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Pagamea spruceana (Rubiaceae, Gaertnereae), a new species from flooded

white-sand forests in the Upper Rio Negro region, Brazil

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 Phytotaxa 269 (3): 186–192 ISSN 1179-3155 (print edition)
http://www.mapress.com/j/pt/
Article PHYTOTAXA
Copyright © 2016 Magnolia Press ISSN 1179-3163 (online edition)

http://dx.doi.org/10.11646/phytotaxa.269.3.2

Pagamea spruceana (Rubiaceae, Gaertnereae), a new species from flooded white-

sand forests in the Upper Rio Negro region, Brazil
EDUARDO MAGALHÃES BORGES PRATA1*, RANGEL BATISTA DE CARVALHO1 & ALBERTO
VICENTINI1*
1
Instituto Nacional de Pesquisas da Amazônia (Inpa), Programa de Pós-Graduação em Botânica, Av. André Araújo, 2.936, 69067-375,
Manaus, Amazonas, Brazil
* Authors for correspondence: eduardombprata@gmail.com, alberto.vicentini@inpa.gov.br

Abstract

Pagamea spruceana, a new species from Northwestern Amazon, Brazil, is endemic to the Upper Rio Negro region, in the
Içana and Uaupés River Basins, and differs from other functionally dioecious species of Pagamea by its capitate and puberu-
lous inflorescences and narrowly elliptic leaf blades with revolute and puberulous margins. Pagamea spruceana is the only
species in the genus known from long-term inundated habitats (igapós) in the Amazon. The new species is here described
and the affinities with morphologically similar and closely related species are discussed.

Key Words: flooded forests, igapó, Rio Negro, white-sand

Resumo

Pagamea spruceana, uma nova espécie para o noroeste da Amazônia, Brasil, é endêmica da região do alto Rio Negro, nas
bacias dos rios Içana e Uaupés, e difere de outras espécies funcionalmente dióicas de Pagamea por suas inflorescências
capitadas e pubérulas, lâmina foliar estreitamente elíptica com margens revolutas e pubérulas. Pagamea spruceana é a única
espécie do gênero de ocorrência em igapós inundáveis por longos períodos na Amazônia. A nova espécie é aqui descrita e
suas afinidades com espécies morfologicamente similares e proximamente relacionadas são discutidas.

Palavras-chave: florestas inundáveis, igapó, Rio Negro, areia-branca

Introduction

Pagamea Aublet (1775: 44, Rubiaceae) is a monophyletic genus generally restricted to nutrient-poor white-sand soils in
the Amazon, Atlantic coast, Andes and the Chocó region in western Colombia (Vicentini & Steyermark 2004, Vicentini
2016). Species of Pagamea are usually shrubs or small trees found on white-sand habitats, from open savannas to tall
forests on dry or flooded soil systems, from sea level to 2800 m (Vicentini 2016). Pagamea is sister to the paleotropical
genus Gaertnera Lamarck (1792: 379), a relationship supported by morphology (sheathing stipules and a secondarily
superior ovary), wood anatomy, pollen (Igersheim et al. 1994, Jansen et al. 1996), and molecular data (Andersson &
Rova 1999, Malcomber 2002), and their divergence occurred in the Middle Miocene (~ 18.2 Mya; Bremer & Eriksson
2009). The sheathing stipules and the secondarily superior ovary that results in a drupe partially inserted in a cupule,
distinguish Pagamea from all other Rubiaceae in South America (Vicentini 2007).
In the latest revision of Pagamea, 31 species were recognized, of which ten were recognized as new, but not
published (Vicentini 2007). Species delimitation is complicated in many lineages of Pagamea for many reasons,
including morphological overlap between morphologically recognized species [e.g. Pagamea pilosa (Standley 1937:
279) Steyermark (1965: 276) and P. puberula Steyermark (1965: 276)] and non-monophyly of some morphologically
well-delimited species in the phylogenetic trees of Pagamea [e.g. P. plicatiformis Steyermark (1965: 274) and P.
spruceana)]. Until now, Pagamea spruceana (Vicentini 2007) has remained an unpublished name that refers to a
lineage morphologically and ecologically distinct from the rest of the genus, with geographical distribution restricted
186 Accepted by Piero Delprete: 28 Jul. 2016; published: 5 Aug. 2016
to the Upper Rio Negro region (basin of Içana and Uaupés Rivers), northwestern Amazon. In the phylogenetic tree of
Pagamea for the ITS region (Vicentini 2016), Pagamea spruceana is represented by a single accession that is most
closely related to one of the two clades of another species with the informal name “P. morphotype occulta”, which
forms two unrelated clades (Figure S1 in Vicentini 2016). Recently, we have assembled more flowering and fruiting
samples for Pagamea spruceana and related species during an ongoing study of the “Guianensis Clade” sensu Vicentini
(2016). In a phylogenetic analysis (to be published elsewhere) based on a high-throughput DNA sequencing for the
Guianensis Clade (N=176 samples, 431 markers), we found that P. spruceana (N=5) is reciprocally monophyletic to a
clade including both clades of “P. morphotype occulta” in Vicentini’s (2016) ITS tree with 100% posterior probability
(Prata et al. in prep.); therefore, according to this phylogenies “P. morphotype occulta” is sister to P. spruceana.
However, Vicentini (2007, 2016) overlooked the published name P. pilosa, whose type specimen (B.A. Krukoff 7083,
holotype F) is from the same locality and is morphologically consistent with specimens of “P. morphotype occulta”
from southern Amazon (Upper Madeira River Basin). For all the above reasons, here we assimilate this informal name
with P. pilosa. Pagamea spruceana and P. pilosa are sister species and sympatric in the Upper Rio Negro region.
Pagamea spruceana is morphologically and ecologically distinct from all other species of Pagamea, being the only
functional dioecious species with capitate inflorescences, and inhabiting the most extreme flooded igapó forests. These
sources of evidence support the circumscription of the new species Pagamea spruceana Vicentini & Prata, which is
described below.

Material & Methods

We collected samples of Pagamea spruceana along the Içana, Piraiauara and Uaupés Rivers during three expeditions
to the Upper Rio Negro region that took place in 2004, 2009 and 2013. Specimens were observed with a dissecting
microscope, and measured with a digital caliper. In the species description, measurements are represented by the range
of minimum and maximum values, followed by the average (mean value) and the standard deviation of the character
between parentheses. We opted for presenting the mean and the standard deviation because these two parameters
together with the range represent the distribution of the character rather than the range alone. For the morphological
description we used the terminology of Harris and Harris (2001). For the habitat description, we used the terminology
of Junk & Piedade (2010) to refer to the most extreme flooded forests in the Amazon. For the species delimitation,
we adopted the Biological Species Concept (Mayr 1992) and the General Lineage Species Concept (de Queiroz
2007), i.e., we interpreted the co-existence of morphologically, ecologically and monophyletic lineages as evidence of
reproductive isolation.
We generated a map in the software QGIS (QGIS Development Team 2015) to show the geographic distribution
of Pagamea with emphasis on the new species Pagamea spruceana, the morphologically similar Pagamea capitata
Benth. (1857: 85) and the closely related P. pilosa. We used IUCN (2016) criteria to determine the conservation status
of the new species.

Taxonomy

Pagamea spruceana Vicentini & Prata, sp. nov. (Figs. 1, 2)

Type:—Brazil. Amazonas: Mun. São Gabriel da Cachoeira, Rio Içana, Lago Jauacanã, 0°23’ N, 67°33’ W, 2 November 1987, C. Farney
& W.A. Rodrigues 1859 (holotype INPA, isotype MO).

Pagamea spruceana differs from other functionally dioecious species of the genus by its capitate and puberulous
inflorescences and narrowly elliptic leaf blades with revolute and puberulous margins, and is the only species known
from long-term inundated igapós in the Amazon. Pagamea spruceana is similar to P. capitata because of the capitate
inflorescence and leaves with revolute margins; the former can be distinguished from the latter by the elliptic leaf blades,
acute or acuminate at apex (vs. ovate, strongly acuminate at apex in P. capitata), caducous stipules (vs. persistent), and
petioles and peduncles glabrous or puberulous (vs. densely pubescent).
Treelets 2–6 m (4 ± 1.7 m) tall; stems 1–8 cm in diameter; outer bark brownish to darkish, slightly to strongly
fissured longitudinally; branchlets brownish to darkish. Stipules sheathing, cylindrical with 4–8 apical setae, 5–14 mm

Pagamea spruceana (Rubiaceae) Phytotaxa 269 (3) © 2016 Magnolia Press • 187
FIGURE 1. Pagamea spruceana. A. Flowering branch. B. Fruiting branch. C. Functionally pistillate flower. D. Ovary with short style in
a functionally staminate flower. E. Detail of leaf blade with puberulous margin. A and D from Carvalho 1612, B and E from Prata 1948,
C from Prata 1960. Drawn by R. B. de Carvalho.

(9.2 ± 2.4 mm) long, caducous or only the base persistent, usually puberulous. Leaves opposite, usually grouped at
the terminal portion of growth units, some branchlets almost entirely composed (up to 10 cm) of leaf scars; petioles
5.9–22 mm (12.3 ± 3.7 mm) long, glabrous to densely puberulous; blades narrowly elliptic, 44–116 x 12–37 mm
(69 ± 16 x 21 ± 5.7 mm), acute at base, acute or cuspidate at apex, coriaceous, glabrous to densely puberulous
abaxially, glabrous adaxially, margin puberulous and usually revolute, midrib sparsely to densely puberulous abaxially
and adaxially, venation eucamptodromous, veins arching, with 4–7 (5 ± 0.9) secondary veins on each side of midrib,
densely puberulous abaxially and glabrous adaxially, with 0–6 domatia at axils of secondary veins. Breeding system
functionally dioecious. Inflorescences capitate, peduncules 8.9–51 mm (32 ± 9.7 mm) long, greenish or reddish orange
at maturity, sparsely puberulous, the main axis 0–4(9) mm (3.1 ± 3.2 mm) long, secondary axis absent or very short.
Flowers small, distylous, sessile. Calyces cup-shaped, 1.5–4.1 mm long, cream-colored or greenish, glabrous inside
and glabrous or sparsely puberulous outside, 4-lobed, 0.3–2.2 mm (0.9 ± 0.4 mm) long. Corolla campanulate, 5.5 mm

188 • Phytotaxa 269 (3) © 2016 Magnolia Press PRATA ET AL.

long, cream-colored or greenish; tube glabrous inside; lobes 4, valvate, 4 mm long, puberulous abaxially, densely
pubescent adaxially with hairs usually longer at the base. Functionally staminate plants: Inflorescence with 30–40
(34.6) flowers; stamen 4, exserted, inserted at the base of the corolla tube, dorsifixed near the base; anthers oblong,
ovary secondarily superior, 2-locular, non functional, ovules solitary in each locule, distally puberulous; style short,
< 0.5 mm, stigmatic lobes 2 appressed against each other, non-papillose, not receptive. Functionally pistillate plants:
Inflorescence with 15–50 (26.6) flowers; stamen 4, exserted, inserted at the base of the corolla tube, dorsifixed near the
base, non functional; anthers oblong, densely packed with raphides, lacking pollen grain; ovary secondarily superior, 2-
locular, ovules solitary in each locule, distally puberulous; style long, > 1 mm long, stigmatic lobes 2, open, papillose,
receptive. Cupule 2.4–5.4 x 4.1–7.7 mm (4 ± 1.5 x 5.6 ± 1.1 mm), reddish orange, glabrous inside, glabrescent outside.
Fruits a fleshy drupe, ellipsoid, 5.2–8.7 x 4.2–5.6 mm (7.1 ± 1.5 x 5 ± 0.7 mm), black, basal portion included in the
cupule. Pyrene 2, hard, obdeltoid, single-seeded.

FIGURE 2. Pagamea spruceana. A. Leaf with revolute margin B. Detail of leaf blade with puberulous margin. C. Capitate inflorescences
with buds and flowers. D. Inflorescence with fruits; main axis and cupules reddish orange and green, immature fruits. E. Inflorescence
head and distal portion of peduncle. F. Ovary with long style in a functionally pistillate flower. G. Ovary with short style in a functionally
staminate flower. H. Stem with dark brown bark. I. Individual of P. spruceana. J. Long-term inundated igapó at Piraiauara River, in the
Upper Rio Negro region. Photos by E. Prata.

Distribution and habitat:—This species is known from the Içana and Uaupés Rivers Basins in the Upper Rio
Negro region (Figure 3), State of Amazonas, Brazil. It occurs in open vegetation or low forests in long-term inundated
white-sand habitats on the margin of lakes and rivers (igapós).

Pagamea spruceana (Rubiaceae) Phytotaxa 269 (3) © 2016 Magnolia Press • 189
FIGURE 3. Distribution map of Pagamea spruceana Vicentini & Prata (red stars), P. capitata (empty circles), P. pilosa (gray circles),
and all Pagamea collections (small circles).

Flowering and fruiting:—Flowering plants were found in June and fruiting specimens (some with few old
flowers) were collected in November and December.
Conservation status:—The geographical distribution of Pagamea spruceana corresponds to one of the less
threatened regions in the Brazilian Amazon, which is mostly protected by the Brazilian laws (Protected Areas and
Indigenous Territories according to Instituto Socioambiental 2016). Pagamea spruceana can therefore be assessed as
Least Concern (LC) according to IUCN categories and criteria (IUCN 2015), despite its narrow distribution.
Etymology:—The specific epithet is dedicated to Richard Spruce (1817–1983). Although Spruce has never
collected this species, he made many collections and described several species of Pagamea.
Additional collection examined (paratypes):—BRAZIL. Amazonas. São Gabriel da Cachoeira, Igarapé Jurupary,
Rio Uaupés, 1°37’0” N, 68°53’0” W, 94 m, 2 November 1932, A. Ducke 24417 (F); Igarapé Tibuiari, afluente do Rio
Uaupés, Monte Cristo, 0°5’0” N, 67°20’0” W, 74 m, 22 November 1987, M.I. Kawasaki 242 (NY); Rio Içana, acima de
Peraiauara, 1°0’0” N, 68°0’10” W, 99 m, 14 May 1973, M.F. Silva & P. Machado 1530 (INPA, US); Rio Içana, Vila de
Jauacanã, 0°33’47” N, 67°24’9” W, 73 m, 27 June 2004, A. Vicentini & L. Rodríguez 2266 (MO); loc. cit., 27 June 2004,
A. Vicentini & L. Rodríguez 2276 (MO); Rio Uaupés, Comunidade Monte Cristo, 67°14’34” N, 0°01’41” W, 72 m, 18
June 2009, F.A. Carvalho, A. Vicentini, M.H. Terra-Araújo, N.C. Dávila & J.M. Brito 1608 (INPA); loc. cit., 18 June
2009, F.A. Carvalho, A. Vicentini, M.H. Terra-Araújo, N.C. Dávila & J.M. Brito 1612 (INPA); loc. cit., 18 June 2009,
F.A. Carvalho, A. Vicentini, M.H. Terra-Araújo, N.C. Dávila & J.M. Brito 1614 (INPA); Rio Piraiauara, afluente do
Rio Içana, 0°49’09” N, 67°32’52” W, 79 m, 5 December 2013, E.M.B. Prata, N.C. Dávila, J.E. Nascimento-Junior, F.
Cabral & O.F. Menezes 1948 (INPA); Rio Piraiauara, afluente do Içana, 0°49’10” N, 67°32’45” W, 85 m, 5 December
2013, E.M.B. Prata, N.C. Dávila, J.E. Nascimento-Junior, F. Cabral & O.F. Menezes 1955 (INPA); Rio Içana, Vila
de Jauacanã, 0°33’56” N, 67°23’52” W, 73 m, 6 December 2013, E.M.B. Prata, N.C. Dávila, J.E. Nascimento-Junior,
F. Cabral & O.F. Menezes 1959 (INPA); Rio Içana, Vila de Jauacanã, 0°33’58” N, 67°23’48” W, 73 m, 6 December
2013, E.M.B. Prata, N.C. Dávila, J.E. Nascimento-Junior, F. Cabral & O.F. Menezes. 1960 (INPA); Rio Içana, Vila de
Jauacanã, 0°33’58” N, 67°23’48” W, 73 m, 6 December 2013, E.M.B. Prata, N.C. Dávila, J.E. Nascimento-Junior, F.
Cabral & O.F. Menezes 1961 (INPA).
190 • Phytotaxa 269 (3) © 2016 Magnolia Press PRATA ET AL.
Discussion

Pagamea spruceana resembles P. capitata because of the capitate inflorescences and leaves with revolute margins. The
former differs from the latter by the elliptic leaf blades acute or acuminate at apex (vs. ovate and strongly acuminate at
apex in P. capitata), caducous stipules (vs. persistent) and glabrous or puberulous petioles and peduncles (vs. densely
pubescent in P. capitata). Regarding the breeding system, P. spruceana has functionally unisexual flowers (plants
are functionally dioecious) and P. capitata has hermaproditic flowers (usually homostylous, rarely distylous in some
individuals). Both species occur in the Içana River Basin in the Upper Rio Negro region, but P. spruceana is found
in long-term inundated igapós while P. capitata is restricted to non-flooded shrub-lands or sandstones formations
(Vicentini 2007, 2016). Furthermore, these species are only distantly related in the phylogenetic trees of the genus
(Vicentini 2016).
Pagamea has been reported to be a distylous genus (Steyermark 1965, 1973), although Bentham (1857) already
noted that in Pagamea “the flowers (…) have a tendency to become polygamous, by the abortion of the female organs
in some flowers, and occasionally of the anthers in others.” Vicentini (2007) described two major breeding systems
for species of Pagamea: homostyly and functional dioecy. Functional dioecy was inferred because specimens with
fruits correspond to long-styled morphs, belonging to functionally pistillate plants, with anthers densely packed with
raphides and lacking pollen grains. On the other hand, functionally staminate plants have extremely reduced styles,
with closed (i.e., lobes appressed against each other), non-papillose, non-receptive stigmatic lobes, and non-functional
ovary. Functional dioecy in Pagamea was later confirmed for Pagamea duckei Standley (1937: 278) based on a
cross-pollination experiment (Terra-Araujo et al. 2012) and for P. coriacea Spruce ex Bentham (1857: 110) based
on floral morphology (Esteves & Vicentini 2013). Breeding system variation is also phylogenetically conserved in
Pagamea despite some intraspecific variation, with functionally dioecious species forming a clade where P. spruceana
is included (Vicentini 2007). Pagamea spruceana is the only species with capitate inflorescences among the 15 species
in this dioecious clade.
According to the molecular phylogenies produced by Vicentini (2016) and Prata et al. (in prep.), Pagamea
spruceana is the sister species of P. pilosa, from which it can be distinguished by the capitate inflorescence (vs. thyrsoid
in P. pilosa), ovaries puberulous in the upper half (vs. glabrous or puberulous only at distal portion) and narrowly
elliptic leaf blades (vs. elliptic-obovate) with puberulous, revolute margins (vs. glabrous and flat). These species are
sympatric at the Içana River Basin, in the Upper Rio Negro region, but P. spruceana is always found in more deeply
(and long-term) inundated igapós. These species are morphologically and ecologically different, sympatric, and form
reciprocally monophyletic clades in the phylogenetic tree (Prata et al. in prep.), suggesting reproductive isolation
and fitting both the Biological Species Concept (Mayr 1992) and the General Lineage Species Concept (de Queiroz
2007).

Acknowledgements

We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Universal 478539/2011-8)
and the Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM, Universal Amazonas 062.00205/2013)
for the financial support for this research and CNPq for the scholarship to EMBP. We are grateful to FOIRN, FUNAI
and Indigenous people for the permits for botanical collection at Indigenous Territories in the Upper Rio Negro region.
We thank to Nallarett C. Dávila, Mário H. Terra-Araújo, Fernanda A. Carvalho, José E. Nascimento-Junior, Fernanda
Cabral, José M. Brito and Onalto F. Menezes for the help during fieldworks. We also thank Piero Delprete and two
anonymous reviewers for their revisions and comments, which improved the manuscript.

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