See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/280087448

Clusia heterocolorata (Clusiaceae), a new species from the Brazilian Atlantic

Forest

Article  in  Phytotaxa · July 2015

DOI: 10.11646/phytotaxa.220.1.8

CITATIONS READS

6 357

3 authors:

Lucas C. Marinho André M. Amorim

Universidade Federal do Maranhão Universidade Estadual de Santa Cruz
74 PUBLICATIONS   138 CITATIONS    188 PUBLICATIONS   2,136 CITATIONS   

SEE PROFILE SEE PROFILE

Volker Bittrich

136 PUBLICATIONS   2,285 CITATIONS   

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Amazonian floristics and taxonomy View project

Flora do Brasil 2020 - Hypericaceae View project

All content following this page was uploaded by Lucas C. Marinho on 04 June 2017.

The user has requested enhancement of the downloaded file.

 Phytotaxa 220 (1): 083–088 ISSN 1179-3155 (print edition)
www.mapress.com/phytotaxa/
Article PHYTOTAXA
Copyright © 2015 Magnolia Press ISSN 1179-3163 (online edition)

http://dx.doi.org/10.11646/phytotaxa.220.1.8

Clusia heterocolorata (Clusiaceae), a new species from the Brazilian Atlantic

Forest
LUCAS CARDOSO MARINHO1,3, ANDRÉ MÁRCIO AMORIM2,3 & VOLKER BITTRICH4
¹ Programa de Pós-Graduação em Botânica, Universidade Estadual de Feira de Santana, Av. Transnordestina, Novo Horizonte, 44036-
900, Feira de Santana, Bahia, Brazil. E-mail: lcmarinho1@gmail.com
2
Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Km 25 Rodovia Ilhéus-Itabuna, 45662-900, Ilhéus, Ba-
hia, Brazil. E-mail: amorim.uesc@gmail.com
3
Centro de Pesquisas do Cacau, Herbário CEPEC, Km 22 Rodovia Itabuna-Ilhéus, 45650-970, Itabuna, Bahia, Brazil
4
R. Mario de Nucci, 500, 13083-290, Campinas, São Paulo, Brazil. E-mail: folcar2007@gmail.com

Abstract

Clusia heterocolorata is described, illustrated, its diagnostic characteristics, morphological affinities, and conservation sta-
tus are discussed, and a geographical distribution map is presented. This new species belongs to the section Phloianthera,
characterized by a dome-shaped androecium with numerous resiniferous stamens and staminodes.

Key words: Bahia, Clusieae, Malpighiales, northwestern Brazil, taxonomy

Resumo

Clusia heterocolorata é descrita, ilustrada, suas características diagnósticas, afinidades morfológicas e status de conservação
são discutidos e um mapa de distribuição geográfica é apresentado. Essa nova espécie pertence à seção Phloianthera, carac-
terizada pelo androceu em formato de cúpula com numerosos estames e estaminódios resiníferos.

Palavras-chave: Bahia, Clusieae, Malpighiales, Nordeste do Brasil, taxonomia

Introduction

Clusia L. (1753: 510) (Clusiaceae, tribe Clusieae) is a neotropical genus distributed from Florida (USA) to Rio Grande
do Sul (Brazil) whose component taxa mostly occur in wetlands, or dryer areas such as savannas and rocky fields.
Approximately 68 species are distributed throughout Brazil (Bittrich et al., 2015).
Clusia comprises about 300 species of mostly dioecious hemiepiphytes, shrubs and trees that always have glabrous,
opposite and carnose leaves (Planchon & Triana, 1860). The fruits are septifragal carnose capsules, with more than
one seed per locule (with few exceptions), usually with a brightly colored aril (Barroso et al., 1999). Wide variations
in morphologies of the androecium and pistil—the former especially important in subgeneric classification—among
species that may have very similar leaf morphologies can lead to errors in identification and delimitation of the species
(Bittrich, 1996).
Recent inventories undertaken in previously unexplored areas of dense montane rainforests in Bahia State, Brazil,
have revealed new occurrences of many vascular plants (Amorim et al., 2009; Matos et al., 2010; Coelho & Amorim,
2014), providing opportunities to analyze collections of otherwise neglected families such as Clusiaceae that show
ample diversity in the Atlantic Forest biome. A number of endemic species from the Atlantic Forest in Bahia have been
described in recent years, especially in the Corcovado Range (e.g., Sundue & Prado, 2005; Goldenberg & Reginato,
2009; Mynssen & Matos, 2012; Marinho et al., 2015), the only known locality of the new species proposed here.

Accepted by Zhi-Qiang Zhang: 3 Jul. 2015; published: 16 Jul. 2015 83

Taxonomy

Clusia heterocolorata L. Marinho & Bittrich, sp. nov. (sect. Phloianthera) (Figs. 1, 2, 3)

Clusia heterocolorata L. Marinho & Bittrich is a dioecious tree with white to cream-colored latex. The staminate
flowers have 5, cream colored petals; the androecium is dome-shaped, circular, with a prominent synandrium,
the basal-lateral region has staminodes covered by resin and pollen. The pistillate flowers have 5, cream colored
petals, with basal half pink; staminodes 4-seriate, resiniferous, surrounding the base of the ovary; 5 stigmas,
smooth, obtusely triangular.
Type:—BRAZIL. Bahia: Mun. Almadina, Mirante da Serra do Corcovado, acesso pela roça do Sr. Francisco, 14º42’13”S, 39º36’08”W,
600–850 m, 20 November 2013, L.C. Marinho, L.C. Gomes, L.H. Daneu & D.S.B. Rocha 578 (fl. ♂) (holotype HUEFS!, isotypes
CEPEC!, K!, NY!, P!, RB!, SPF!).

FIGURE 1. Map showing the geographic distribution of Clusia heterocolorata (black circle).

Trees up to 6 m tall, dioecious, with latex white to cream-colored; young branches cylindrical, with smooth surfaces,
linear colleters present in the petiole axils. Petiole 6–8 mm long, cylindrical. Leaf blade coriaceous, discolorous, adaxial
surface dark brown in sicco, obovate, (3–)5.8–8.5 cm long and (2–)4–5.5 cm wide, apex rounded, base rounded, rarely
attenuate, margin revolute; midrib prominent on the adaxial surface and conspicuous up to the mid blade, secondary
veins 13–15 pairs, prominent on abaxial and adaxial surfaces only in sicco, immersed in vivo, 3.5–5 mm distant from
each other and forming an angle of 45º–60º with the midrib, basal veins inconspicuous; latex canals inconspicuous on
adaxial surface, immersed, conspicuous only on abaxial surface in sicco, 0.1–0.4 mm distant from each other, parallel
to the secondary veins, forming an angle of about 45º with the midrib. Inflorescence cymose, compact, 6-flowered
(staminate plants) or 3-flowered (pistillate plants), bracts and bracteoles ca. 2.5 mm long, triangular, pedicels 0.5–15
mm long, cylindrical. Floral buds 10–11 mm long, orbicular. Epicalyx bracts 2, united at base, triangular. Sepals 8

84 • Phytotaxa 220 (1) © 2015 Magnolia Press MARINHO ET AL.

(2+2, 2+2), green or light green, oblong to obtusely triangular; external sepals 8–10 mm long and 5–6 mm wide,
internal sepals 6–7 mm long and 5–6 mm wide. Staminate flower with 5 petals, 10–11 mm long and 7.5–10 mm
wide, obdeltiform to obovate, cream-colored, margin entire, not sinuous; androecium forming a dome-shaped, circular,
prominent synandrium, 3–4 mm tall and 3–4 mm wide, composed of ca. 250 densely packed stamens, the upper
surface covered by pollen during anthesis with low resin production, free portions of the filaments ca. 1 mm long,
anther ca. 0.5 mm long, dehiscent by apical slits with inconspicuous apertures, base-lateral region of the dome-shaped
androecium without anthers (staminodes) covered by a mixture of resin and pollen. Pistillate flower with 5 petals,
10–11 mm long and 9–10 mm wide, obdeltiform, cream-colored with basal half pink, margin entire and sinuous; 4
series of staminodes ca. 0.7 mm long surrounding the base of the ovary, secreting resins at their apices; staminodes
orange, truncated at apex, without sterile anthers; styles ca. 1 mm long; stigmas 5, ca. 1.5 mm long, apical, yellowish,
obtusely triangular, smooth; ovary 1.5–1.8 cm long, white, 5-locular, ovules 2–3 per locule. Fruit not seen.

FIGURE 2. Clusia heterocolorata. A—Stem with floral buds; B—Abaxial surface of the leaf; C—Detail of bracteoles and sepals of the
staminate flowers; D—Staminate flowers; E—Detail of the androecium (L.C. Marinho 578); F—Detail of the bracteoles and sepals of
the pistillate flower; G—Pistillate flower; H—Detail of the pistil and staminodes (L.C. Marinho 922); I—View of the Corcovado Range,
Bahia State, Brazil (arrow indicates the collection site). Photos: A–E, I by L.C. Marinho; F–H by A. Francener.

Clusia heterocolorata (Clusiaceae) Phytotaxa 220 (1) © 2015 Magnolia Press • 85

FIGURE 3. Clusia heterocolorata. A—Stem with floral buds and staminate flowers; B—Floral bud; C—Detail of the bracteoles and
sepals of the staminate flower in abaxial view; D—External sepal; E—Internal sepal; F—Petal of the staminate flower; G—Staminate
flower; H—Detail of the androecium. I—Petal of pistillate flower; J—Pistillate flower; K—Detail of a pistil (A–H: L.C. Marinho 578,
holotype; I–K: L.C. Marinho 922). Illustration by L.C. Marinho.

86 • Phytotaxa 220 (1) © 2015 Magnolia Press MARINHO ET AL.

 Comparison: Clusia heterocolorata was assigned to the section Phloianthera (1860: 319) proposed by Planchon
& Triana and confirmed by Gustafsson et al. (2007). This section comprises 11 species, mostly occurring in eastern
Brazil, although some Amazonian and Andean species have been described. The androecium is commonly dome-
shaped in this section, with numerous resiniferous stamens and staminodes. The male flowers of some species of the
section, however, such as Clusia microstemon Planchon & Triana (1860: 331) and Clusia nitida Bittrich & F.N. Cabral
(2013: 36), have a flat, disc-shaped androecium with fertile stamens producing resins (i.e. as the male flowers lack
staminodes).
Clusia heterocolorata is sympatric with Clusia melchiorii Gleason (1931: 403), but they can be easily distinguished
by the former having 5 petals (4 in C. melchiorii), much more numerous stamens with very short filaments, and the
presence of staminodes on the male flowers (the male flowers of C. melchiorii have up to 40 stamens with 3–5 mm
long filaments, and lack staminodes) and floral resin (completely lacking in the nectariferous flowers of C. melchiorii),
besides, C. melchiorii belongs to C. sect. Anandrogyne. Clusia pilgeriana Mansf. (1924: 154), is also similar to the
new species and belongs to the same section (Phloianthera). It occurs on mountains covered by Atlantic Forest stands
within the otherwise dry caatinga region (“brejos de altitude”) in Pernambuco and southern Paraiba States. Clusia
pilgeriana can be distinguished by having less numerous sepals (4–5 instead of 8), the diameters of its flowers (35–40
mm vs. 23–25 mm in both flowers of C. heterocolorata), its larger campanulate instead of radiate flowers (sepals
12–15 × 15–16 mm, petals 12–15 × 11–15 mm), and a 5–8-locular ovary (vs. 5-locular) with larger and sessile or
subsessile stigmas (2–3.5 vs. ca. 1.5 mm long).
Etymology:—Greek heteros = different; Latin colorata = color. The specific epithet refers to the remarkably
different colors of the corollas of the staminate and pistillate flowers.
Distribution, habitat, and conservation:—Clusia heterocolorata occurs in southern Bahia State, Brazil, in areas
of dense montane rainforest (800 to 850 m alt.). The specimens were collected on a rocky massif (a type of inselberg)
in the Corcovado Range. This mountain range is located at about 65 km from the coast in the municipality of Almadina
and forms part of the Almadina River basin (Coelho & Amorim, 2014).
The Clusia heterocolorata population examined contains approximately 20 staminate and pistillate plants that are
randomly dispersed throughout an area of ca. 10 km². As they grew on the top of the Corcovado massif, these trees are
exposed to full sunlight and comprise part of the low canopy of this forested area. According to the criteria adopted
by IUCN (2015), the species can be considered critically endangered as the population is composed of less than 50
individuals (D) and its extent of occurrence (B1) and area of occupancy (B2) are less than 100 km².
Additional specimen examined (paratypes):—BRAZIL. Bahia: Mun. Almadina, Serra do Corcovado, entrando
pela fazenda de Seu Francisco, 14º42’12.7”S, 39º36’8.6”W, 836 m, 23 November 2014 (fl. ♀), L.C. Marinho, L.H.
Daneu, R.C. Asprino, R.F. Almeida & A. Francener 922 (ALCB, CEPEC, HUEFS, RB, UEC, UFP); Mun. Almadina,
Serra do Corcovado, entrando pela fazenda de Seu Francisco, 14º42’12.7”S, 39º36’8.6”W, 836 m, 23 November 2014
(fl. ♂), L.C. Marinho L.H. Daneu, R.C. Asprino, R.F. Almeida & A. Francener 923 (CEPEC, HUEFS).

Acknowledgments

The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for awarding a PhD
Fellowship to LCM (grant #141561/2015-7) and a Research Productivity Fellowship to AMA (grant # 306992/2012-4).
The laboratory and fieldwork was financially supported by CNPq (Edital Reflora Malpighiales grant # 563548/2010-
0, PPBIO Mata Atlântica grant # 457483/2012-1, Universal grant # 486079/2013-9) and CAPES (PNADB Rede de
Epífitas grant # 1398/2010). We also thank the Programa de Pós-Graduação em Botânica (PPPGBot/UEFS) for the
laboratory structure, Dr. Barry Hammel for the invaluable contributions and Lukas Daneu at the CEPEC Herbarium
for his invaluable help with the fieldwork.

References

Amorim, A.M., Jardim, J.G., Lopes, M.M.M., Fiaschi, P., Borges, R.A.X., Perdiz, R.O. & Thomas, W.W. (2009) Angiospermas em
remanescentes de floresta Montana no sul da Bahia, Brasil. Biota Neotropica 9: 313–348.
Barroso, G.M., Morim, M.P., Peixoto, A.L. & Ichaso, C.L.F. (1999) Frutos e sementes: morfologia aplicada à sistemática de dicotiledôneas.

Clusia heterocolorata (Clusiaceae) Phytotaxa 220 (1) © 2015 Magnolia Press • 87

 Viçosa: Universidade Federal de Viçosa, Minas Gerais, Brasil, 443 pp.
Bittrich, V. (1996) Três novas espécies do gênero Clusia (Guttiferae) do Brasil. Boletim de Botânica da Universidade de São Paulo 15:
733–782.
Bittrich, V., Cabral, F.N. & Hopkins, M.J.G. (2013) Clusia nitida, a new species of Clusia (Clusiaceae) from the Brazilian Amazon.
Phytotaxa 100 (1): 36–40.
http://dx.doi.org/10.11646/phytotaxa.100.1.4
Bittrich, V., Trad, R.J., Cabral, F. & Nascimento-Jr., J.E. (2015) Clusiaceae. In: Lista de Espécies da Flora do Brasil. Jardim Botânico do
Rio de Janeiro. Available from: http://floradobrasil.jbrj.gov.br/2012/FB006883 (accessed 20 January 2015)
Coelho, M.M. & Amorim, A.M. (2014) Floristic composition of the Montane Forest in the Almadina–Barro Preto axis, Southern Bahia,
Brazil. Biota Neotropica 14: 1–41.
http://dx.doi.org/10.1590/S1676-06033878
Gleason, H.A. (1931) Botanical results of the Tyler-Duida Expedition, continued from the May issue. Bulletin of the Torrey Botanical
Club 58: 345–404.
Goldenberg, R. & Reginato, M. (2009) New species of Behuria, Miconia, and Ossaea (Melastomataceae) from Eastern Brazil. The
Journal of the Torrey Botanical Society 136 (3): 293–301.
http://dx.doi.org/10.3159/09-RA-019.1
Gustafsson, M.H.G., Winter, K. & Bittrich, V. (2007) Diversity, phylogeny and classification of Clusia. In: Lüttge, U. (Ed.) Clusia—A
woody Neotropical genus of remarkable plasticity and diversity. Springer, New York, pp. 95–116.
http://dx.doi.org/10.1007/978-3-540-37243-1_7.
IUCN (2015) Guidelines for Using the IUCN Red List Categories and Criteria. Version 11. Prepared by the Standards and Petitions
Subcommittee, Gland and Cambridge. Available from: http://www.iucnredlist.org/documents/RedListGuidelines.pdf (accessed 20
January 2015).
Linnaeus, C. (1753) Species Plantarum. Laurentius Salvius, Stockholm, 1200 pp.
Mansfeld, R. (1924) Plantae Luetzelburgianae brasilienses V. Notizblatt des Botanischen Gartens und Museums zu Berlin-Dahlem 9:
153–156.
Marinho, L.C., Fiaschi, P. & Amorim, A.M. (2015) A new species of Tovomita Aubl. (Clusiaceae) from the Brazilian Atlantic Forest.
Phytotaxa 207 (2): 193–199.
http://dx.doi.org/10.11646/phytotaxa.207.2.6
Matos, F.B., Amorim, A.M. & Labiak, P.H. (2010) The Ferns and Lycophytes of a Montane Tropical Forest in Southern Bahia, Brazil.
Botanical Research Institute of Texas Journal 4: 333–346.
Mynssen, C.M. & Matos, F.B. (2012) Diplazium fimbriatum (Athyriaceae), a New species from Brazil. American Fern Journal 102:
167–173.
http://dx.doi.org/10.1640/0002-8444-102.2.167
Planchon, J.E. & Triana, J. (1860) Mémoire sur la famille de Guttifères. Annales des Sciences Naturelles, Botanique, Séries IV 13:
303–376.
Sundue, M.A. & Prado, J. (2005) Adiantum diphyllum, a rare and endemic species of Bahia State, Brazil and its close relatives. Brittonia
57: 123–128.
http://dx.doi.org/10.1663/0007-196X(2005)057[0123:ADARAE]2.0.CO;2

88 • Phytotaxa 220 (1) © 2015 Magnolia Press MARINHO ET AL.

View publication stats