastrum, and the two species of Lophomyrtus form a clade that is sister to the Australian endemic Lenwebbia. Neomyrtus and Lophomyrtus are not closely related within the context of the tribe. This change to the understanding of Myrteae phylogeny is discussed in terms of available morphological character data and the biogeography of the tribe. Myrtastrum is currently treated as incertae sedis at subtribal rank, but along with Neomyrtus could be considered as representing a new subtribe as our analyses suggest they are not part of any of the clades hitherto recognised as subtribes.
... Morphological traits frequently studied by those interested in the systematics and evolution of Myrteae (McVaugh, 1958(McVaugh, , 1968Landrum, 1981a;Landrum & Kawasaki, 1997;Lucas et al., 2007Lucas et al., , 2018Lucas et al., , 2019Vasconcelos et al., 2019c) are briefly summarized. Most diagnostic characters involve reproductive organs operating under more acute selective pressure to maximize pollination and dispersal efficiency and effectiveness (Vasconcelos & Proença, 2015). ...
... Flowers of Myrteae are superficially similar, but possess characters used with varying degrees of accuracy for distinguishing taxa and subtle variations never fully explored in the context of systematics and macroevolutionary dynamics but discussed by Vasconcelos et al. ( , 2019c, and references therein). The number of perianth parts varies from four to five, occasionally six, with the number strongly conserved in some genera (e.g. ...
... These characters are strongly interdependent, and the evolution of the different arrangements was described by Vasconcelos et al. (2019c). Ovary characters are not strongly correlated with phylogeny of Myrteae, but are successfully used as part of suites of characters to define genera (e.g. ...
Article
Myrtaceae are one of the largest families of flowering plants and are widely distributed in the Neotropics, where they are mainly represented by the tribe Myrteae. Myrteae are the most species-rich tribe of Myrtaceae and include groups with significant ecological and economic importance. Myrteae are considered to be a model group for biodiversity studies in the Neotropics, and so understanding the history of their diversification in this area is extremely important. The last decade has witnessed an increase in macro- and microevolutionary studies of the group, and summarizing this knowledge is now crucial to plan future steps in research on Myrteae. Here we provide the first overview of evolution and diversification studies on Myrteae, highlighting recent advances in understanding their evolutionary history. We discuss biogeography, phylogeny, phylogeography, population genetics, genomics and cytology in light of current knowledge. Finally, we provide perspectives and open hypotheses to be tested in future studies to fill gaps in the evolutionary knowledge of specific groups/taxa in Myrteae.
... The newly resolved phylogenetic position of Neomyrtus will necessitate a reappraisal of taxon circumscriptions and will likely impact morphological character mapping and inference of pleisiomorphic and synapomorphic character states as previously understood (e.g. Lucas et al. 2007;Retamales 2017;Vasconcelos et al. 2019). Specific matters to reconsider include (1) identification of synapomorphies for Neomyrtus + Myrtastrum and the distinguishing characters and circumscription of each genus, and (2) synapomorphies for Lenwebbia + Lophomyrtus and their generic circumscriptions. ...
... The placement of Neomyrtus in Ugninae Vasconcelos et al. 2019) is not too surprising as Neomyrtus and Ugni share a number of characters, including 5 sepals, 5 petals, biseriate ovules on the placenta, straight stamens in bud, and larger glandulous anthers. These characters, and others, now need to be reconsidered in relation to the newly established relationship between Neomyrtus and Myrtastrum, especially if these genera are to be recognised as a new subtribe. ...
... For example, the misidentified Belsham M42 (OTA 57310) was used by Belsham and Orlovich (2002) to describe hypanthium and androecium development in N. pedunculata, but the specimen on which their study is based is now considered to be L. obcordata. Further, Burret (1941), Allan (1961), and Lucas et al. (2007) describe the Neomyrtus gynoecium as unilocular, but Vasconcelos et al. (2019) and our examination of herbarium specimens shows it is bilocular with a distinct septum (CHR 531002, MJA Simpson 8413; CHR 285438, BPJ Molloy s.n.; CHR 619881, AF Mark s.n.). It appears that when one or more ovules in one locule are fertilised they suppress the development of ovules in the other locule, giving the appearance of being unilocular; further examination of locule number and placentation is required. ...
... 3 to 180). Anthers vary by an order of magnitude in size, from 0.3 to 3 mm, and usually have an apical gland and a few smaller glands scattered along the connective, although some species have no glands and species with long anthers may have many scattered glands (Landrum, 2017;Vasconcelos et al., 2019). ...
Article
Background and Aims Psidium is the 4th largest genus of Myrtaceae in the Neotropics. Psidium guajava is widely cultivated in the tropics for its edible fruit. It is commercially under threat due to the disease guava decline. P. cattleyanum is one of the 100 most invasive organisms in the world. Knowledge of the phylogenetic relationships within Psidium is poor. We aim to provide a review of the biology, morphology and ecology of Psidium, a phylogenetic tree, an infra-generic classification and a list of species. Methods Morphological and geographic data were obtained by studying Psidium in herbaria and in the field between 1988 and 2020. Forty-six herbaria were visited personally. A database of c. 6,000 specimens was constructed, and the literature was reviewed. Thirty species (c. 1/3 of the species in the genus) were sampled for molecular phylogenetic inference. Two chloroplast (psbA-trnH and ndhF) and two nuclear (ETS and ITS) regions were targeted. Phylogenetic trees were constructed using Maximum Likelihood (ML; RaxML) and Bayesian Inference (BI; MrBayes). Key Results Psidium is a monophyletic genus with four major clades recognized as sections. Section Psidium (ten species), to which P. guajava belongs, is sister to the rest of the genus; it is widespread across the Neotropics. Section Obversifolia (six species; restricted to the Brazilian Atlantic Forest), which includes P. cattleyanum, is sister to the innermost clade composed of sister sections Apertiflora (31 species; widespread but most diverse in the Brazilian Atlantic Forest) + Mitranthes (26 species; widespread in dry forests and probably diverse in the Caribbean). Characters associated to diversification within Psidium are discussed. Conclusions Research on prefoliation, colleters, leaf anatomy, leaf physiology, staminal development, placentation, and germination associated to the anatomy of the opercular plug is desirable. Studies are biased towards sections Psidium and Obversifolia, with other sections poorly known.
... The most species-rich tribe of Myrtaceae is Myrteae that comprises about 51 genera and 2500 species, representing nearly half of the family diversity (Govaerts et al., 2021). Tribe Myrteae has a pantropical distribution, with greater diversity in neotropical regions (Wilson, 2011;Vasconcelos et al., 2017Vasconcelos et al., , 2019Govaerts et al., 2021). Lucas et al. (2005Lucas et al. ( , 2007 proposed seven informal groups that were further categorized into nine subtribes by Lucas et al. (2019) Eugenia L. is the largest genus of neotropical Myrtaceae and comprises 1100 species (Govaerts et al., 2021). ...
Article
The genus Eugenia is of great ecological importance and due to being very diverse has been the subject of a comprehensive phylogenetic and taxonomic review to create an accurate classification. This study sought to describe the pericarp ontogeny of species in the subtribe Eugeniinae to reveal anatomical features that can be used to characterize morphologically similar sections. Buds, flowers, and fruits were collected at different development stages from herbarium specimens and plants in the field. Herbarium material underwent a reversal procedure, and fresh material was submitted to conventional anatomical analysis techniques and evaluated under an optical light microscope. By analyzing the species, we verified some promising characteristics, such as the following: a drupe-like fruit in Myrcianthes pungens (which is in the genus sister to Eugenia) that is a novelty for this species; trichomes in the inner epidermis of the ovary in species in Eugenia sect. Hexachlamys and E. sect. Pilothecium; and the absence of intercellular spaces in the most internal layers of the mesocarp in a species of E. section Speciosae. Representatives from the subtribe showed predominant cell division in the layers subjacent to the exocarp (dorsal meristem) and endocarp (ventral meristem) and the outer, middle and inner mesocarp.
... Myrcia sect. Myrcia species are mostly pollinated by bees and dispersed by mammals and birds (Vasconcelos et al. 2019b). The most recent diagnosis of Myrcia sect. ...
... Eugenia section Speciosae Bünger & Mazine also has an unstable relationship, of note as species of these sections were previously included in genus Phyllocalyx O.Berg. The apparent polyphyly of Pimenta reflects historical uncertainty in Myrtinae and Pimentinae Vasconcelos et al., 2019) with small but significant differences apparent in nuclear only analyses (e.g., Salywon, 2003), vs. those including plastid markers (e.g., Vasconcelos et al., 2017), which recovered a monophyletic Pimenta, including Pimenta pseudocaryophyllus within Pimentinae. It is of note that several taxa formerly assigned to subtribe Myrtinae sensu Berg (1859), with subtropical or temperate distributions, have unstable relationships. ...
Article
Full-text available
Premise To further advance the understanding of the species-rich, economically and ecologically important angiosperm order Myrtales in the rosid clade, comprising nine families, approximately 400 genera and almost 14,000 species occurring on all continents (except Antarctica), we tested the Angiosperms353 probe kit. Methods We combined high-throughput sequencing and target enrichment with the Angiosperms353 probe kit to evaluate a sample of 485 species across 305 genera (76% of all genera in the order). Results Results provide the most comprehensive phylogenetic hypothesis for the order to date. Relationships at all ranks, such as the relationship of the early-diverging families, often reflect previous studies, but gene conflict is evident, and relationships previously found to be uncertain often remain so. Technical considerations for processing HTS data are also discussed. Conclusions High-throughput sequencing and the Angiosperms353 probe kit are powerful tools for phylogenomic analysis, but better understanding of the genetic data available is required to identify genes and gene trees that account for likely incomplete lineage sorting and/or hybridization events.
Article
We present a taxonomic study of the Myrtaceae family in a fragmented landscape known as Amazonian Maranhão. The botanical collections were made from August 2019 to February 2020. Other collections were studied in loco at HST, IAN, IPA, MAR, MG, NY, PEUFR, and SLUI, and others online at virtual herbaria. Myrtaceae are represented in Amazonian Maranhão by 37 species. The most diverse genera are Myrcia with 16 species and Eugenia with 15 species, followed by Myrciaria and Psidium with two species each, and Campomanesia and Calycolpus with one each. Some of the species are cited here from Maranhão for the first time, and have their geographic distribution extended, including Eugenia dittocrepis, E. lambertiana, E. patens, E. patrisii, Myrcia bracteata, M. eximia, and Psidium acutangulum. A taxonomic treatment for the family in the region, with an identification key to the species, detailed descriptions and taxonomic comments for each species is presented.
Chapter
The floral diversity of Melastomataceae is stunning and clearly expressed in sepal and stamen structure and in the position of the ovary. Comparative developmental studies are effective in order to understand these variations because they reveal the often-enigmatic origin of the structures. The diverse calyx structure originates from variations in the degree of union between the sepals. The contort corolla aestivation, widespread in the family, is influenced by the floral architecture. Stamen size and shape depend on the space available in the floral bud after the growth of the perigynous hypanthium that may cause the delay in stamen emergence and flexion. Dimorphic stamens originate from differences in their developmental time and position. Prolonged connectives and most of their appendages are formed late during floral development. Ontogeny also explains the decrease or increase in organ number. The intercalary meristems can promote the formation of a hypanthium associated with the gynoecium, and their extension is responsible for the gradual variation in ovary position. These meristems also act on the development of a perigynous hypanthium. Thus, intercalary meristems play an important role for floral diversification in Melastomataceae. The potential of comparative floral development is wide and is illustrated here through several examples in this family.
Article
Campomanesia (Myrtaceae) comprises approximately 45 species restricted to South America, 35 of which are found in Brazil. In this study, we ontogenetically analyzed species in the genus with the objectives of understanding and comparing the ovary and pericarp parts, highlighting characters that distinguish the species and providing information that could help to elucidate phylogenetic relationships in the future. We examined flower buds, flowers and fruits from herbarium specimens of 12 species. Results corroborate features that can be used as synapomorphies for the genus, such as the high number of locules, the development of one ovule per locule or the total sterilization of locules, and glandular locule wall. Campomanesia aurea, C. cavalcantina and C. xanthocarpa fruits have one or two layers of secretory cavities around the locules, whereas the remaining species have one layer. Sclereids were found in the ovarian mesophyll of C. guazumifolia, C. rufa and C. sessiliflora, while in the other species these only became evident when the pericarp was fully formed. The presence of trichomes and crystals was not consistent across species. Some anatomical characteristics, such as the disposition of secretory cavities in the outer and inner regions of the mesophyll and mesocarp, the presence or absence of sclereids, and the presence of trichomes and crystals at determined development phases, are promising to distinguish species in the genus. These features were compared with species in other closely related genera of Myrtaceae.
Article
Full-text available
Myrtaceae is commonly known to have an inferior ovary of appendicular, receptacular or mixed origin. Other characters of the ovary, such as the number of carpels, number of locules, vascularisation pattern, number of ovules, placentation and presence of compitum have also been of interest to researchers aiming to better understand the evolutionary history of the tribe. In the present study, aspects of the structure of the inferior ovary of 21 species of Myrteae are analysed and reviewed as potential characters for better understanding the evolutionary history of Myrteae. Flower buds were embedded in historesin and paraplast and sectioned transversely and longitudinally with a rotary microtome. Results suggested that most species have an inferior ovary of appendicular origin and that a compitum, or compitum tissue, is present in all species analysed, differing only in the degree of development. Number of carpels and locules vary, with most species having two locules. Vascular supply is transeptal and axial, the latter being the most common condition in the investigated species. Data presented here enhance current evolutionary understanding of the tribe and its history. Results indicated that the inferior ovary of ancestral Myrteae may has had an appendicular origin, that the presence and nature of the compitum may have a positive effect on fertilisation efficiency and a relationship with number of ovules and that transepetal vascular supply may be taxonomically useful to define large groups such as Pimenta and Eugenia.
Article
Full-text available
A new classification of the large Neotropical genus Myrcia s.l. is proposed. Nine sections are presented that correspond to recently published clades. Of these nine sections, sects. Myrcia, Aulomyrcia and Sympodiomyrcia are already published, sects. Reticulosae and Tomentosae are new sections, sect. Eugeniopsis is a new combination whilst sects. Aguava, Calyptranthes and Gomidesia are new combinations at a new rank (comb. & stat. nov.). Six lectotypifications are made for sections or genera. Estimates of species per section are listed.
Article
Full-text available
Background and aims: Comparative floral ontogeny represents a valuable tool to understand angiosperm evolution. Such an approach may elucidate subtle changes in development that discretely modify floral architecture and underlie reproductive lability in groups with superficial homogeneous morphology. This study presents a comparative survey of floral development in Eugenia (Myrtaceae), one of the largest genera of angiosperms, and shows how previously undocumented ontogenetic trends help to explain the evolution of its megadiversity in contrast to its apparent flower uniformity. Methods: Using scanning electron microscopy, selected steps of the floral ontogeny of a model species (Eugenia punicifolia) are described and compared with 20 further species representing all ten major clades in the Eugenia phylogenetic tree. Additional floral trait data are contrasted for correlation analysis and character reconstructions performed against the Myrtaceae phylogenetic tree. Key results: Eugenia flowers show similar organ arrangement patterns: radially symmetrical, (most commonly) tetramerous flowers with variable numbers of stamens and ovules. Despite a similar general organization, heterochrony is evident from size differences between tissues and structures at similar developmental stages. These differences underlie variable levels of investment in protection, subtle modifications to symmetry, herkogamic effects and independent androecium and gynoecium variation, producing a wide spectrum of floral display and contributing to fluctuations in fitness. During Eugenia's bud development, the hypanthium (as defined here) is completely covered by stamen primordia, unusual in other Myrtaceae. This is the likely plesiomorphic state for Myrteae and may have represented a key evolutionary novelty in the tribe. Conclusions: Floral evolution in Eugenia depends on heterochronic patterns rather than changes in complexity to promote flexibility in floral strategies. The successful early establishment of Myrteae, previously mainly linked to the key innovation of fleshy fruit, may also have benefitted from changes in flower structure.
Article
Full-text available
Significance Large floristic datasets that purportedly represent the diversity and composition of the Amazon tree flora are being widely used to draw conclusions about the patterns and evolution of Amazon plant diversity, but these datasets are fundamentally flawed in both their methodology and the resulting content. We have assembled a comprehensive dataset of Amazonian seed plant species from published sources that includes falsifiable data based on voucher specimens identified by taxonomic specialists. This growing list should serve as a basis for addressing the long-standing debate on the number of plant species in the Amazon, as well as for downstream ecological and evolutionary analyses aimed at understanding the origin and function of the exceptional biodiversity of the vast Amazonian forests.
Article
A new classification of the predominantly Neotropical tribe Myrteae is proposed to replace Berg’s three traditional subtribes, the Myrciinae, Eugeniinae, and Myrtinae. Nine subtribes are here proposed that are supported by molecular and morphological data. In addition to the three traditionally recognized but modified here, subtribe Pimentinae (originally described as Pimentoideae) is reinstated and five new subtribes are proposed: Blepharocalycinae, Decasperminae, Luminae, Pliniinae, and Ugninae. A key to the nine subtribes is followed by descriptions of each, listing genera included, approximate species numbers, general distribution patterns, and notes. The genera Feijoa O. Berg and Temu O. Berg are reinstated. Morphological structures of importance for classification of Myrteae subtribes are illustrated.
Thesis
Blepharocalyx salicifolius (Kunth) O. Berg presents a wide latitudinal distribution in South America, mainly in Brazilian territory and occurs in both Cerrado and Atlantic Forest. The objective of this thesis was to study this species by collecting data on variations in leaf morphology in different biomes, genetic variation of different populations on a regional scale using four genetic markers (psbA-trnH, matK, ETS and ITS) and local aspects of population structure and population dynamics of the species in areas of cerrado in the restricted sense (preserved from fire and disturbed by frequent fire) in areas of preservation of Neotropical Savannah. The species presented high leaf plasticity evidenced by mor