Content uploaded by Thiago Fernandes
Author content
All content in this area was uploaded by Thiago Fernandes on Mar 21, 2024
Content may be subject to copyright.
Vol.:(0123456789)
KEW BULLETIN
DOI 10.1007/S12225-023-10159-Z
© The Board of Trustees of the Royal Botanic Gardens, Kew, 2024
Eugenia guapiassuana (Myrtaceae), a remarkable new tree
species from the Brazilian Atlantic Forest
Thiago Fernandes1 , Pablo Viany Prieto2, Marco Túlio Côrtes de Lacerda3, Mariana Bünger4 &
João Marcelo Alvarenga Braga1
Summary. This study proposes a new species of Eugenia sect. Phyllocalyx from Atlantic Forest remnants in the
Brazilian state of Rio de Janeiro. The new taxon, Eugenia guapiassuana, is proposed based on literature survey,
examination of herbarium material and eld work. We herein provide a morphological description, including
comments on fruit taste, along with information on distribution, habitat, phenology, vernacular name, taxonomy
and conservation status. Figures showing fresh and dry material and a map of the occurrence records are also
presented. Eugenia guapiassuana is morphologically similar to E. involucrata and E. superba, and these species are
contrasted in the discussion. Following an assessment, the conservation status of Eugenia guapiassuana is provision-
ally determined as Critically Endangered [CR B2ab(iii)].
Key Words. Cereja-de-guapiaçu, Eugenia sect. Phyllocalyx, fruit tree, Reserva Ecológica de Guapiaçu, threatened
species
Introduction
Currently comprising 414 species, Eugenia P.Micheli ex
L. (Linnaeus 1753: 470) is the most species-rich Myrta-
ceae genus occurring in Brazil (Mazine et al. 2020),
and in the Brazilian Atlantic Forest, Eugenia is remarka-
ble for its species richness, often topping lists of species
in oristic surveys (e.g., Oliveira-Filho & Fontes 2000;
Barros 2008; Urbanetz et al. 2010; Giaretta et al. 2013).
Eugenia species produce eshy fruits that contribute
signicantly as food sources for frugivores in the Atlan-
tic Forest (Pizo 2000; Nic Lughadha & Proença 1996;
Gressler et al. 2006; Staggemeier et al. 2017).
Eugenia sect. Phyllocalyx Nied. (Niedenzu 1893: 82)
is one of 11 currently accepted sections within Eugenia
and is placed in subg. Eugenia (Mazine et al. 2018). It
comprises 17 species, occurring mainly in the Brazil-
ian Atlantic Forest, and can be recognised by auxotelic
inorescences combined with relatively large owers
with foliaceous bracteoles and sepals (Bünger et al.
2020). The morphology of Eugenia sect. Phyllocalyx is
also partly shared with its sister group, Eugenia sect.
Speciosae Bünger & Mazine (in Bünger et al. 2016: 75),
but bracteoles in Speciosae are liform and deciduous
(see Bünger et al. 2016, 2020).
In 2022, a tall, remarkable tree with a distinctively
smooth trunk, whitish-pink owers and red fruits was
found by Mr Messias Gomes da Silva, a local resident
and forest ranger of Reserva Ecológica de Guapiaçu
(REGUA). His discovery was the foundation of this
study, as it made us aware of this tree and prompted
us to collect samples for herbaria. REGUA is a private,
protected area, totalling 8000 hectares of Atlantic For-
est, in southeastern Brazil (see https:// www. regua. org.
br/).
Herein we propose the aforementioned species as
a new taxon of Eugenia sect. Phyllocalyx. We provide
a morphological description, including comments on
the taste of its fruit, and information about its distribu-
tion, habitat, phenology and conservation status. We
include a vernacular name and some additional taxo-
nomic notes. Figures showing fresh and dry material
and a map with occurrence records of the new taxa
are presented.
Material and Methods
A literature survey and examination of virtual and
physical herbarium specimens conrmed the recog-
nition of the taxon as a new species. The following her-
baria were visited: BHCB, BM, BR, C, CEPEC, ESA, G,
HB, HPL, HRCB, HUENF, HUFU, HUFSJ, K, LE, M,
MBM, MBML, NIT, OUPR, OXF, P, R, RB, RBR, RFA,
RFFP, S, SP, SPF, UEC, UPCB, and W (acronyms follow
Thiers 2023, continuously updated; HUENF follows
Nascimento et al. 2023). In addition, high-resolution
images of specimens of Atlantic Forest Eugenia were
ISSN 1874-933X (print)
ISSN 0075-5974 (electronic)
Accepted for publication 17 November 2023.
1 Instituto de Pesquisas, Jardim do Botânico do Rio de Janeiro, Rua Pacheco Leão, 915, Rio de Janeiro 22460-030, Brazil. e-mail: thiagofernandes@id.uff.br
2 Universidade do Estado do Rio de Janeiro, Programa de Pós-graduação em Ecologia e Evolução, Rua São Francisco Xavier, 524, Rio de Janeiro, RJ 20550–
013, Brazil
3 Coleção Botânica Sítio E-jardim, Estr. do Aviário s.n., Xerém, Duque de Caxias, RJ 25250–597, Brazil
4 Departamento de Biologia, Universidade Federal do Ceará, Campus do Pici Prof. Prisco Bezerra, bl. 906, 60440-900, Fortaleza, CE, Brazil
KEW BULLETIN
© The Board of Trustees of the Royal Botanic Gardens, Kew, 2024
examined through REFLORA (2022), CRIA (2022),
and JSTOR Global Plants (2022). We examined all
the types of names assigned to Eugenia sect. Phylloca-
lyx and E. sect. Speciosae, and recent taxonomic studies
on these sections (Bünger et al. 2016, 2020) were con-
sulted throughout.
All measurements presented in the description
were taken from dried material. Colours were obtained
from freshly collected material. Terminology on indu-
mentum is according to Hewson (1988); leaf features
according to Hickey (1973); general shapes accord-
ing to Radford et al. (1974); and general morphology
according to Beentje (2010). The terms “auxotelic”
and “anauxotelic” are applied in the sense of Briggs
& Johnson (1979).
The Area of Occupancy (AOO) was calculated using
GeoCAT (Bachman et al. 2011), and the map of occur-
rence records was built using QGis Desktop version
2.16.3 (QGIS Development Team 2022). Conservation
assessments follow the IUCN Red List categories, crite-
ria and guidelines (IUCN 2012, 2022).
Taxonomic Treatment
Eugenia guapiassuana T.Fern., M.T.C.Lacerda &
J.M.A.Braga sp. nov. Type: Brazil, Rio de Janeiro, Cach-
oeiras de Macacu, 1 Sept. 2022, ., T. Fernandes, M. G.
da Silva & P. V. Prieto 1218 (holotype RB; isotypes NIT,
K, R). Figs 1, 2 and 3.
http:// www. ipni. org// urn: lsid: ipni. org: names: 77331 883-1
Deciduous tree up to 20 m tall. Trunk smooth, light
brown when owering and fruiting; bark thick, some-
times detaching in irregular plates. Leafy shoots adaxi-
ally sericeous and glabrescent, trichomes golden, 0.5
– 0.8 mm long; in fresh state adaxially cinereous, abaxi-
ally vinaceous. Young twigs attened, trichomes similar
to those on leafy shoots, glabrescent; epidermal surface
beneath trichomes densely glandular. Mature branches
straight, terete, brownish, smooth, not exfoliating.
Leaves: petioles 10 – 17 × 1.8 – 3.5 mm, adaxially sul-
cate, trichomes similar to those on leafy shoots, glabres-
cent; blades 80 – 120 × 40 – 70 mm, usually obovate,
base cuneate, apex usually mucronate or sometimes
rounded or rarely slightly emarginate, coriaceous,
essentially concolorous, drying brown, mostly glabrous
or sometimes puberulent on both surfaces, with tri-
chomes visibly concentrated at the midvein; midvein
canaliculate adaxially and strongly raised abaxially,
venation slightly raised and barely conspicuous, sec-
ondary veins 12 – 15 on each side, leaving the midvein
at angles of 50 – 60º; marginal veins two, the inner one
2 – 3 mm from the margin, conspicuous, the outer
one 0.5 – 1 mm from the margin, barely conspicuous;
glands up to 0.2 mm in diam., conspicuous on both
surfaces, adaxially black and foveolate, abaxially dark-
brown and raised. Inorescences in auxotelic racemes,
1 – 3 pairs of decussate owers, ower internodes c. 1
mm long; Bracts at the inorescence base 3.5 – 4.5 × 1
– 2 mm, linear, base truncate, apex obtuse, tomentose,
with rusty or brownish simple trichomes c. 0.5 mm,
falling at anthesis or occasionally persisting, although
marcescent in fruiting material; bracts at the axis
nodes not seen, probably deciduous before anthesis.
Pedicels 15 – 30 mm long, attened; when owering 1
– 1.8 mm wide, densely sericeous, trichomes similar to
those on young twigs; when fruiting 2.5 – 3 mm wide,
puberulent to glabrous; verrucose and swollen at base
and apex in fresh state. Bracteoles 8.5 – 10 × 7.2 – 9.8
mm, cordiform; apex obtuse or with an obtuse acu-
men; free from each other, partially or completely con-
cealing the ovary, foliaceous; persistent after anthesis,
deciduous in fruit; vinaceous; densely punctate, puber-
ulent to glabrous, except for the densely sericeous
midvein, ciliate; trichomes similar to those on young
twigs. Flowers: buds 12 – 14 × 12 – 14 mm, globose; com-
pletely concealed by bracteoles when immature; when
mature bracteoles only concealing the ovary. Floral
disk subquadrate, 6 – 8 mm between the edges. Sepals
8.5 – 11.3 × 6 – 7.5 mm, widely-deltoid; apex obtuse or
with a short, obtuse acumen; externally mostly puberu-
lent, except moderately sericeous at base, internally
moderately to densely sericeous; margins with golden
cilia up to 0.2 mm long; opening perpendicularly to
the ovary axis at anthesis; pinkish to vinaceous when
fresh. Petals 20 – 22.5 × 12 – 19 mm, obovate, base
truncate, apex obtuse or rounded, puberulent or gla-
brous, except for golden cilia up to 0.2 mm long at
margins, concave, whitish-pink when fresh. Staminal
ring 2.5 – 3 mm thick, rounded, densely covered with
erect, golden trichomes c. 0.5 mm long; stamens 205
– 235 (counted in bud), laments 5 – 10 mm long;
anthers c. 1 × 1 mm, bilocular, with a visible septum.
Ovary c. 0.3 × 0.2 mm; externally densely sericeous, tri-
chomes golden, c. 0.5 mm long, markedly distinct from
the calyx; internally with two, glabrous locules, each
with 42 – 46 ovules. Fruits 28 – 46 × 14 – 20 mm, ellip-
soid, green when immature, passing through yellow
then red to vinaceous when mature; pulp orange, juicy
and abundant, rmly adhering to the seed; surface lus-
trous, puberulent but with trichomes concentrated at
the transition with the calyx; calyx in fruit persistent,
accrescent, usually erect, red to vinaceous. Seeds one
per fruit, c. 25 × 15 mm, ellipsoid; cotyledons fused,
hypocotyl lighter and conspicuous.
RECOGNITION. Morphologically closely related to
Eugenia involucrata DC. (de Candolle 1828: 264), E.
guapiassuana diers in having petioles 10 – 17 mm
long (vs 3 – 7 mm long); bracteoles and sepals cili-
ate (vs glabrous); bracteoles deciduous in fruit (vs
KEW BULLETIN
© The Board of Trustees of the Royal Botanic Gardens, Kew, 2024
Fig. 1. Morphology of Eugenia guapiassuana from dried specimens. A & inset, leaf adaxial surface; B & inset, leaf abaxial sur-
face; C & inset, inorescence with ower buds, mostly concealed by the bracteoles, developing along with leaf shoots; D ower
bud, frontal bracteole detached; E open ower, from above; F open ower, from below; G ovary with two locules; H fruit; J
embryo; A – G from Fernandes 1218; H – J from Fernandes 1268.
KEW BULLETIN
© The Board of Trustees of the Royal Botanic Gardens, Kew, 2024
persistent); pedicels verrucose in fruit (vs smooth); ova-
ries with golden indumentum (vs rusty); mature fruits
with persistent indumentum, at least on the transition
with the calyx (vs glabrous); and in pulp rmly adher-
ing to the seeds when fresh (vs pulp almost entirely
free from the seeds, so that the fruit display a hollow
cavity between the endocarp and the seed coat). Also
remarkable are the whitish-pink owers of Eugenia gua-
piassuana, which contrasts with all other species of E.
sect. Phyllocalyx, which have owers with green sepals
and white petals and stamens. Other dierences are
described in Table 1.
Eugenia guapiassuana is also similar to E. superba
T.Fern., M.C.Souza & J.M.A.Braga (Fernandes et al.
2023: 100), another tall, deciduous tree with smooth
trunk bark from the Atlantic Forest, which is also
assigned to E. sect. Phyllocalyx. It diers, however, as
the trunk detaches as thick plates (vs exfoliates as
papyraceous plates in E. superba), mature branches are
brownish and not exfoliating (vs reddish and exfoliat-
ing), leaf blades are essentially concolorous when dry
(vs markedly discolorous), the indumentum on owers
is golden (vs whitish), the fruits are markedly ellipsoid
and red when ripe (vs suglobose to slightly ellipsoid
and yellow to orange); and the bracteoles are usually
deciduous (vs persistent and accrescent).
DISTRIBUTION. Restricted to the municipality of Cach-
oeiras de Macacu, in Rio de Janeiro State, southeast-
ern Brazil (Map 1). There it occurs in Atlantic rainfor-
ests at the base and on the slopes of the Serra do Mar
mountain range, up to 500 m, close to watercourses.
SPECIMENS EXAMINED. BRAZIL. Rio de Janeiro: Cach-
oeiras de Macacu, Fragmento de floresta aluvial
próximo à Reserva Ecológica de Guapiaçu (REGUA),
22º27'1.7"S, 42º48'42.2"W, 80 m a.s.l., 16 Oct. 2022, fr.,
T. Fernandes, M. G. da Silva & P. V. Prieto 1268 (BHCB,
K, MBML, NIT, NY, RB, R, RBR, RFFP, SPF).
HABITAT AND ECOLOGY. We collected samples of Eugenia
guapiassuana from two adult trees only, found at a sin-
gle locality in the Guapiaçu river watershed. The site
is within an 194 ha fragment of early to mid-secondary
forest, on an alluvial plain, adjacent to a small creek.
It is supposed that Eugenia guapiassuana is a late-suc-
cessional species, so these two trees are probably remi-
niscent of old-growth forests that covered the area in
the past. Another two trees could be reliably identi-
ed from photographs as the same species, so were
included on the distribution map. They are together,
Fig. 2. Eugenia guapiassuana in its natural habitat at the type locality. A two individuals; B detail of trunk bark. photos: thiago
fernandes.
KEW BULLETIN
© The Board of Trustees of the Royal Botanic Gardens, Kew, 2024
Fig. 3. Morphology of Eugenia guapiassuana. A leaf adaxial surfaces with puberulent indument; B leaf abaxial surface; C leafy
shoots, adaxially cinereous, sericeous, abaxially glabrous and vinaceous; D inorescences developing along with leafy shoots; E
ower bud at early stages of development; F pre-anthetic ower; G owers at anthesis; H ower from below, showing the cor-
diform bracteoles; J post-anthetic ower, after stamens fall; K detail of the thick, verrucose pedicel in fruit, swollen at base and
apex; L mature fruit with persistent trichomes concentrated on the transition with the calyx (arrowed); M mature fruits. A – J
from Fernandes 1218; K – M from Fernandes 1268. photos: thiago fernandes.
KEW BULLETIN
© The Board of Trustees of the Royal Botanic Gardens, Kew, 2024
at a hard to access site, ve kilometres away from the
type locality, in the same watershed, in old-growth for-
est, growing on a rocky slope.
Wood density is highly conserved at the genus level
among neotropical trees (Chave et al. 2006), so Eugenia
guapiassuana is likely to have dense wood, comparable
to that of the closely related E. involucrata (0.9 g/cm3;
Carvalho 2008). The species also has a large maximum
size and large seed, which, along with dense wood, are
typically associated with slow-growing, shade-tolerant,
late-successional tree species (Lohbeck et al. 2015;
Rüger et al. 2018).
CONSERVATION STATUS. Eugenia guapiassuana is only
known from four mature individuals that occur in a
very small area. The AOO is 8 km2 and the species is
restricted to two sites about 5 km apart, but likely to
be prone to a single threat event, as described below,
so considered a single locality sensu IUCN (2022). The
type locality is within a forest fragment, surrounded
by pastures and agricultural elds, which may lead
Table 1. Morphological comparison between Eugenia guapiassuana and its relatives, E. involucrata and E. superba.
E. guapiassuana E. involucrata E. superba
Seasonality deciduous mostly evergreen deciduous
Petioles length (mm) 10 – 17 3 – 7 7.7 – 18.5
Bracteoles vinaceous, ciliate, deciduous in fruit green, not ciliate, accrescent in fruit green, ciliate, accrescent in fruit
Pedicel in fruit verrucose, swollen at base and apex smooth, not swollen smooth, not swollen
Sepals in fresh state pinkish or vinaceous green, sometimes with red spots green
Petals in fresh state whitish-pink white, sometimes with green spots white
Ovary indumentum golden rusty cream to golden
Fruits ellipsoid, red when mature, pulp
rmly adhering to the seed
ellipsoid, red when mature, pulp
almost entirely free from the seed subglobose, orange, pulp
rmly adhering to the seed
Map 1. Geographic distribution of Eugenia guapiassuana.
KEW BULLETIN
© The Board of Trustees of the Royal Botanic Gardens, Kew, 2024
to a loss of habitat quality due to edge eects. Urban
expansion is taking place rapidly in the adjacent land-
scape and also constitutes a direct threat. Therefore,
Eugenia guapiassuana is provisionally assessed as Criti-
cally Endangered [CR B2ab(iii)]. Legal protection for
the type locality is urgently required, as is propaga-
tion of the species for both ex-situ conservation and
enrichment of restoration plantations. Cultivation of
E. guapiassuana as an ornamental and fruit tree is also
highly recommended, as this may help to reduce its
chances of extinction.
PHENOLOGY. Flowers in August – September and fruits
in October.
ETYMOLOGY. The epithet is a tribute to Reserva
Ecológica de Guapiaçu (REGUA), an outstandingly
important area for the conservation of Atlantic Forest
biodiversity, close to which the new species was found.
Guapiaçu (latinised Guapiassu) is treated as an insti-
tutional name and adjectivised as guapiassuana. The
Tupi indigenous word Guapiaçu (= large headwaters)
is the name of the main river crossing the Reserve.
VERNACULAR NAME. The popular name ‘cereja-de-
guapiaçu’ (‘cherry of Guapiaçu’) is given to Eugenia
guapiassuana. The word ‘cereja’ (‘cherry’) is widely
used for fruits of Eugenia sect. Phyllocalyx, especially
those of the closely related E. involucrata (Lorenzi et
al. 2015).
NOTES. Eugenia guapiassuana can be recognised in its
habitat by its distinctively smooth, light-brown trunk
(when flowering and fruiting); leaf shoots adaxi-
ally cinereous, abaxially vinaceous; bracteoles and
sepals pinkish or vinaceous; petals whitish-pink; and
by its large, ellipsoid fruits that are red to vinaceous
and orange-eshed when ripe. The fruits are edible
and present a nice sweet-acid balance, resembling
other Eugenia sect. Phyllocalyx species. The edible
skin is very thin and red when fully ripe, enwrapping
the orange, juicy and abundant pulp, which rmly
adheres to the seed.
The morphology of Eugenia guapiassuana ts well
with the morphological concept of Eugenia sect.
Phyllocalyx, although the fruits lack the accrescent
bracteoles that are so typical of the section. Within
Eugenia sect. Phyllocalyx, mature fruits without brac-
teoles appear consistently only in E. selloi B.D.Jacks.
(Jackson 1893: 911).
Eugenia guapiassuana is morphologically closely
related to the widespread E. involucrata, the type
species of E. sect. Phyllocalyx. E. involucrata is com-
monly cultivated as a fruit tree in southern and south-
eastern Brazil, usually under the vernacular name
“cereja-do-rio-grande” (Lorenzi et al. 2015; Mazine
et al. 2020). It is also cultivated in other tropical to
subtropical countries, e.g., Florida, USA, where it has
been grown since 1938 under the popular designa-
tion of ‘Cherry of the Rio Grande’ (Menninger 1959).
Indeed, fruits of the two species have a similar taste
(see description above). E. guapiassuana diers from
E. involucrata, however, by the characters given in the
Recognition section above and described in Table 1.
Acknowledgements
TF thanks Conselho Nacional de Desenvolvimento
Cientíco e Tecnológico (CNPq) for a scholarship
(Process nº. 141327/2020-0) and Universidade Fed-
eral Fluminense (UFF) and NIT herbarium for lab-
oratory support. PVP benets from a post-doc grant
from CNPq (Process nº. 152888/2022-5). The authors
are especially grateful to the REGUA team, especially
managers Nicholas Locke and Raquel Locke, and for-
est ranger Messias Gomes da Silva, whose support was
fundamental for the preparation of this study.
Declarations
Conict of Interest The authors declare they have no
conict of interest.
References
Bachman, S., Moat, J., Hill, A. W., de la Torre, J. &
Scott, B. (2011). Supporting Red List threat assess-
ments with GeoCAT: geospatial conservation assess-
ment tool. ZooKeys 150: 117 – 126. https:// doi. org/
10. 3897/ zooke ys. 150. 2109.
Barros, A. A. M. (2008). Análise florística e estrutural
do Parque Estadual da Serra da Tiririca, Niterói
e Maricá, RJ, Brasil. PhD thesis, Instituto de
Pesquisas Jardim Botânico do Rio de Janeiro, Rio
de Janeiro.
Beentje, H. (2010). The Kew Plant Glossary. Royal
Botanic Gardens, Kew.
Briggs, B. G. & Johnson, L. A. S. (1979). Evolution in
the Myrtaceae — Evidence from inorescence struc-
ture. Proc. Linn. Soc. New South Wales 102: 157 – 254.
Bünger, M. O., Mazine, F. F., Lucas, E. J. & Stehmann,
J. R. (2016). Circumscription and synopsis of
Eugenia section Speciosae Bünger & Mazine (Myrta-
ceae). PhytoKeys 61: 73 – 80. https:// doi. org/ 10.
3897/ phyto keys. 61. 7904.
Bünger, M. O., Mazine, F. F. & Stehmann, J. R. (2020).
Revision of Eugenia section Phyllocalyx (Myrtaceae).
Phytotaxa 474: 99 – 118. https:// doi. org/ 10. 11646/
phyto taxa. 474.2.1.
Carvalho, P. E. R. (2008). Espécies arbóreas brasileiras.
Vol. 3. Embrapa Informação tecnológica, Brasília.
Chave, J., Muller-Landau, H. C., Baker, T. R., Easdale,
T. A., ter Steege, H. & Webb, C. O. (2006). Regional
and phylogenetic variation of wood density across
2456 neotropical tree species. Ecol. Applic. 16: 2356
KEW BULLETIN
© The Board of Trustees of the Royal Botanic Gardens, Kew, 2024
– 2367. https:// doi. org/ 10. 1890/ 1051- 0761(2006)
016[2356: RAPVOW] 2.0. CO;2.
CRIA (Centro de Referência em Informação Ambi-
ental) (2022). Herbário Virtual da Flora e dos Fun-
gos. Available from: http:// inct. splink. org. br/
[Accessed 19 May 2023].
de Candolle, A. P. (1828). Myrtacées. In: A. P. de Can-
dolle (ed.), Prodromus systematis naturalis regni vegeta-
bilis 3: 207 – 296. Treuttel & Würtz, Paris. https://
www. biodi versi tylib rary. org/ item/ 7152# page/ 218/
mode/ 1up.
Fernandes, T., da Silva Machado, D. N., da Costa
Souza, M., Bünger, M., de Barros, A. A. M., Prieto,
P. V. & Braga, J. M. A. (2023). Two new species of
Eugenia (Myrtaceae) from the Brazilian Atlantic
Forest. Kew Bull. 78: 95 – 105. https:// doi. org/ 10.
1007/ s12225- 022- 10070-z.
Giaretta, A., Menezes, L. F. T. & Pereira, O. J. (2013).
Structure and floristic pattern of a coastal dunes
in southeastern Brazil. Acta Bot. Bras. 27: 87 – 107.
https:// doi. org/ 10. 1590/ S0102- 33062 01300 01000 11.
Gressler, E., Pizo, M. A. & Morellato, P. C. (2006). Pol-
lination and seed dispersal of Brazilian Myrtaceae.
Brazil. J. Bot. 29: 509 – 530. https:// doi. org/ 10.
1590/ S0100- 84042 00600 04000 02.
Hewson, H. J. (1988). Plant Indumentum, a handbook
of terminology. Australian Government Publishing
Service, Canberra.
Hickey, L. J. (1973). Classication of the architecture
of Dicotyledonous leaves. Amer. J. Bot. 60: 17 – 33.
https:// doi. org/ 10. 1002/j. 1537- 2197. 1973. tb101 92.x.
IUCN (2012). IUCN Red List Categories and Criteria,
Version 3.1. 2nd edition. Prepared by the Species
Survival Commission. International Union for Con-
servation of Nature, Gland and Cambridge. Avail-
able from: https:// porta ls. iucn. org/ libra ry/ sites/
libra ry/ files/ docum ents/ RL- 2001- 001- 2nd. pdf.
[Accessed 19 May 2023].
IUCN (2022). Guidelines for Using the IUCN Red List
Categories and Criteria. Version 15.1. Prepared by the
Standards and Petitions Subcommittee. Interna-
tional Union for Conservation of Nature, Gland and
Cambridge. Available from: http:// www. iucnr edlist.
org/ docum ents/ RedLi stGui delin es. pdf. [Accessed
19 May 2023].
Jackson, B. D. (1893). Index Kewensis: an enumeration of
the genera and species of owering plants from the time
of Linnaeus to the year 1885 inclusive together with their
authors’ names, the works in which they were rst pub-
lished, their native countries and their synonyms. Vol. 1
(fasc. 2) – A-Cran. Clarendon Press, Oxford.
JSTOR Global Plants (2022). https:// plants. jstor. org/.
[Accessed 19 May 2023].
Linnaeus, C. (1753). Species Plantarum. Vol. 1. Impensis
Laurentii Salvii, Stockholm. https:// www. biodi versi
tylib rary. org/ page/ 358012# page/ 482/ mode/ 1up.
Lohbeck, M., Lebrija-Trejos, E., Martínez-Ramos, M.,
Meave, J. A., Poorter, L. & Bongers, F. (2015). Func-
tional trait strategies of trees in dry and wet tropical
forests are similar but dier in their consequences
for succession. PLoS ONE 10: e0123741. https:// doi.
org/ 10. 1371/ journ al. pone. 01237 41.
Lorenzi, H., Lacerda, M. T. C. & Bacher, L. B. (2015).
Frutas no Brasil: nativas e exóticas (de consumo in nat-
ura). Instituto Plantarum de Estudos da Flora, São
Paulo.
Mazine, F. F., Faria, J. E. Q., Giaretta, A., Vasconcelos,
T., Forest, F. & Lucas, E. (2018). Phylogeny and
biogeography of the hyper-diverse genus Eugenia
(Myrtaceae: Myrteae), with emphasis on E. sect.
Umbellatae, the most unmanageable clade. Taxon 67:
752 – 769. https:// doi. org/ 10. 12705/ 674.5.
Mazine, F. F., Valdemarin, K. S., Bünger, M. O., Faria,
J. E. Q., Fernandes, T., Giaretta, A., Santana, K.
C., Sobral, M. & Souza, M. A. D. (2020). Eugenia
in Flora do Brasil 2020. Jardim Botânico do Rio de
Janeiro. Available from: http:// ora dobra sil. jbrj.
gov. br/ reo ra/ ora dobra sil/ FB103 38. [Accessed
19 May 2023].
Menninger, E. A. (1959). The cultivated Eugenias in
American gardens, part 2. Natl. Hort. Mag. 38: 145
– 163.
Nascimento, M., da Cunha, M. & Vieira, T. (2023).
HUENF herbarium - Universidade Estadual do Norte
Fluminense — Herbário Virtual REFLORA. Version
1.142. Instituto de Pesquisas Jardim Botanico do
Rio de Janeiro. Occurrence dataset. Available from:
https:// ipt. jbrj. gov. br/ reo ra/ resou rce?r= huenf
&v= 1. 142.
Nic Lughadha, E. N. & Proença, C. (1996). A survey
of the reproductive biology of the Myrtoideae
(Myrtaceae). Ann. Missouri Bot. Gard. 83: 480 – 503.
https:// doi. org/ 10. 2307/ 23999 90.
Niedenzu, F. (1893). Myrtaceae. In: A. Engler & K.
Prantl (eds), Die Natürlichen Panzenfamilien 3 (7):
57 – 105. Engelmann, Leipzig.
Oliveira-Filho, A. T. & Fontes, M. A. L. (2000). Patterns
of oristic dierentiation among Atlantic forests in
southeastern Brazil and the inuence of climate.
Biotropica 32 (4b): 793 – 810. https:// doi. org/ 10.
1111/j. 1744- 7429. 2000. tb006 19.x.
Pizo, M. A. (2000). The seed-dispersers and fruit
syndromes of Myrtaceae in the Brazilian Atlantic
Forest, pp. 129 – 143. In: D. J. Levey, W. R. Silva &
M. Galetti (eds), Seed Dispersal and Frugivory: Ecol-
ogy, Evolution and Conservation. CABI Publishing,
Oxon. https:// doi. org/ 10. 1079/ 97808 51995 250.
0129.
QGIS Development Team (2022). QGIS Geographic
Information System. Open Source Geospatial Foun-
dation Project. Available from: http:// qgis. osgeo.
org/. [Accessed 19 May 2023].
KEW BULLETIN
© The Board of Trustees of the Royal Botanic Gardens, Kew, 2024
Radford, A. E., Dickson, W. C., Massey, J. R. & Bell, C.
R. (1974). Vascular Plant Systematics. Harper & Row
Publisher, New York.
REFLORA (2022). Herbário. Available online from:
http:// ora dobra sil. jbrj. gov. br/ reo ra/ herba rioVi
rtual. [Accessed 19 May 2023].
Rüger, N., Comita, L. S., Condit, R., Purves, D., Rosen-
baum, B., Visser, M. D., Wright, S. J. & Wirth, C. (2018).
Beyond the fast-slow continuum: demographic dimen-
sions structuring a tropical tree community. Ecol. Letters
21: 1075 – 1084. https:// doi. org/ 10. 1111/ ele. 12974.
Staggemeier, V. G., Cazetta, E. & Morellato, L. P. C.
(2017). Hyperdominance in fruit production in the
Brazilian Atlantic rain forest: the functional role of
plants in sustaining frugivores. Biotropica 49: 71 – 82.
https:// doi. org/ 10. 1111/ btp. 12358.
Thiers, B. (2023, continuously updated). Index Herbariorum:
A Global Directory of Public Herbaria and Associated Sta. New
York Botanical Garden’s Virtual Herbarium. http:// sweet
gum. nybg. org/ scien ce/ ih/. [Accessed 19 May 2023].
Urbanetz, C., Tamashiro, J. Y. & Kinoshita, L. S. (2010).
Floristic composition and similarity analysis of an
Atlantic rain forest fragment in Cananéia, São Paulo
State, Brazil. Brazil. J. Bot. 33: 639 – 651. https:// doi.
org/ 10. 1590/ S0100- 84042 01000 04000 12.
Publisher's Note
Springer Nature remains neutral with regard to juris-
dictional claims in published maps and institutional
aliations.
Springer Nature or its licensor (e.g. a society or other partner)
holds exclusive rights to this article under a publishing
agreement with the author(s) or other rightsholder(s);
author self-archiving of the accepted manuscript version of
this article is solely governed by the terms of such publishing
agreement and applicable law.
