Rediscovery of Utricularia cutleri Steyerm. (Lentibulariaceae) in Rio Grande do Norte, Brazil: Taxonomic Reestablishment, Geographic Distribution, and Notes on Pollen and Bladder-Trap Micromorphology

Abstract

The rediscovery of a carnivorous plant, Utricularia cutleri, in a seasonally flooded coastal plain in the Atlantic Forest domain, is here reported. This species was first described in 1952 with a few collections from that time, and since 1989 was considered a synonym of U. viscosa. Combined macro- and micromorphological evidence using SEM analysis is provided to propose its taxonomic reestablishment. Utricularia cutleri was originally known only from the type collection in Ceara ́ state, and here we report two new records from Mato Grosso and Rio Grande do Norte states, in central-western and northeastern Brazil. Updated morphological description, geographic distribution, and conservation status are provided, as well as comparative discussion with U. viscosa. Moreover, an updated identification key to species of Lentibulariaceae from Rio Grande do Norte is also presented.

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Rediscovery of Utricularia cutleri Steyerm. (Lentibulariaceae) in Rio
Grande do Norte, Brazil: Taxonomic Reestablishment, Geographic
Distribution, and Notes on Pollen and Bladder-Trap Micromorphology
Authors: Felipe Martins Guedes, Gabriel Santos Garcia, Giselle B. Araújo, Alessandra Ike
Coan, and Marccus Alves
Source: Systematic Botany, 44(3) : 708-718
Published By: The American Society of Plant Taxonomists
URL: https://doi.org/10.1600/036364419X15620114943864
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Systematic Botany (2019), 44(3): pp. 708–718
© Copyright 2019 by the American Society of Plant Taxonomists
DOI 10.1600/036364419X15620114943864
Date of publication August 6, 2019
Rediscovery of Utricularia cutleri Steyerm. (Lentibulariaceae) in Rio Grande do Norte,
Brazil: Taxonomic Reestablishment, Geographic Distribution, and Notes on Pollen and
Bladder-Trap Micromorphology
Felipe Martins Guedes,
1,4
Gabriel Santos Garcia,
2
Giselle B. Ara ´ujo,
3
Alessandra Ike Coan,
3
and Marccus Alves
1
1
Programa de P´os-Graduaç~
ao em Biologia Vegetal. Laborat´orio de Morfo-Taxonomia Vegetal, Departamento de Botˆanica,
Centro de Biociˆencias, Universidade Federal de Pernambuco, Avenida Professor Moraes Rego, 1235 - Cidade Universit´aria,
CEP 50670-901, Recife, PE, Brazil
2
Laborat´orio de Botˆanica Sistem´atica, Departamento de Botˆanica e Zoologia, Universidade Federal do Rio Grande do Norte,
Natal, RN, Brazil
3
Programa de P´os-Graduaç~
ao em Ciˆencias Biol´ogicas (Biologia Vegetal), Instituto de Biociˆencias de Rio Claro, Departamento
de Botˆanica, Universidade Estadual Paulista J ´ulio de Mesquita Filho, Avenida 24-A, 1515 - Bela Vista, CEP 13506-900,
Rio Claro, SP, Brazil
4
Author for correspondence (felipehmartins09@gmail.com)
Communicating Editor: Timothy M. Evans
Abstract—The rediscovery of a carnivorous plant, Utricularia cutleri, in a seasonally flooded coastal plain in the Atlantic Forest domain, is here
reported. This species was first described in 1952 with a few collections from that time, and since 1989 was considered a synonym of U. viscosa.
Combined macro- and micromorphological evidence using SEM analysis is provided to propose its taxonomic reestablishment. Utricularia cutleri
was originally known only from the type collection in Cear ´a state, and here we report two new records from Mato Grosso and Rio Grande do Norte
states, in central-western and northeastern Brazil. Updated morphological description, geographic distribution, and conservation status are
provided, as well as comparative discussion with U. viscosa. Moreover, an updated identification key to species of Lentibulariaceae from Rio Grande
do Norte is also presented.
Keywords—Atlantic Forest, carnivorous plants, pioneer formations, synonym, taxonomy.
The carnivorous genus Utricularia L. is the largest within the
family Lentibulariaceae, comprising about 230 rootless and
herbaceous species capable of colonizing different types of wet
habitats (Jobson et al. 2018). It is also the most diverse in regard
to life and growth forms, such as suspended aquatics (hy-
drophytes), terrestrial, amphibians (helophytes), epiphytes,
rheophytes, and lithophytes (Ellenberg and Mueller-Dombois
1967; Taylor 1989; Cook 1996). Utricularia species are ver-
nacularly known as bladderworts because of their tiny,
bladder-shaped traps, which are modified leaves, active in
prey capture. They suck in microscopic animals, with excep-
tion of the passive traps of U. multifida R.Br. (U. subgen.
Polypompholyx), and secrete hydrolytic enzymes, which digest
them and absorb their nutrients (Lloyd 1935; Adamec et al.
2010; Poppinga et al. 2015; Westermeier et al. 2017).
Trichomes are key features in the bladders’mechanism,
playing a significant role in prey capture (Adamec 2011). There
are three main functional types present in different portions of
the traps. The trigger trichomes are located just at the trap
doorway and are sensitive, responsible for prey detection,
triggering the suction process. The bifid (two-armed) tri-
chomes are located on the interior side of the threshold and
play a role in transporting water out of the trap after the
suctioning process. And finally, the quadrifid (four-armed)
trichomes cover the entire inner surface of the traps and
are involved in enzyme secretion and nutrient absorption
(Reifenrath et al. 2006).
The infrageneric classification proposed by Taylor (1989),
based mainly on morphology of traps and reproductive
characters, is largely accepted and most of its sections are
supported by phylogenetic studies, albeit some incongruences
still need resolution (Jobson and Albert 2002; Jobson et al. 2003;
M¨uller and Borsch 2005; Reut and Jobson 2010; Rodrigues et al.
2017; Jobson et al. 2017, 2018; Silva et al. 2018). South America
is the diversity centre of Utricularia, with dispersion routes to
North America, Africa, Eurasia, and Australia (Jobson et al.
2003; Silva et al. 2018). Of the 80 South American species, 52 are
endemic, and of the 64 found in Brazil, 16 are endemic (Taylor
1989; Miranda et al. 2018; Silva et al. 2018).
The greatest diversity concentrates in lowland seasonally
flooded sandy areas, such as coastal plains (restingas and
pioneer formation areas) and Amazonian campinaranas, in
highland Brazilian fields, such as campos rupestres and
campos de altitude, and in highland white-sand savannas,
such as the Guyana Shield tepuis (Cheek and Taylor 1995;
Miranda and Absy 2000; Fromm-Trinta 2004; Silva et al. 2011;
Costa et al. 2016; Guedes et al. 2018).
About 60% of the Utricularia found in Brazil occurs in the
northeastern region, and of those, five are endemic (Miranda
et al. 2018); therefore, it is a remarkable diversity centre. In this
region are inserted four of the five Centres of Endemism of the
Atlantic Forest, and one of them is the Pernambuco Centre of
Endemism, which comprises the coastal forests that extend
from Rio Grande do Norte to Alagoas, a critically threatened
area (Silva and Casteleti 2005). It is considered a hotspot within
one of the most important hotspots due to its five vegetation
types and its great biological diversity, with high endemism
values (Silva and Casteleti 2005; Tabarelli et al. 2005). Yet,
Guedes et al. (2018) highlighted that northeastern Brazil
consists of an area still not well botanically known, and until
recently, very little knowledge was available about the real
diversity of Lentibulariaceae, since floristic surveys often ig-
nore the herbaceous stratum.
During fieldwork carried out in an area of pioneer formation
phytophysiognomy (Atlantic Forest domain) in Rio Grande do
Norte state, specimens of U. viscosa Spruce ex Oliv. were
collected as well as specimens that slightly resemble U. viscosa
with regard to their sticky scape and vegetative morphology,
but with notably different flowers. Our data evidences the
existence of substantial differences between them. Herein we
report two new records and provide an updated taxonomic
treatment, geographic distribution, illustration, photographs
708
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of living specimens, and a key to all Lentibulariaceae species in
Rio Grande do Norte. In addition to that we assessed its
conservation status and analysed its pollen grains and
bladder-trap structure using scanning electron microscope
(SEM) analysis.
Materials and Methods
Intensive fieldwork was undertaken by the first two authors between
2015 and 2018 in northeastern Brazil. The morphological description of the
species is based on dried and living specimens collected in Rio Grande do
Norte state and personal examination of dried specimens from Cear ´aand
Mato Grosso deposited at the K, R, RB, and UFRN herbaria. Description
and morphological characters follow Harris and Harris (2001), except for
those characters specific to Utricularia, which are according to Taylor
(1989). The identification key is based on specimens from Rio Grande do
Norte available at K, R, RB, UFP, and UFRN herbaria (acronyms according
to Thiers 2018).
Using scanning electron microscope (SEM) analysis, micromorpho-
logical evidence in pollen grains and bladder-trap structure was observed.
Fixed mature anthers and traps were used from each specimen of U. cutleri
(F.M. Guedes 58 and G.S. Garcia - UFP and U. viscosa (F.M. Guedes 101 and
110 - UFP), from the known populations in the state of Rio Grande do
Norte. Four specimens (eight anthers and eight traps) of each species were
analysed. The samples were carefully dissected in 70% ethanol, then
dehydrated through an ethanol series, critical-point dried (Bal-Tec CPD
030), and coated with gold (Bal-Tec SCD 050). SEM observations were
made using a Hitachi TM3000 microscope. The general pollen terminology
follows Punt et al. (2007).
The distribution map (Fig. 1) was prepared using software QGIS 2.18
(available at http://qgis.org/en/site/), based on spatial cartographic data
available at the Brazilian Institute of Geography and Statistics (IBGE)
website (http://www.ibge.gov.br), herbaria vouchers carefully checked,
and our own field observations. The conservation status for this species
was assessed according to the IUCN Red List criteria (IUCN 2017). The
vegetation characterization was based on IBGE (2012). The illustration
(Fig. 2) was made by the first author.
Results and Discussion
UTRICULARIA CUTLERI Steyerm., Bull. Torrey Bot. Club 79: 311.
1952. TYPE:BRAZIL, Cear ´a: Caucaia, 4 km north of Soure
(Caucaia), 10 June 1945, H.C. Cutler 8363 (holotype: F
photo!; isotype: MO photo!).
Terrestrial (helophyte) annual herb, 1–25 cm tall. Stolons ca.
0.2 mm thick, hispid. Rhizoids with papillose branches.
Leaves 6–10 30.1 mm, cylindrical, simple. Traps ca. 1 mm
long, stalked, ovoid, covered with scattered long, uniseriate,
glandular trichomes, doorway lateral, without external ap-
pendages. Inflorescence erect, simple, lax, single to 10-flowered;
scape 0.3–0.5 mm diam, green, sparsely hispid at the base,
viscid glandular above. Scales and bracts 1–1.3 30.4–0.5 mm,
subpeltate, margins irregularly denticulate, viscid glandular,
upper part ovate with apex acuminate, lower part ovate-
deltoid to quadrate with apex truncate or 2–3-fid. Bracteoles
absent. Pedicels 2–15 mm long, cylindrical, ascending, viscid
glandular. Sepals ovate, margins entire, viscid glandular,
conspicuously nerved; upper sepal 1.5–231–1.5 mm,
apex acute to acuminate, obscurely to distinctly 3-denticulate;
lower sepal 1.2–1.8 31–1.5 mm, apex emarginate. Corolla 8–12
Fig. 1. Distribution map of Utricularia cutleri Steyerm. and U. viscosa Spruce ex Oliv. based on checked herbaria vouchers.
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Fig. 2. Utricularia cutleri Steyerm. A. Habit. B. Base of scape with stolons. C. Trap. D. Bract. E. Flower in lateral view. F. Calyx in dorsal view. G. Corolla in
frontal view. H. Stamen. I. Pistil. J. Capsule. K. Seed. Drawn by F. M. Guedes from the type specimen.
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mm long, pale lilac with a yellow palate and a purple blotch at
the base of the upper lip; upper lip 5–632.5–3.5 mm, entire,
triangular, margins strongly reflexed, apex emarginate; lower
lip 4–534–5 mm, quadrate in outline, plan, irregularly crenate,
with a gibbous papillose palate; spur 5.5–6mmlong,narrowly
conical, straight, apex acute. Stamens ca. 1 mm long, filaments
straight, with an extrorse lateral projection, anther thecae dis-
tinct. Pollen grains oblate, 11–13-colporate, ends of colpi
anastomosed. Ovary 1–1.2 30.5–0.6 mm, globose, upper stigma
lip obsolete, lower stigma lip ovate, apex retuse. Capsule
1.5–2 mm diam, globose, lead-coloured, dehiscence longitudi-
nal. Seeds ca. 0.3 mm diam, globose, testal cells isodiametric, ca.
60 mm wide, periclinal wall smooth, anticlinal walls straight and
raised. Figures 2–3.
Specimens Examined—Brazil.—CEAR ´
A: s.l., s.d., F.F.A. Cysneiros 917b
(R!).—MATO GROSSO: Nova Xavantina, Barra dos Garças-Xavantina road,
Fig. 3. Utricularia sect. Sprucea.A–D, J. U. cutleri Steyerm. E–I. U. viscosa Spruce ex Oliv. K. Corolla of U. cutleri on the left and two corollas of U. viscosa
on the right.
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10 km South of Xavantina, 07 Jun 1966, D.R. Hunt 5849 (K!); ibidem, May
1949, D.R.H. Sickl 455 and 456 (RB!).—RIO GRANDE do NORTE: Maxar-
anguape, baixada interdunar pr ´ox. `a Maracaja ´u (5°44022”S, 35°320180W),
13 Oct 2015, G.S. Garcia 67 (UFRN!); ibidem, 03 Oct 2017, F.M. Guedes 58 and
G.S. Garcia (UFP!); N´
ısia Floresta, Lagoa de Alcaçuz, 5°59’59”S, 35°090060
W), 28 Nov 2018, G.S. Garcia 615 (UFRN!).
Distribution and Habitat—Utricularia cutleri is endemic to
Brazil and originally known from the coastline of Cear´a, in
northeastern Brazil (Fig. 1). The type locality is a seasonally
flooded coastal plain, in Caucaia municipality, with edaphic
vegetation (pioneer formation) and fluvial influence, with
abundance of Copernicia prunifera (Mill.) H.E.Moore, a vege-
tation also known as Carnaubais, under the Caatinga phy-
togeographic domain (IBGE 2012; Moro et al. 2015). The area is
largely sampled and yet no other material is available from
Cear´a apart from the type specimens and a collection of Freire
Alem~
ao Cysneiros without specific locality, but certainly from
1861 based on the label of other specimens collected by him
(Alem~
ao 2006, 2007; Guedes and Matias in press).
In Rio Grande do Norte the habitat shares edaphic simi-
larities with the type locality, also a pioneer formation in
coastal plains, however, in more open herbaceous-shrubby
vegetation within the Atlantic Forest domain (IBGE 2012).
Two populations were recorded, one in the southeast coast of
the state, near Alcaçuz village in N´
ısia Floresta municipality,
and another at the northeast coast, near Maracaja ´u village in
Maxaranguape municipality. Although a nearby population of
its closer species U. viscosa is reported to Maxaranguape (about
only 10 km apart), no sympatric occurrence was observed. It
grows on sandy quartzitic soil as emergent, sympatric with
Xyris spp., Acisanthera bivalvis (Aubl.) Cogn., Helanthium ten-
ellum (Mart. ex Schult.f.) J.G.Sm., and other species of Lenti-
bulariaceae, mainly U. cornuta Michx., U. subulata L., and
U. resupinata B.D. Greene ex Bigelow. Both areas are in-
tensively used for tourist purposes including lagoon bathing
and crossing vehicles.
A few specimens collected in Nova Xavantina, Mato Grosso
state, although with much longer inflorescences (25 cm tall vs.
up to 3 cm tall in RN), also match in floral morphology, thus
constituting another highly isolated population of U. cutleri.
The reported habitat comprises a grassy-woody savannah in a
swampy valley, known as campos limpos of the Cerrado
domain (Ratter et al. 1973; IBGE 2012).
Phenology—Collected in flower and fruit in May in the
central-western region, and between June and October in the
northeastern region, during the dry season.
Etymology—The epithet ‘cutleri’is named after the Amer-
ican botanist Hugh C. Cutler, who collected the type specimen
in 1945.
Notes—A careful examination of the specimens collected in
Rio Grande do Norte led us to conclude that they correspond
to Utricularia cutleri Steyerm. This species was described in
1952 based on a collection of Hugh Carson Cutler (H.C. Cutler
8363) in Cear´a state. Later, it was synonymized to U. viscosa by
Taylor (1989) and accepted as synonym by Fromm-Trinta (1989,
1991). We also examined many herbaria vouchers and
detected a few other specimens of U. cutleri among U. viscosa
Table 1. Comparative diagnostic characters between U. cutleri and U. viscosa, including distribution range.
U. cutleri Steyerm. U. viscosa Spruce ex Oliv.
Trigger trichomes Four Three
Quadrifid trichomes Arms cylindrical, ca. 105 mm long,
7–8mm thick, apices acute, cuticle
smooth to finely striate
Arms flattened dorsiventrally, ca. 85
mm long, 10–13 mm thick, apices
obtuse, cuticle roughly striate
Scape 0.3–0.5 mm diam 0.7–1 mm diam
Bracts and scales Margins irregularly denticulate Margins entire
Upper sepal apex Acute to acuminate, obscurely to
distinctly 3-denticulate
Acute to acuminate
Corolla size 8–12 mm long 6–7 mm long
Upper corolla lip 5–5.5 32.5–3.5 mm, triangular,
margins strongly reflexed, apex
emarginate
ca. 2.5 32 mm, ovate, margins plan,
apex rounded or retuse
Lower corolla lip 4–4.5 34–4.5 mm, irregularly
crenate
ca. 1.5 32.3 mm, truncate or
obscurely 3-crenate
Spur 5.5–6 mm long, narrowly conical,
apex acute
ca. 4 mm long, narrowly cylindrical,
apex obtuse
Stigma Upper stigma lip obsolete; lower
stigma lip ovate, apex retuse
Upper stigma lip deltoid; lower
stigma lip semicircular, apex
rounded
Stamens Filaments with extrorse lateral
projections
Filaments with no lateral projection
Pollen grains Oblate; 11–13 colporate;
anastomosing colpori present;
fossulate apocolpia; psilate
tectum; thickened mesocolpia
present
Oblate spheroidal; 9–11 colporate;
colpori not anastomosing; regular
apocolpia; regulate tectum;
thickened mesocolpia absent
Distribution range (based on
checked herbaria vouchers)
Brazil (Cear´a, Mato Grosso and
Rio Grande do Norte)
Belize, Nicaragua, Trinidad and
Tobago, Venezuela, Guyana,
Suriname, French Guyana and
Brazil (Amazonas, Par´a, Rio Grande
do Norte and Roraima)
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identifications, with the latest collection from 1966. Macro- and
micromorphological distinctive characters were observed,
which justify it as a distinct taxon at species rank (Table 1).
Utricularia cutleri belongs to U. subgen. Utricularia sect.
Sprucea, as can be seen from its traps with no external ap-
pendages and covered with long, uniseriate trichomes, viscid
glandular scape, pedicels, and sepals, violet corolla, globose
seeds with smooth isodiametric testal cells, and 11–13-colporate
pollen (Taylor 1989).
An isotype of U. cutleri in GH herbarium (GH 93385) and
four isotypes of U. viscosa not previously reported in the latest
taxonomic revision (Taylor 1989) were also located: Brazil,
Par´a, Santarem, R. Spruce 1042 (E 259142 photo!, E 259143
photo!, GH 993392 photo! and M 185879 photo!).
SEM Analysis—The traps of U. cutleri and U. viscosa are
ovoid and lack external appendages (Fig. 4A, B), which is also
observed in a few other sections, such as U. sect. Stomoisia, U.
sect. Benjaminia, and U. sect. Stylotheca (Taylor 1989). The
doorway is positioned laterally (Fig. 4C, D), with a dorsal
projection only in U. cutleri. The outer surfaces of the traps are
formed by rectangular to fusiform cells with a convex outer
periclinal wall, covered by a rugose cuticle (Fig. 4E, F).
Trichomes (Fig. 4A–F: arrowheads) are long and uniseriate in
both species (during the process of dehydration and coating
Fig. 4. SEM micrographs of traps of Utricularia cutleri Steyerm. (A, C, E) and U. viscosa Spruce ex Oliv. (B, D, F). A, B. Lateral views. C, D. Ventral views.
E, F. Details of the outer surface. Arrowheads 5outer surface trichomes. Scale bars: A–D5250 mm; E, F 550 mm.
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Fig. 5. SEM micrographs of traps of Utricularia cutleri Steyerm. (A, C, E, G, H) and U. viscosa Spruce ex Oliv. (B, D, F, I, J). A, B. Doorway. C, D. Details of
glandular trichomes at the doorway. E, F. Details of trigger hairs. G–J. Details of quadrifid hairs. Asterisk 5two-armed trichomes; lt 5long-stalked
glandular trichomes; st 5short-stalked glandular trichomes; tt 5trigger trichomes. Scale bars: A, B 5150 mm; C, D 550 mm; E, F 525 mm; G, I 540 mm;
H530 mm; J 515 mm.
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in gold most of them break). As morphology of the external
glands has yet proven useful for species distinction (Yang
etal.2009),itsupportsU. sect. Sprucea now comprising two
species.
In all traps sampled of both species, the doorway is orna-
mented with two distinct types of trichomes: glandular and
trigger trichomes (Fig. 5A, B). The glandular trichomes are
short or long-stalked globose (Fig. 5A, B). In U. cutleri the
short-stalked trichomes, with ca. 20 mm in overall length, are
regularly distributed on the entire surface of the doorway
(Fig. 5A). In U. viscosa, they are longer (ca. 25 mm) and are
sparsely distributed (Fig. 5B). In both species, the long-stalked
trichomes are restricted to one or two rows in the interior of the
trap doorway (Fig. 5C, D). In U. cutleri they have ca. 40 mmin
Fig. 6. SEM micrographs of pollen grains of Utricularia cutleri Steyerm. (A, C, E) and U. viscosa Spruce ex Oliv. (B, D, F). A, B. Groups of pollen grains
in dehiscent anthers. C, D. Pollen grains in equatorial view. E, F. Pollen grains in polar view. Arrowheads 5minute perforations. Scale bars: A, B 515 mm;
C–F55mm.
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overall length, being much longer in U. viscosa, which can
reach ca. 90 mm long.
The trigger trichomes are located near the midbasal region
of the trap door and there are four in U. cutleri (Fig. 5E) and
three in U. viscosa (Fig. 5F). Small two-armed trichomes are
arranged close to them (Fig. 5E, F: asterisks).
Quadrifid trichomes are distributed over the entire inner
surface of the traps (Fig. 5G–J). Their four arms are oriented
parallel to the trap inner surface. In U. cutleri (Fig. 5G, H),
they are ca. 105 mm long with cylindrical arms (7–8mmthick)
and acute apices, one pair diverging at about 30° and the
other one at about 50°, and the cuticle is smooth to finely
striate. In U. viscosa (Fig. 5I, J), they are ca. 85 mmlongwith
flattened dorsiventrally arms (10–13 mmthick)andobtuse
apices, both pairs diverging at 41–58°, and the cuticle is
roughly striate.
Among other diagnostic micromorphological features in the
delimitation of U. cutleri, the occurrence of four trigger hairs in
the trap doorway is remarkable and consistent in all traps
sampled (Table 1). The morphology of the quadrifids, al-
though widely used in the characterization of Utricularia
(Taylor 1989), must be carefully considered for both species.
Results show differences in U. viscosa when compared to
Taylor (1989) which reinforces that morphological variation in
the quadrifid trichomes can occur in the same species.
Pollen grains of U. cutleri are oblate (Fig. 6A), while those of
U. viscosa are oblate spheroidal (Fig. 6B). In both species the
grains are radially symmetric and zonocolporate (Fig. 6C–F);
the number of colpori varies from 11–13 in U. cutleri and from
9–11 in U. viscosa. The profile of the colpus margin is regular
and the colpus membrane is smooth (Fig. 6B–F); anastomosing
colpori are common near the polar region only in grains of
U. cutleri (Fig. 6A, C, E). The polar regions (apocolpia) are
similar in size in both species, being fossulate in U. cutleri
(Fig. 6C, E) and regular in U. viscosa (Fig. 6D, F). In the latter
species, minute perforations are rare and restricted to the polar
region (Fig. 6B: arrowheads). The ornamentation of the tectum
is psilate with sporadic minute perforations in U. cutleri
(Fig. 6A, C, E: arrowheads) and rugulate in U. viscosa (Fig. 6D,
F). The equatorial regions (mesocolpia) are thickened only in
U. cutleri (Fig. 6A, C).
Micromorphological studies with pollen grains of Lenti-
bulariaceae have already been highlighted as important in
species delimitation (Erdtman 1952; Huynh 1968; Fromm-
Trinta 1979, 1981; Lobreau-Callen et al. 1999; Rodondi et al.
2010; Beretta et al. 2014; Cruz et al. 2018). Palynological fea-
tures, especially those related to shape, aperture, and
endoaperture were recently used by Cruz et al. (2018) in the
characterization of Lentibulariaceae species from Western
Cuba; for the seven species of Utricularia sampled, the authors
categorize three pollen types. In the present study, palyno-
logical characters provide additional diagnostic evidence for
the new species as presented in Table 1.
Conservation Status—According to the IUCN (2017) Red
List criteria, U. cutleri may be treated as Endangered (EN)
[B2a,c(i,ii)] due to its highly fragmented geographical distri-
bution and consistent loss of habitat quality. The type locality
is severely impacted by deforestation and urban development
(Zuquette et al. 2004; Antongiovanni et al. 2018), and besides, it
remains unknown whether there are any remnant populations
since the last collection more than 60 yr ago. Comparisons of
occupancy areas of U. cutleri in Rio Grande do Norte suggests
there may still exist suitable habitats for the species in nearby
locations.
Loss of suitable area to agricultural fields may have affected
the population recorded from Nova Xavantina, since mono-
culture fields have quickly expanded over the last 30 yr in vast
landscapes throughout the entire Cerrado domain (Jepson
2005). As the extent of both original and current distribution of
U. cutleri in the area is unknown, we assume some vegetation
fragments can hold the species. A possible area is the Parque
Municipal M´ario Viana (Pires et al. 2016) which fairly matches
the locality description for the last collected specimens (in
1966), and this also suggests it may occur within a protected
area; however, field investigations are necessary to confirm,
since no available material is geo-referenced. Considering
pollution and waste accumulation to be a major threat to the
genus (Jennings and Rohr 2011), the population is subjected to
all possible impacts related to coexistence with nearby agri-
cultural fields, such as accumulation of pesticide and herbicide
wastes, already linked to some human health issues in the area
(Oliveira et al. 2014).
Despite over a century environmental degradation (Ribeiro
et al. 2009), the species populations recorded for the two lo-
calities in Rio Grande do Norte lie between the best conserved
habitats known for the species, with one of them included
within an established conservation unit ( ´
Area de Proteç~
ao
Ambiental Bonfim-Guara´
ıras). Both localities are subject to
similar human pressures, located near small, touristy, very
active villages (Urano et al. 2015). The individuals in both
areas are centred within less than a kilometre radius, in
seasonal shallow lagoons. The major threats faced by
U. cutleri at both localities seem to be unmanaged activity of
off-road and quadricycle vehicles in the species’inhabited
areas, especially during early summer when water level
retreats, as reported for aquatic macrophytes as well (Leroy
2015). The resultant loss of individuals may affect the
maintenance of the population in a way that is still
unevaluated.
Thus, three of all four confirmed localities are not under any
protection effort and are located alongside state highways,
liable to suffer future deforestation and habitat loss. No other
population or subpopulation could be found in surrounding
areas nor in other pioneer formation areas of northeastern
Brazil despite intensive fieldwork carried out between 2015
and 2018.
KEY to ALL LENTIBULARIACEAE SPECIES in RIO GRANDE do NORTE,BRAZIL
1. Calyx with 5 sepals (Genlisea)...........................................................................................G. filiformis
1. Calyx with 2 sepals (Utricularia)..................................................................................................2
2. Suspended aquatics (hydrophytes); capillary, dichotomously branched leaves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3. Presence of a whorl of fusiform floats at the base of the scape; lilac or white corolla, botuliform spur, 2–3timeslongerthanthelowerlip.....
.............................................................................................................U. benjaminiana
3. Absence of floats; yellow or rose pink corolla; conical spur, shorter than or as long as the lower lip . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
4. Rose pink corolla with a yellow palate; presence of a cleistogamous flower at the base of the scape . . . . . ..................U. hydrocarpa
4. Yellow corolla; only chasmogamous flowers . . . . . . . . . . . . .....................................................................5
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5. Inflated scape; bilobate lower corolla lip; pedicel deflexed in fruit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. foliosa
5. Slender scape; obscurely trilobate lower corolla lip; pedicel ascending in fruit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. gibba
2. Terrestrial or amphibians (helophytes); laminar or cylindrical leaves, simple or pinnately branched . . . ...................................6
6. Tubular bracts; resupinate lower corolla lip . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. resupinata
6. Bracts not tubular; lower corolla lip not resupinate . . ...........................................................................7
7. Peltate or subpeltate bracts . . .............................................................................................8
8. Subpeltate bracts; sticky, glandular scape; lilac or pale lilac corolla, quadrate lower lip . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
9. Corolla 6–7 mm long, ovate upper corolla lip margins not reflexed, spur twice as long as the lower lip ...................U. viscosa
9. Corolla 8–12 mm long, triangular upper corolla lip with strongly reflexed margins, spur slightly longer than the lower lip ...........
............................................................................................................U. cutleri
8. Peltate bracts; glabrous scape; yellow corolla, trilobate lower lip .............................................................10
10. Presence of sterile bracts on the raceme axis; spur twice as long as the lower lip . . ....................................U. pusilla
10. Absence of sterile bracts on the raceme axis; spur as long as or slightly longer than the lower lip .............................11
11. Pinnately branched leaves; inconspicuously nerved sepals . . . . . . ............................................U. trichophylla
11. Simple leaves; conspicuously nerved sepals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
12. Sepals with prominent nerves converging at the apex; scarcely trilobate lower corolla lip ........................U. triloba
12. Sepals with no prominent nerves reaching the apex; deeply trilobate lower corolla lip .........................U. subulata
7. Basifixedbracts........................................................................................................13
13. Fimbriate or laciniate-denticulate scales, bracts, and bracteoles . . ...........................................................14
14. Fimbriate, auriculate scales and bracts; deeply fimbriate sepals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. simulans
14. Laciniate-denticulate, not auriculate scales and bracts; erose sepals ................................................U. hispida
13. Entire scales, bracts, and bracteoles ....................................................................................15
15. Obsolete, saccate spur . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. guyanensis
15. Conspicuous, subulate spur .......................................................................................16
16. Coriaceous sepals with involute margins, inconspicuously nerved . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. erectiflora
16. Membranous sepals margins not involute, conspicuously nerved . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........17
17. Upper sepal with not prominent nerves . . . . . . . . . . . .....................................................U. adpressa
17. Upper sepal with prominent ridged nerves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...............................18
18. Lower sepal larger than the upper sepal; upper corolla lip narrowly oblong .................................U. nana
18. Lower sepal smaller than the upper sepal; upper corolla lip broadly obovate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
19. Corolla 0.2–1.5 cm long; lax inflorescence, scape 0.4–1mmdiam......................................U. juncea
19. Corolla 1.5–2 cm long; congested inflorescence, scape 0.5–1.5mmdiam...............................U. cornuta
Acknowledgments
First, we are grateful and fully in debt to the reviewers of the previous
version of the manuscript, especially to Richard W. Jobson for kindly
suggested a major change of approach on it. We also thank the curators of
K, R, RB, UFP, and UFRN herbaria for providing access to Lentibulariaceae
specimens for this study. This study was financed by the Coordenaç~
ao de
Aperfeiçoamento de Pessoal de N´
ıvel Superior –Brasil (CAPES) –Finance
Code 001. Thanks also to the Postgraduate Program in Plant Biology, CCB/
UFPE, for granting logistic and laboratory support.
Author Contributions
Felipe Guedes, Gabriel Garcia, and Marccus Alves conceived and
conducted the research described in this manuscript, including field trips,
photographs, and herbarium visits. Felipe Guedes was the primary author
of the taxonomic treatment which is part of his Master’s dissertation under
supervision of Marccus Alves. Giselle Ara ´ujo and Alessandra Coan per-
formed the dissection of anthers and traps for SEM analysis and con-
tributed with anatomical expertise for the topic “SEM Analysis”of the
manuscript.
LITERATURE CITED
Adamec, L. 2011. Functional characteristics of traps of aquatic carnivorous
Utricularia species. Aquatic Botany 95: 226–233.
Adamec, L., D. Sirov´a, J. Vrba, and E. Rejm ´ankov´a. 2010. Enzyme pro-
duction in the traps of aquatic Utricularia species. Biologia 65: 273–278.
Alem~
ao, F. F. 2006. Di´ario de Viagem de Francisco Freire Alem~
ao: Fortaleza –
Crato, 1859, vol. 1 (Coleç~
ao Comiss~
ao Cient´
ıfica de Exploraç~
ao, 3).
Fortaleza: Museu do Cear ´a, Secretaria de Cultura do Estado do Cear ´a.
Alem~
ao,F.F.2007.Di´ario de Viagem de Francisco Freire Alem~
ao: Crato –Rio de
Janeiro, 1859 / 1860,vol.2(Coleç
~
ao Comiss~
ao Cient´
ıfica de Exploraç~
ao, 4).
Fortaleza: Museu do Cear´a, Secretaria de Cultura do Estado do Cear´a.
Antongiovanni, M., E. M. Venticinque, and C. R. Fonseca. 2018. Frag-
mentation patterns of the Caatinga drylands. Landscape Ecology 33:
1353–1367.
Beretta, M., G. Rodondi, L. Adamec, and C. Andreis. 2014. Pollen mor-
phology of European bladderworts (Utricularia L., Lentibulariaceae).
Review of Palaeobotany and Palynology 205: 22–30.
Cheek, M. and P. Taylor. 1995. Lentibulariaceae. Pp. 395–406 in Flora of the
Pico das Almas, Chapada Diamantina, Bahia, Brazil, ed. B. Stannard.
London: Royal Botanic Garden, Kew.
Cook, C. D. K. 1996. Aquatic Plant Book. Amsterdam: SPB Academic
Publishing.
Costa, S. M., V. Bittrich, and M. C. E. Amaral. 2016. Lentibulariaceae from
the Viru´a National Park in the northern Amazon, Roraima, Brazil.
Phytotaxa 258: 1–25.
Cruz, D., Y. Dominguez, C. M. P. Vald´es, V. F. O. Miranda, and
E. C. Gasparino. 2018. Pollen morphology of selected species of
Lentibulariaceae Rich. from Western Cuba based on light microscopy
and its taxonomic implications. Phytotaxa 350: 187–200.
Ellenberg, H. and D. Mueller-Dombois. 1967. A key to Raunkiaer plant life
forms with revised subdivisions. Bericht ¨uber das Geobotanisches Institut
Eidgen¨ossische Technische Hochschule Z ¨urich.Stiftung R¨ubel 37: 56–73.
Erdtman, G. 1952. Pollen Morphology and Plant Taxonomy. Angiosperms.
Stockholm: Almqvist and Wiksell.
Fromm-Trinta, E. 1979. Revis~
ao das esp´ecies do g ˆenero Genlisea A.St.-Hil.
(Lentibulariaceae) das regi~
oes sudeste e sul do Brasil. Rodrigu´esia 31:
17–139.
Fromm-Trinta, E. 1981. Revis~
ao do gˆenero Genlisea A.St.-Hil (Lentibular-
iaceae) no Brasil. Boletim do Museu Nacional Rio de Janeiro.Botanica
61: 1–20.
Fromm-Trinta, E. 1989. O gˆenero Utricularia L. no Brasil. III. Esp´ecies da
Regi~
ao Nordeste. Bradea.Boletim do Herbarium Bradeanum 5: 188–195.
Fromm-Trinta, E. 1991. Lentibulariaceae do Brasil. Utricul ´arias Aqu´aticas.
II. Esp´ecies fixas. Bradea.Boletim do Herbarium Bradeanum 6: 1–12.
Fromm-Trinta, E. 2004. Flora de Gr~
ao-Mogol, Minas Gerais: Lentibular-
iaceae. Boletim de Botˆanica da Universidade de S~
ao Paulo 22: 267–271.
Guedes, F. M. and L. Q. Matias. In press. Flora do Cear ´a, Brasil: Lenti-
bulariaceae. Rodrigu´esia (in press).
Guedes, F. M., G. S. Garcia, L. M. Versieux, L. Q. Matias, and M. Alves.
2018. Insights on underestimated Lentibulariaceae diversity in
northeastern Brazil: new records and notes on distribution, diversity
and endemism. Brazilian Journal of Botany 41: 867–887.
Harris,J.G.andM.W.Harris.2001.Plant Identification Terminology:
An Illustrated Glossary, ed. 2. Spring Lake, Utah: Spring Lake
Publishing.
Huynh, K.-L. 1968. ´
Etude de la morphologie du pollen du genre Utricularia
L. Pollen et Spores 10: 11–55.
IBGE. 2012. Manual t´ecnico da vegetaç~
ao brasileira, ed. 2. Rio de Janeiro:
Instituto Brasileiro de Biogeografia e Estat´
ıstica –IBGE.
IUCN. 2017. Guidelines for using the IUCN red list categories and criteria
version 13. Prepared by the Standards and Petitions Subcommittee.
www.iucnredlist.org/documents/RedListGuidelines.pdf. (accessed
12 March 2018).
GUEDES ET AL.: REDISCOVERY AND REESTABLISHMENT OF UTRICULARIA CUTLERI 7172019]
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 Federal de Pernambuco (UFPE)

Jepson, W. 2005. A disappearing biome? Reconsidering land-cover change
in the Brazilian savanna. The Geographical Journal 171: 99–111.
Jennings, D. E. and J. R. Rohr. 2011. A review of the conservation threats to
carnivorous plants. Biological Conservation 144: 1356–1363.
Jobson, R. W. and V. A. Albert. 2002. Molecular rates parallel di-
versification contrasts between carnivorous plant sister lineages.
Cladistics 18: 127–136.
Jobson, R. W., J. Playford, K. M. Cameron, and V. A. Albert. 2003. Mo-
lecular phylogenetics of Lentibulariaceae inferred from plastid rps16
intron and trnL-F DNA sequences: Implications for character evolu-
tion and biogeography. Systematic Botany 28: 157–171.
Jobson, R. W., P. C. Baleeiro, and M. S. Reut. 2017. Molecular phylogeny of
subgenus Polypompholyx (Utricularia; Lentibulariaceae) based on three
plastid markers: Diversification and proposal for a new section.
Australian Systematic Botany 30: 259–278.
Jobson, R. W., P. C. Baleeiro, and C. Guisande. 2018. Systematics and
evolution of Lentibulariaceae: III. Utricularia. Pp. 89–104 in Carnivo-
rous Plants: Physiology, Ecology and Evolution, eds. A. M. Ellison and
L. Adamec. Oxford: Oxford University Press.
Leroy,J. A. S. 2015.Checklistdas macr´ofitas aqu ´aticasdo Rio Grande doNorte
com esforço amostral e flor´
ıstica do grupo na APA Bonfim-Guara´
ıras.
Thesis. Natal, Brazil: Federal University of Rio Grande do Norte.
Lloyd, F. E. 1935. Utricularia. Biological Reviews of the Cambridge Philosophical
Society 10: 72–110.
Lobreau-Callen, D., J. J´er ´emie, and M. Suarez-Cervera. 1999. Morphologie
et ultrastructure du pollen dansle genre Utricularia L. (Lentibulariaceae).
Canadian Journal of Botany 77: 744–767.
Miranda, I. S. and M. L. Absy. 2000. Fisionomia das savanas de Roraima,
Brasil. Acta Amazonica 30: 423–440.
Miranda, V. F. O., C. G. Menezes, S. R. Silva, Y. C. A. D´
ıaz, and
F. Rivadavia. 2018. Lentibulariaceae in Flora do Brasil 2020 em con-
struç~
ao. Jardim Botˆanico do Rio de Janeiro. http://reflora.jbrj.gov.br/
reflora/floradobrasil/FB8575 (accessed 28 February 2018).
Moro, M. F., M. B. Macedo, M. M. de Moura-F´e, A. S. F. Castro, and
R. C. da Costa. 2015. Vegetaç~
ao, unidades fitoecol ´ogicas e diversidade
paisag´
ıstica do estado do Cear´a. Rodrigu´esia 66: A1–A10.
M¨uller, K. and T. Borsch. 2005. Phylogenetics of Utricularia (Lentibular-
iaceae) and molecular evolution of the trnK intron in a lineage with
high substitutional rates. Plant Systematics and Evolution 250: 39–67.
Oliveira, N. P., G. P. Moi, M. Atanaka-Santos, A. M. C. Silva, and
W. A. Pignati. 2014. Malformaç~
oes congˆenitas em munic´
ıpios de
grande utilizaç~
ao de agrot ´oxicos em Mato Grosso, Brasil. Ciencia &
Saude Coletiva 19: 4123–4130.
Pires, K. R. P., B. S. Marimon, T. R. S. Souza, T. C. S. Anacleto, and
G. Laforga. 2016. Percepç~
ao ambiental e caracterizaç~
ao socio-
econˆomica da comunidade do entorno do Parque Municipal do
Bacaba, Nova Xavantina (MT). Caminhos de Geografia 17: 1–15.
Poppinga, S., C. Weisskopf, A. S. Westermeier, T. Masselter, and T. Speck.
2015. Fastest predators in the plant kingdom: Functional morphology
and biomechanics of suction traps found in the largest genus of
carnivorous plants. AoB Plants 8: plv140, doi: 10.1093/aobpla/plv140.
Punt, W., P. P. Hoen, S. Blackmore, S. Nilsson, and A. Le Thomas. 2007.
Glossary of pollen and spore terminology. Review of Palaeobotany and
Palynology 143: 1–81.
Ratter, J. A., P. W. Richards, G. Argent, and D. R. Gifford. 1973. Obser-
vations on the vegetation of northeastern Mato Grosso. I. The woody
vegetation types of the Xavantina-Cachimbo expedition area. Philo-
sophical Transactions of the Royal Society of London. Series B, Biological
Sciences 226: 449–492.
Reifenrath, K., I. Theisen, J. Schnitzler, S. Porembski, and W. Barthlott.
2006. Trap architecture in carnivorous Utricularia (Lentibulariaceae).
Flora 201: 597–605.
Reut, M. S. and R. W. Jobson. 2010. A phylogenetic study of subgenus
Polypompholyx: A parallel radiation of Utricularia (Lentibulariaceae)
throughout Australasia. Australian Systematic Botany 23: 152–161.
Ribeiro, M. C., J. P. Metzger, A. C. Martensen, F. J. Ponzoni, and
M. M. Hirota. 2009. The Brazilian Atlantic Forest: How much is left,
and how is the remaining forest distributed? Implications for con-
servation. Biological Conservation 142: 1141–1153.
Rodondi, G., M. Beretta, and C. Andreis. 2010. Pollen morphology of alpine
butterworts (Pinguicula L., Lentibulariaceae). Review of Palaeobotany
and Palynology 162: 1–10.
Rodrigues, F. G., N. F. Marulanda, S. R. Silva, B. J. Płachno, L. Adamec, and
V. F. O. Miranda. 2017. Phylogeny of the ‘orchid-like’bladderworts
(gen. Utricularia sect. Orchidioides and Iperua: Lentibulariaceae) with
remarks on the stolon-tuber system. Annals of Botany 120: 709–723.
Silva, J. M. C. and C. H. M. Casteleti. 2005. Estado da biodiversidade da
Mata Atlˆantica brasileira. Pp. 43–59 in Mata Atlˆantica: Biodiversidade,
Ameaças e Perspectivas, eds. C. Galindo-Leal and I. G. C ˆamara. S~
ao
Paulo/Belo Horizonte, Brazil: Fundaç~
ao SOS Mata Atlˆantica/Con-
servaç~
ao Internacional.
Silva, N. G., R. J. V. Alves, J. F. Pereira, and F. Rivadavia. 2011. Lenti-
bulariaceae, Serra de S~
ao Jos´e, Minas Gerais, Brazil. Check List 7:
120–127.
Silva, S. R., R. Gibson, L. Adamec, Y. Dom´
ınguez, and V. F. O. Miranda.
2018. Molecular phylogeny of bladderworts: A wide approach of
Utricularia (Lentibulariaceae) species relationships based on six
plastidial and nuclear DNA sequences. Molecular Phylogenetics and
Evolution 118: 244–264.
Tabarelli, M., P. L. Pinto, J. M. C. Silva, M. M. Hirota, and L. C. Bedˆe. 2005.
Desafios e oportunidades para a conservaç~
ao da biodiversidade na
Mata Atlˆantica brasileira. Megadiversidade 1: 132–138.
Taylor, P. 1989. The Genus Utricularia: A Taxonomic Monograph,ed.1.
London: Royal Botanic Gardens, Kew.
Thiers, B. 2018 [continuously updated]. Index Herbariorum: A global di-
rectory of public herbaria and associated staff. New York Botanical
Garden’s Virtual Herbarium. http://sweetgum.nybg.org/science/
ih/ (last accessed March 2018).
Urano, D. G., A. Cochand, S. L. Figueiredo, W. R. M. N´obrega, and
K. E. Sonaglio. 2015. Turismo e desenvolvimento em comunidades
litorˆaneas no Nordeste Brasileiro: Os casos de Canoa Quebrada, CE e
Maracaja ´u, RN. Revista Rosa dos Ventos 7: 574–590.
Westermeier, A. S., A. Fleischmann, K. M ¨uller, B. Sch ¨aferhoff, C. Rubach,
T. Speck, and S. Poppinga. 2017. Trap diversity and character evo-
lution in carnivorous bladderworts (Utricularia, Lentibulariaceae).
Scientific Reports 7: 12052, doi: 10.1038/s41598-017-12324-4.
Yang, Y.-P., H.-L. Liu, and Y.-S. Chao. 2009. Trap gland morphology and its
systematic implications in Taiwan Utricularia (Lentibulariaceae). Flora
204: 692–699.
Zuquette,L.V.,O.J.Pejon,andJ.Q.S.Collares.2004.Landdegradation
assessment based on environmental geoindicators in the Fortaleza met-
ropolitan region, state of Cear´a, Brazil. Environmental Geology 45: 408–425.
SYSTEMATIC BOTANY [Volume 44718
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