# Monograph of tribe Sipaneeae (Rubiaceae, Ixoroideae). A Neotropical group with its center of diversity on the Guiana Shield

Piero G. Delprete

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Piero G. Delprete. Monograph of tribe Sipaneeae (Rubiaceae, Ixoroideae). A Neotropical group with its center of diversity on the Guiana Shield. Webbia: Journal of Plant Taxonomy and Geography, 77 (1), pp.1-284, 2022, 10.3625/jopt-13963. hal-03869429

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WEBBIA

Journal of Plant
Taxonomy and Geography

2022
Vol. 77 - n. 1 Suppl.

Piero G. Delprete

Monograph of tribe Sipaneeae
(Rubiaceae, Ixoroideae). A Neotropical
group with its center of diversity on the
Guiana Shield

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<figure><img src="image_3.png" /></figure>

FIRENZE
UNIVERSITY
PRESS
**Journal of Plant Taxonomy and Geography (Webbia)** is a peer-reviewed journal on Plant Taxonomy, Nomenclature, Phylogeny, Phytogeography and Palaeobotany of the Vascular Plants.

The journal aims to allow research in botanical topics such as taxonomy, systematics, nomenclature, molecular phylogeny, conservation, biogeography, and history of botany, and botanical collections.

It was founded in 1905 in Florence by **Ugolino Martelli** (1860-1934), a botanist well known for his studies of and contributions to the systematics of the tropical genus *Pandanus* and on the Flora of Sardinia.

In the 19th century Florence represented one of the most important European centres in Plant Taxonomy and Phytogeography with several notable Italian botanists worth mentioning such as Filippo Parlatore, Teodoro Caruel, Eugenio Baroni, Stefano Sommier, Odoardo Beccari and Ugolino Martelli himself. In 1842 **Filippo Parlatore** (1817-1877) founded in Florence the *Herbarium Centrale Italicum (FI)*, which soon became one of the most important herbaria in the world. Most of the specimens described and/or cited in *Webbia* are still kept in it.

In 1905, and as a consequence of this multitude of activities in Plant Systematics and Phytogeography, Ugolino Martelli established the journal *Webbia-Raccolta di Scritti Botanici*, firstly published annually in a single issue, and later twice a year. Webbia also began to be a place of publication of contributions from Tropical Botany, especially after the Royal Colonial Herbarium founded in 1904 in Rome was moved to Florence in 1914, currently named Tropical Herbarium Study Center (Centro Studi Erbario Tropicale - Herbarium FT) belonging to the Department of Biology of the University of Florence.

*Webbia* had been created in honor of **Philip Barker Webb** (1793-1845), a close friend of Filippo Parlatore, who before passing away entrusted his personal herbarium and a library rich of old botanical books and publications to the then Botanical Museum in Florence.

**EDITOR IN CHIEF**

Riccardo M. Baldini (Italy)

**MANAGING EDITOR**

Lia Pignotti (Italy)

**ASSOCIATE EDITORS**

*Carlos Aedo*, Researcher – Real Jardín Botánico, Consejo Superior de Investigaciones Científicas, Madrid, Spain

*Freek T. Bakker*, Professor – Biosystematics Group, Wageningen University, Wageningen, The Netherlands

*Henk J. Beentje*, Honorary Research Associate – Royal Botanic Gardens, Kew, Surrey, United Kingdom

*Peter C. Boyce*, Researcher – Dipartimento di Biologia, Centro Studi Erbario Tropicale (Herbarium FT), Università di Firenze, Firenze, Italy

*Marcos A. Caraballo-Ortiz* – Department of Botany, Smithsonian National Museum of Natural History, Washington DC, USA

*Lynn G. Clark*, Professor – Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, USA

*Giovanni Cristofolini*, Professor – Orto Botanico ed Erbario, Sistema Museale di Ateneo, Università di Bologna, Bologna, Italy

*Thomas F. Daniel*, Researcher – Department of Botany, California Academy of Sciences, San Francisco, CA, USA

*Douglas Daly*, Researcher – New York Botanical Garden, The Bronx, New York, USA

*Piero Delprete*, Researcher – AMAP, IRD, Herbier de Guyane, Cayenne, French Guiana, France

*Hans-Joachim Esser*, Researcher & Curator – Herbarium, Botanische Staatssammlung München, München, Germany

*Javier Francisco-Ortega*, Professor – Department of Biological Sciences, Florida International University, Miami, FL, USA

*Ib Friis*, Honorary Professor – Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark

*Bruno Foggi*, Professor – Dipartimento di Biologia, Università di Firenze, Firenze, Italia

*David J. Goyder*, Research Leader – Royal Botanic Gardens, Kew Surrey, United Kingdom

*Gustavo Hassemer*, Professor – Federal University of Mato Grosso do Sul, Três Lagoas, MS, Brazil

*Alistair Hay*, Honorary Research Associate, Royal Botanic Gardens, Sydney, Australia

*Charles E. Jarvis*, Researcher and Curator, The Natural History Museum, London, UK

*Orlando O. Ortiz*, Researcher – Herbario PMA, Facultad de Ciencias Biológicas, Universidad de Panamá, Panama City, Panamá

*Alessio Papini*, Professor – Dipartimento di Biologia, Università di Firenze, Firenze, Italy

*Paul Peterson*, Researcher – Department of Botany, Smithsonian National Museum of Natural History, Washington DC, USA

*Prabukumar Km*, Plant Systematics & Genetic Resources Division & 'CMPR' Herbarium, Centre for Medicinal Plants Research (CMPR), Malappuram, Kerala, India

*Jefferson Prado*, Professor – Instituto de Botânica, Universidade de São Paulo, São Paulo, Brazil

*Heimo Rainer*, Researcher and Curator – Naturhistorisches Museum Wien, Wien, Austria

*Douglas E. Soltis*, Professor – Lab. of Molecular Systematics & Evolutionary, Department of Biology, University of Florida, Gainesville, FL, USA

*Pamela S. Soltis*, Professor – Lab. of Molecular Systematics & Evolutionary, Department of Biology & Florida Museum of Natural History, University of Florida, Gainesville FL, USA

*Robert Soreng*, Researcher – Department of Botany, Smithsonian National Museum of Natural History, Washington DC, USA

*Fred W. Stauffer*, Researcher and Head Curator – Conservatoire et Jardin botaniques de la Ville de Genève, Université de Genève, Chambésy, GE, Switzerland

*Mike Thiv*, Professor – Botany Department, Natural History Museum Stuttgart, Stuttgart, Germany

*Angelo Troia*, Researcher – Dipartimento STEBICEF, Università di Palermo, Palermo, Italy

*Wong Sin Yeng*, Institute of Biodiversity and Environmental Conservation, Universiti Malaysia, Sarawak & Harvard University Herbaria, Cambridge, USA
Journal of Plant Taxonomy
and Geography

WEBBIA

Vol. 77, n. 1 Suppl. - 2022
**Webbia. Journal of Plant Taxonomy and Geography**

Published by

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Direttore responsabile: **Romeo Perrotta**

Direttore scientifico: **Riccardo Maria Baldini**, University of Florence, Italy

Cover image: *Pteridocalyx appunii*. Upper Potaro River, near Chenapou Village, Guyana. Photo by Piero Delprete.

**Copyright** © 2022 Author. The author retain all rights to the original work without any restriction.

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OPEN ACCESS

**Citation:** Piero G. Delprete (2022) Monograph of tribe Sipaneeae (Rubiaceae, Ixoroideae). A Neotropical group with its center of diversity on the Guiana Shield. *Webbia. Journal of Plant TaxonomyandGeography*77(1 Suppl.):1-284. doi: 10.36253/jopt-13963

**Received:** February 3, 2022

**Accepted:** November 13, 2022

**Published:** November 16, 2022

**Copyright:** ©2022 Piero G. Delprete. This is an open access, peer-reviewed article published by Firenze University Press (http://www.fupress.com/webbia) and distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

**Data Availability Statement:** All relevant data are within the paper and its Supporting Information files.

**Competing Interests:** The Author(s) declare(s) no conflict of interest.

**Editor:** Riccardo M. Baldini

**ORCID:**
PGD: 0000-0001-5844-3945

# Monograph of tribe Sipaneeae (Rubiaceae, Ixoroideae). A Neotropical group with its center of diversity on the Guiana Shield

PIERO G. DELPRETE

AMAP Lab, IRD, CNRS, CIRAD, INRA, Université de Montpellier, 34398 Montpellier, France; AMAP Lab, IRD, Herbier de Guyane, B.P. 90165, 97323 Cayenne, French Guiana, France

E-mail: piero.delprete@ird.fr

**Abstract.** The tribe Sipaneeae (subfamily Ixoroideae) includes the genera *Chalepophyllum* (3 spp.), *Dendrosipanea* (3 spp.), *Limnosipanea* (3 spp.), *Maguireothamnus* (3 spp.), *Neblinathamnus* (2 spp.), *Neobertiera* (5 spp.), *Pteridocalyx* (1 sp.), *Sipanea* (17 spp.), *Sipaneopsis* (8 spp.), and *Steyermarkia* (1 sp.), for a total of 44 species. This tribe has its center of diversity on the Guiana Shield (northern South America), where 9 of the 10 genera occur. Only *Sipanea* and *Limnosipanea* are also present on the Brazilian Shield and the Orinoquia Region with a total of 4 species, while *Steyermarkia*, *Sipanea* and *Limnosipanea* are present in Central America with one species each. The genera *Sipaneopsis*, *Chalepophyllum*, and *Dendrosipanea* are endemic to white sand areas of the Amazon Basin. The habit in the tribe Sipaneeae ranges from herbs (terrestrial, amphibian or rarely aquatic), subshrubs, shrubs to treelets. Within the tribe, *Chalepophyllum*, *Dendrosipanea*, *Neobertiera*, *Pteridocalyx* and *Sipanea* are heterostylous, while the other genera are homostylous. Several recent articles have been dedicated to the description of new species in this tribe, and only *Limnosipanea spruceana* var. *macrantha* is newly described here. In the present work 21 names are newly typified; a list of these names is present at the end of the taxonomic treatment. For all the taxa of this tribe, full synonymy, typification, description, ecological observations, geographic distribution, illustrations, IUCN conservation assessment, and cited specimens are provided.

**Keywords:** *Chalepophyllum*, *Dendrosipanea*, *Limnosipanea*, *Maguireothamnus*, *Neblinathamnus*, *Neobertiera*, *Pteridocalyx*, *Sipanea*, *Sipaneopsis*, *Steyermarkia*, Neotropics, Central America, South America, monographic treatment, heterostyly, homostyly.
TABLE OF CONTENTS

<table><tbody><tr><td>Introduction</td><td>2</td></tr><tr><td>Historical summary</td><td>2</td></tr><tr><td>Material and Methods</td><td>7</td></tr><tr><td>Species and Variety Concepts</td><td>8</td></tr><tr><td>General Morphology</td><td>8</td></tr><tr><td>Habit</td><td>8</td></tr><tr><td>Stipules</td><td>9</td></tr><tr><td>Leaves</td><td>10</td></tr><tr><td>Leaf domatia</td><td>12</td></tr><tr><td>Colleters</td><td>12</td></tr><tr><td>Inflorescences</td><td>16</td></tr><tr><td>Flower</td><td>17</td></tr><tr><td>Heterostyly</td><td>18</td></tr><tr><td>Flowering modality</td><td>21</td></tr><tr><td>Hypanthia</td><td>21</td></tr><tr><td>Calyces</td><td>22</td></tr><tr><td>Calycophylls</td><td>24</td></tr><tr><td>Corollas</td><td>24</td></tr><tr><td>Stamens</td><td>27</td></tr><tr><td>Pollen</td><td>28</td></tr><tr><td>Styles</td><td>30</td></tr><tr><td>Ovaries</td><td>32</td></tr><tr><td>Fruits</td><td>32</td></tr><tr><td>Systematic treatment</td><td>33</td></tr><tr><td>Description of the tribe Sipaneeae</td><td>33</td></tr><tr><td>Key to the Sipaneeae genera</td><td>33</td></tr><tr><td>1. Chalepophyllum</td><td>35</td></tr><tr><td>2. Dendrosipanea</td><td>43</td></tr><tr><td>3. Limnosipanea</td><td>53</td></tr><tr><td>4. Maguireothamnus</td><td>73</td></tr><tr><td>5. Neblinathomnus</td><td>85</td></tr><tr><td>6. Neobertiera</td><td>90</td></tr><tr><td>7. Pteridocalyx</td><td>107</td></tr><tr><td>8. Sipanea</td><td>113</td></tr><tr><td>9. Sipaneopsis</td><td>226</td></tr><tr><td>10. Steyermarkia</td><td>254</td></tr><tr><td>Acknowledgments</td><td>257</td></tr><tr><td>References</td><td>259</td></tr><tr><td>List of Names typified in this Volume</td><td>266</td></tr><tr><td>Numerical List of Taxa</td><td>266</td></tr><tr><td>List of Specimens Examined</td><td>267</td></tr><tr><td>Index to Scientific Names</td><td>280</td></tr><tr><td>Biographical sketch of the Author</td><td>284</td></tr></tbody></table>

INTRODUCTION

The tribe Sipaneeae is here delimited according to the molecular phylogenies published by Rova et al. (2002) and Delprete & Cortés-B. (2004). A key to all the genera Rondeletieae sensu lato, including the genera here included in the Sipaneeae, is available in Delprete (1999). To facilitate the identification of the members of the Sipaneeae as here delimited, a key to genera is provided. Keys to species are available under each genus.

HISTORICAL SUMMARY

The present historical summary refers to the genera included in the tribe Sipaneeae as here delimited.

Aublet (1775: 147, tab. 56) published the first genus of this tribe, *Sipanea* Aubl. and positioned it in Pentandria Monogynia. He described this genus with the sole species *S. pratensis* Aubl., using specimens that he collected near Cayenne, French Guiana.

Rottbøll (1776: 7, tab. 2, fig. 2) published *Rondeletia biflora* Rottb. [= *Sipanea biflora* (Rottb.) Cham. & Schltdl.] citing material collected by Rolander in Suriname (see discussion under *Sipanea biflora* for further information).

Linnaeus filius (1782 ["1781"): 17) published the genus *Virecta* L.f. and placed it in Pentandria Monogynia. In *Virecta*, he described *V. biflora* L.f. [= *Sipanea biflora* (Rottb.) Cham. & Schltdl.] without citing *Rondeletia biflora* Rottb. He certainly referred to the species described by Rottbøll, based on the habit, the floral characters, and the specific epithet. Therefore, the binomial *Virecta biflora* should be treated as a new combination. For a complete explanation regarding this taxon, see discussion under *Sipanea biflora* (Rottb.) Cham. & Schltdl.

James Edward Smith (1818), in Abraham Rees' *Cyclopaedia* volume 4 part 2, described in great detail *Virecta* and the four species that he included in the genus: *V. biflora* [= *Sipanea biflora*], *V. procumbens* Sm. [= *Virectaria procumbens* (Sm.) Bremek.], *V. pratensis* [= *Sipanea pratensis*], and *V. multiflora* Sm. [= *Virectaria multiflora* (Sm.) Bremek.].

Kunth (1821 ["1820"): 397–398) described two new species of *Sipanea* using material collected by Bonpland and Humboldt in Venezuela: *S. glomerata* Kunth and *S. dichotoma* Kunth [= *S. pratensis* var. *dichotoma* (Kunth) Steyerm.].

Chamisso and Schlechtendal (1829) proposed the new combination *Sipanea biflora* citing both *Rondeletia biflora* Rottb. and *Virecta biflora* L.f. as synonyms. Along
with this new combination, they cited the two species recently published by Kunth, *S. dichotoma* Kunth [= *S. pratensis* var. *dichotoma*] and *S. glomerata* Kunth. They also commented that *Sipanea* is similar to *Rondeletia* L., from which it can be distinguished by the corolla mouth pubescent and the herbaceous stems (vs. corolla mouth glabrous and woody stems in *Rondeletia*).

Achille Richard presented a new Rubiaceae classification of 11 tribes and 154 genera, with the descriptions of numerous new genera and new species, in an oral conference at the Royal Academy of Sciences in Paris on 7 July 1829. He submitted his *Mémoire sur la famille Rubiacées* for publication 1829, in Paris, but was published in December 1830 (and reprinted in 1834). In the preface of his *Mémoire* he published the following warning notes ("Avertissement") (translated from French): "The *Mémoire* that I am publishing today was presented as an oral presentation at the Royal Academy of Sciences on 7 July 1829. Mister De Candolle at that time was studying the family Rubiaceae for the third volume of his *Prodromus*, and he had the kindness to ask me the presentation of my *Mémoire*, to avoid the double use [of names] that could result from the publication of the two works completed at the same time and on the same subject. I hastened to satisfy the request of this savant, and I gave him my manuscript and an atlas containg 45 plates in-4, all drawn by me, and representing the detailed analysis of 7/8 of the genera that compose the family Rubiaceae. From that atlas I extracted the 15 plates that accompany this *Mémoire*, as I was forced to reduce their number to avoid the considerable costs demanded for the impression of such high number of plates. Other circumstances independent of my will delayed until today the publication, and in this interval the fourth volume of the *Prodromus*, containing among other families, that of the Rubiaceae, was published. Meanwhile, I took advantage of the time that passed between the presentation of my *Memoire* at the Academy and its publication, to make some improvements. It resulted from these circumstances, although my work was precedent of that of the Professor Savant of Geneva, that his work was published first, and seems to have priority over my work; and as both our works were published at the same time, numerous genera and species that I established, they are indicated in the *Prodromus* under other names. This inconvenient is not that serious; however, I thought that it is necessary to report it, so that I will not be accused of unnecessarily give new names to genera or species that already had a name. It was already too late, when the *Prodromus* was published, so that I could correspond my names of genera and species with those in the work by Mister De Candolle. Paris, 1 December 1830."

Richard's new taxa published in the *Prodromus* were inconsistently cited by Candolle, some of them followed by "Rich." and others without the citation of A. Richard as original author. According to Stearn (1957), Delprete (1999) and Persson & Delprete (2017), the authority of the new taxa and new combinations of A. Richard published with Richard's authority in Candolle's *Prodromus* should be cited as: "A. Rich., in A.P. de Candolle" where "in A.P. de Candolle" is the bibliographic reference. However, Art. 46.8 of the current Code (Turland et al. 2018) states that "In determining the correct author citation, only internal evidence in the publication (as defined in Art. 35.4) where the name was validly published is to be accepted, including ascription of the name, statements in the introduction, title, or acknowledgedgedments, and typographical or stylistic distinctions in the text." Therefore, although there is ovewelming external evidence that Achille Richard is the rightful author of his new taxa published in the *Prodromus*, and that he was the author that studied the material at P, the use of the authority "A. Rich. in DC." is incorrect according to the current Code, and "A. Rich. ex DC." should be used instead. In addition, for Richard's new taxa published in Candolle's *Prodromus*, the original specimens are integrated in the Paris general herbarium (P), and highlighted by the note "Herb. Richard" that was handwritten in red ink by Albert Belhomme de Franqueville (1814-1891). While in G and G-DC are present only fragments of Richard's original specimens that were extracted from the P specimens. All the above factors should be taken into account when the action of typification is undertaken for Richard's new taxa published in Candolle's *Prodromus*.

Achille Richard (December 1830) in his *Memoire* described the tribe Cinchoneae to include the rubiaceous genera with bilocular, many-seeded capsules, and winged seeds, a group in which he included nine genera of the Rondeletieae s.l., with *Sipanea* among them. Within *Sipanea*, he included *S. pratensis*, and described the two African species that were already published in synonymy by A.P. de Candolle (September 1830) in *Virecta: Sipanea angustifolia* A. Rich. and *S. elatior* A. Rich., which are both illegitimate names (see below). Richard did not cite the two *Sipanea* species described by Kunth (1821 ["1820"]). He treated *Virecta* as a synonym of *Rondeletia* L., and published the new combination *Rondeletia biflora* (L.f.) A. Rich.; however, this binomial had been previously published by Rottbøll (1776), and Richard's combination is an isonym. Richard explained the publication of this binomial by stating that Linnaeus filius described *Virecta* as a unilocular capsule, while in this species they are clearly bilocular.
August Pyramus de Candolle (September 1830) largely followed Achille Richard's classification (December 1830) in the manuscript that Richard gave to him to be published in the *Prodromus*. However, Candolle provided several modifications and innovations with respect to Richard's classification, presenting a system of 13 tribes and 223 genera. He divided the tribe Hedyotidae (described as "Fructus capsularis bilocularis. Semina non alata") into two subtribes, and in the subtribe Rondeletieae (described as "Stipulae utrique binae concretae aut distinctae, nec vaginatae, nec multisetosae"), he positioned *Sipanea* and *Virecta* as closely related. He distinguished *Sipanea* from *Virecta* only by the included stamens and style, while he described the stamens and style of *Virecta* as exserted. Within *Sipanea*, Candolle included *S. pratensis*, *S. dichotoma* [= *S. pratensis* var. *dichotoma*], *S. glomerata*, and *S. biflora*. In *Virecta* he included *V. multiflora* Sm. [= *Virectaria multiflora* (Sm.) Bremek.], and *V. procumbens* Sm. [= *Virectaria procumbens* (Sm.) Bremek.], both names were originally published by J.E. Smith using material collected by Mr. Afzelius in Sierra Leone. Candolle (1830, p. 414) cited *Sipanea angustifolia* A. Rich. in synonymy under *V. multiflora*, and *Sipanea elatior* A. Rich. in synonymy under *V. procumbens*, making both Richard's names illegitimate and superfluous.

Joseph Dalton Hooker (1868: 38, tab. 1050) described the new genus *Limnosipanea* Hook.f., and positioned it in the Rondeletieae, to accommodate three species of semi-aquatic herbs: *L. spruceana* Hook.f., *L. schomburgkii* Hook.f. [= *L. palustris* (Seem.) Hook. f.], and *L. palustris* (Seem.) Hook.f.

Hooker (1873) proposed the first Rubiaceae classification influenced by the evolutionary concepts proposed by Darwin (1859). He was the first to introduce corolla aestivation as a significant character to be used for tribal definition within the Rubiaceae. He maintained *Sipanea* and *Limnosipanea* in the Rondeletieae, treating the herbaceous habit of these two taxa as a variable character within the tribe. In the same work, he published the new genus *Chalepophyllum* Hook.f., and positioned it in the Rondeletieae, indicating that it had only one species collected by Schomburgk in Guyana, but he did not publish the name of the species. Three years later, he published *Chalepophyllum guyanense* Hook.f., citing the same material collected by Schomburgk.

Baillon (1880, 1881), well-known for his excessive lumping of distinct genera, differed from Hooker (1873), and treated corolla aestivation as a trivial taxonomic character for tribal delimitation within the Rubiaceae. In addition, he treated *Limnosipanea* as a synonym of *Sipanea* and included the latter in the Portlandia Series or Portlandieae (Baillon 1881, pp. 331–337, 469–479). To

explain this decision, he wrote that (English version; Baillon 1881, p. 337) "The true *Sipanea* [or "*Eusipanea*"] has the flowers of *Rondeletia*, but with contorted corolla [lobes]. The calycinal divisions are lanceolate and subfoliaceous in those named *Limnosipania* [sic!] in which stamens are exserted and the leaves are verticillate, whilst in *Sipanea* proper the sepals are subulate, the stamens enclosed and the leaves verticillate [sic! the leaves in *Sipanea* are opposite, and in *Limnosipanea* are opposite or whorled]. They are annual or perennial herbs of tropical America, with flowers in axillary and terminal, often corymbiform cymes."

Schumann (1889, 1891) followed Hooker's delimitation of the Rondeletieae, and positioned *Sipanea* and *Limnosipanea* in that tribe. In addition, Schumann (1889: 249; 1891: 38–39) divided *Sipanea* into two sections: 1) Sect. I. *Eusipanea* K.Schum. "inflorescencia terminalis multi-rarissime uniflora coarctata, demum in cincinnos plus minus elongates transiens; capsula crustaceo-sub lignosa" [inflorescence terminal, multiflorous, or very rarely uniflorous, in more or less elongated cincinni; capsule crustaceous-subligneous] where he positioned *S. glomerata* and *S. pratensis*, and 2) Sect. II. *Panisea* K.Schum., "inflorescencia stricte axillaris 1-2 radius 3-flora (rarius ob gemmam apicalem parvam spurie terminalis); capsula papyracea" [inflorescence strictly axillary, 1-2(-3)-flowered (rarely appearing terminal at the apical bud); capsule papyraceous], where he positioned *S. biflora*. However, the inflorescences of *S. biflora* are terminal, sometimes appearing subaxillary, due to the reiteration of the axillary bud subtending the terminal inflorescence. In addition, in *Flora Brasiliensis* he treated *S. pratensis* as widely delimited [incl. *S. dichotoma*, *S. trichantha*, *S. vinca*, *S. hispida* Benth. ex Wernham, *S. acinifolia* Spruce ex Sprague (= *S. veris* S. Moore)], and his description was produced with a mixture of characters derived from specimens of several species, which he cited in the material examined, and the figure of the supposed *S. pratensis* (Schumann 1889, tab. 122) is instead of *S. hispida* Benth. ex Wernham. Schumann's wide delimitation of *S. pratensis* gave raise to considerable confusion among specialists, and the identity of this species was eventually clarified by recent authors (e.g., Steyermark 1972a; Delprete & Steyermark 2004e; Delprete 2010c). An expanded discussion of Schumann's confusion about these two species is available under *S. pratensis* (see Taxonomic Treatment, below).

Spencer Moore (1895: 398) described *Sipanea veris* S. Moore from a collection that he made in the state of Mato Grosso, Brazil.

Nicholas Edward Brown (1901: 33, tab. 33, fig. 10–17) added a second species to *Chalepophyllum*, describing *C*.
*speciosum* N.E. Br., and cited three collections made by McConnell and Quelch on Mount Roraima, at the triple border of Venezuela, Guyana and Brazil.

Wernham (1911) described the new genus *Pteridocalyx* Wernham as monotypic, and included it in the Rondeletieae, stating that it "is distinct from the rest of the tribe in the basal insertion of the stamens, the bifid stipules, and the combination of contorted aestivation with petaloid development of one or more of the calyx-lobes. *Pallasia* [Klotzsch (1853: 498), *nom. illeg. hom.* = *Wittmackanthus* Kuntze (1891: 302)] seems to be the nearest ally, but in *Pallasia* the aestivation is imbricate, and the stipules entire." The basal position of the stamens attributed to the *Pteridocalyx* was due to the fact that he studied a long-styled form of the taxon. Two years later, Wernham (1913) added a second species to the genus, *Pteridocalyx minor* Wernham, indicating that the "chief distinction from *P. appunii* lies in the undivided stipules, the much narrower foliaceous calyx-segments, and the wider corolla-tube."

Wernham (1917) described the genus *Neobertiera* Wernham, with a single species, and positioned it in the Hamelieae. He stated that "This genus falls indisputably into the tribe Hamelieae on the score of its fruits, seed, and corolla-characters, but it cannot be included with any genus yet described. The nearest ally is, perhaps, *Pseudohamelia* [Wernham 1912: 242], from which the present plant is readily separated by its contorted corolla, appreciably long filaments, glabrous conspicuous disc, and comparatively few and large globose seeds." He also stated that the inflorescence of *Neobertiera* is similar to those of a section of *Bertiera* Aubl., from which he derived the generic name. Wernham's description and discussion of *Neobertiera* are erroneous because he stated that its fruits are berries with a few seeds; however, subsequent observations by various authors (e.g., Steyermark, Delprete) confirmed that this genus belongs to the Sipaneeae. In the same article, Wernham (1917) revised *Sipanea* and recognized the following species: *S. galioides* Wernham (1917: 172), *S. spraguei* Wernham [= *S. veris*], *S. veris*, *S. biflora*, *S. pratensis*, *S. glabrata* Wernham, *S. hispida* Benth. ex Wernham, *S. trianae* Wernham [= *S. hispida*], *S. brasiliensis* Wernham [= *S. hispida*], and *S. colombiana* Wernham [= *S. pratensis* var. *dichotoma* (Kunth) Steyerm.]. He also listed the following species of which he was unable to examine the type: *S. glomerata*, *S. trichantha* Miq. [= *S. pratensis* var. *dichotoma*], "S. vinca* Mart. ex K. Sch. in Fl. Bras. VI. vi. 250 [*nom. illeg., pro syn.*], identified by Schumann with *S. pratensis*, may be *S. hispida*," and "*S. carnea* Neumann in Rev. Hort. II. ii. 445 (cum tab.) has been referred to above" [= *Pentas lanceolata* (Forssk.) Deflers].

Sandwith (1928) described *Sipanea micrantha* Sandwith, the species with the smallest flowers in the genus, hence the specific epithet, and stated that it was most similar to *S. biflora*, and maintained the genus in the Rondeletieae.

Bremekamp (1934a) treated *Sipanea* in the *Flora of Surinam*, where he recognized *S. stahelii* Bremek., *S. pratensis*, *S. coppenamensis* Bremek. [= *S. pratensis* var. *pratensis*], *S. ovalifolia* Bremek., and *S. biflora*, without mentioning the tribal affiliation of the genus.

Bremekamp (1934b), focusing on the Rubiaceae of Surinam, founded the tribe Sipaneeae Bremek. (as "Sipaneae"), stating that "The only Surinam genus of the Rondeletieae, *Sipanea*, ought to be excluded from that tribe on account of the contorted aestivation of its corolla lobes, and of its herbaceous growth. Together with the nearly related *Limnosipanea* it forms a separate tribe, for which I propose the name: *Sipaneae*."

Ducke (1935) described *Dendrosipanea* Ducke and positioned it in the Rondeletieae, commenting that it resembles *Ucriana* [certainly referring to *Ucriana longifolia* Spreng. = *Augusta longifolia* (Spreng.) Rehder, from central and southern Brazil], and *Sipanea*, in general aspect, although the latter is an herb and *Dendrosipanea* is a shrub or treelet. Ducke also stated that his new genus has loculicidal capsules, but, as Steyermark (1964: 195, 199) later corrected, its capsules are septicidal. *Dendrosipanea* differs from *Sipanea* by being a shrub or treelet with septicidal capsules, while species of *Sipanea* are prostrate, decumbent or erect herbs (a few species are somewhat woody at basal nodes) with loculicidal capsules. In addition, in the molecular phylogenetic analysis of Delprete and Cortés-B. (2004) *Dendrosipanea* was retrieved at a basal position within the tribe, indicating that the woody habit is ancestral within the tribe, while *Sipanea* was found on another clade.

Standley (1940) described *Steyermarkia* Standl. from material collected in Guatemala. He treated *Steyermarkia* as related to *Sipanea*, and placed these two genera in the widely circumscribed Rondeletieae (incl. Sipaneeae).

Verdcourt (1958) maintained *Sipanea*, *Limnosipanea* and *Steyermarkia* in the tribe Rondeletieae as widely delimited, treating the herbaceous habit as a trivial character for the separation of the Sipaneeae.

Bremekamp (1966: 20) proposed a new classification of the Rubiaceae, dividing the family into eight subfamilies. In this treatment, he characterized the Sipaneeae as "a small tribe containing but three genera; on account of their herbaceous growth they occupy a somewhat isolated position in the subfamily [Cinchonoideae]. These genera are *Sipanea* Aublet, *Virecta* Vahl [=*Sipanea*] and *Limnosipanea* Hook.f."
Steyermark (1964) in the series *Botany of the Guayana Highlands* treated *Chalepophyllum*, and emended *Dendrosipanea*, separating them by numerous morphological characters. In the same work he described the new genera *Maguireothamnus* Steyerm. and *Neblinathamnus* Steyerm., and positioned them in the Rondeletieae.

Steyermark (1967: 284–289) described the new genus *Sipaneopsis* Steyerm., where he included six species, stating that it is “similar to both *Sipanea* and *Rondeletia*. Because of the imbricate aestivation of the corolla lobes, it is more closely related to *Rondeletia*." In the key to the Rondeletieae genera, Steyermark (1967: 234–235) characterized *Sipaneopsis* as having “Fruit indehiscent, endocarp hard, bony-crustaceous; seeds relatively few, turgid, 6–12 in a fruit; orifice of corolla with 5 thickened triangular projections covered with erect brushy white hairs.” In the same key to the Rondeletieae genera, the he included: *Gleasonia* Standl., *Sipaneopsis*, *Cuatrecassiosiodendron* Standl. & Steyerm. ex Steyerm. [= *Arachnothryx* Planch.], *Rondeletia* L., *Arachnothryx*, *Pteridocalyx*, *Neobertiera*, *Maguireothamnus*, *Neblinathamnus* [as “*Neblinanthus*”], *Sipanea*, *Limnosipanea*, *Chalepophyllum*, and *Dendrosipanea*.

Steyermark (1974), in the Rubiaceae of the *Flora de Venezuela* maintained the same delimitation of the Rondeletieae of 1967. Of the tribe *Sipaneeae*, as here delimited, he treated *Sipaneopsis*, *Maguireothamnus*, *Neblinathamnus*, *Sipanea*, *Limnosipanea*, *Chalepophyllum*, and *Dendrosipanea*, providing keys, full descriptions, geographic distributions, and specimens cited for the species occurring in Venezuela.

Robbrecht (1988) “provisionally maintained [the *Sipaneeae* as] Bremekamp’s segregate of Rondeletieae for these three genera with herbaceous habit and contorted aestivation” adding that “a revision of the Rondeletieae/Condamineae complex may well show that this is not justified”. In the *Sipaneeae* he included *Sipanea*, *Limnosipanea* and *Steyermarkia*, while he positioned the other genera of this tribe, as here delimited, in the tribe Rondeletieae, and treated *Neobertiera* as a dubious genus probably related to *Bertiera*.

Delprete (1999) followed Verdcourt (1958) and Steyermark (1964, 1967, 1974), and included the *Sipaneeae* and part of the Condamineae within a very widely circumscribed Rondeletieae, mostly due to general morphological similarities. In Delprete’s treatment, there is a key to all the genera of the broadly delimited Rondeletieae, including all the genera here included in the *Sipaneeae*.

Because of the standing uncertainty about the delimitation of the above cited tribes, Rova et al. (2002)

undertook a molecular phylogenetic study of the Condamineae-Rondeletieae-Sipaneeae complex using *trnL-F* sequence data, and arrived at several unexpected results. In that study, *Maguireothamnus*, *Sipanea*, *Sipaneopsis* and *Neobertiera* were found on a strongly supported clade, which corresponded to the tribe *Sipaneeae* as here delimited. The positioning of *Maguireothamnus* within this group was a surprise. Historically, it was placed within Rondeletieae s.str. due to its suffrutescent habit and many-seeded capsules, but was exceptional in either tribe because of its large, long-tubular corollas. To add morphological support for the position of *Maguireothamnus* in *Sipaneeae*, Rova et al. (2002) presented a convincing set of palynological characters. Also, *Sipaneeae* genera were retrieved, for the first time, within the subfamily Ixoroideae, along with a portion of Rondeletieae, sensu Delprete (1999). In addition, for the first time, the *Sipaneeae* clade was found to be sister to a small clade containing *Gleasonia* (tribe Henriquezieae), *Posoqueria* Aubl., and *Molopanthera* Turcz. The last two genera are unique in the family because of their peculiar pollen catapult mechanism (Schumann 1888; Delprete et al. 2005; Rova et al. 2002), and were later transferred by Delprete (2004, 2009) to the tribe *Posoquerieae*.

The results of Rova et al. (2002) stimulated Delprete and Cortés-B. (2004) to undertake a phylogenetic analysis of the *Sipaneeae*, using *trnL-F* and ITS sequences, where they included other genera believed to be related to *Sipaneeae* due to their overall morphological similarity with the core genera, and many representative members of the subfamily Ixoroideae. With these additional genera, the *Sipaneeae* group under study included *Chalepophyllum*, *Dendrosipanea*, *Limnosipanea*, *Maguireothamnus*, *Neblinathamnus*, *Neobertiera*, *Pteridocalyx*, *Sipanea*, *Sipaneopsis*, and *Steyermarkia*, for a total of about 50 species. In both combined *trnL-F* + ITS and *trnL-F* analyses, the tribe *Sipaneeae* was shown to be monophyletic, and positioned within the subfamily Ixoroideae. Within the *Sipaneeae*, the *Sipanea* clade was found to be sister to the *Neobertiera-Sipaneopsis* clade. Delprete and Cortés-B. (2004) also tested the two sections of *Sipanea* proposed by Steyermark (1967): 1) Sect. *Sipanea*, characterized by erect or ascending herbs with 3-20(-many)-flowered inflorescences and thick-walled capsules; 2) Sect. *Virectaria* (L.f.) Steyerm., characterized by prostrate or creeping herbs with 1-3(-5)-flowered inflorescences and thin-walled capsules. In the molecular phylogenies of Delprete and Cortés-B. (2004), the species of the two sections are intermixed, and therefore concluded that Steyermark’s sections are not monophyletic. In addition, it is interesting to note the alternation of erect and prostrate habit
of *Sipanea* species in the phylogenies obtained. However, because only 9 out of the 17 species were sampled, they refrained from suggesting any further evolutionary inferences within the genus. *Sipanea* and *Limnosipanea* have been traditionally treated as closely related genera (e.g., Bremekamp 1934b, 1966; Steyermark 1974; Delprete 1999), because of their herbaceous habit and morphological similarity, but the phylogenies of Delprete and Cortés-B. (2004) contrasted with this opinion. While their molecular analyses confirmed the monophyly of both genera, *Sipanea* and *Limnosipanea* are not sister taxa, and therefore the herbaceous habit originated at least twice within the tribe. The genera *Seyermarkia*, *Pteridocalyx* and *Neblinathamnus* were not included in Delprete and Cortés-B. (2004) analyses, due to unsuccessful attempts to extract DNA from relatively old herbarium specimens, and therefore, it was impossible to test their phylogenetic position within the tribe. However, because of their general morphological similarities (e.g., membranous corola with left-contorted aestivation, capsular fruits, and stalked placenta with many seeds), they were tentatively maintained in the Sipaneeae, pending future molecular phylogenetic studies.

Delprete (2015a) emended the description of *Neobertiera*, reported for the first time that the genus is heterostylous, and described three additional species. The four species are restricted to the Guayana Shield, with two species probably restricted to Guyana, and two species probably restricted to French Guiana.

Delprete (2018) described two new species of *Dendrosipanea* and *Sipaneopsis*. The two new species, *D. prancei* Delprete and *S. duckei* Delprete, are endemic to white-sand areas from the Brazilian and Colombian Amazon. He demonstrated, for the first time, that *Dendrosipanea* is heterostylous and added a key to the three recognized species of this genus.

Delprete (2019a) revised *Pteridocalyx* and treated it as a monospecific, heterostylous genus. In addition, he described the placenta of *Pteridocalyx* as longitudinally adnate along the central septum; however, recent anatomical studies (Delprete, pers. obs., see below) revealed that the placenta has a minute stalk inserted at the distalmost portion of the septum, i.e., near the roof of the locule, and terminates with a pendulous, narrowly cylindrical extension almost as long as the locule. Following these studies, *Pteridocalyx* is here confirmed as unique within the Sipaneeae because of its calycophylls and placenta with a stalk inserted at the distalmost portion of the septum, with a pendulous cylindrical extension, on which the ovules are inserted.

Delprete (2019b) presented an additional study on *Neobertiera* in which a new species, *N. montedouraden-

sis* Delprete, was published based on a specimen from the town of Monte Dourado, near the Jari River, state of Pará, Brazil. It is unique within the genus because of hypanthia and fruits with basally tuberculate trichomes. Specimens recently analyzed showed that this species was collected in other localities in the states of Pará and Amapá. In the same study, the type specimen of *Bertiera palustris* A.Rich. (in A.P. de Candolle 1830: 392) was analyzed, and it was concluded that it is synonymous with *N. glomerata* Delprete, a name recently published for a species occurring in French Guiana; therefore, the new combination *N. palustris* (A.Rich.) Delprete was proposed.

In conclusion, according to the results and discussion presented by Delprete and Cortés (2004) and Delprete (2015a, 2018, 2019a, 2019b), the tribe Sipaneeae is here delimited to include the genera *Chalepophyllum* (1 spp.), *Dendrosipanea* (3 spp.), *Limnosipanea* (3 spp.), *Maguireothamnus* (3 spp.), *Neblinathamnus* (2 spp.), *Neobertiera* (5 spp.), *Pteridocalyx* (1 sp.), *Sipanea* (17 spp.), *Sipaneopsis* (8 spp.), and *Seyermarkia* (1 sp.), for a total of 44 species.

## MATERIAL AND METHODS

This study is based on examinations of herbarium specimens, material preserved in 60% ethanol, and field observations. Herbarium specimens were studied either on site or through loans from the B, B-W, BBS, BM, BR, BRB, C, CAY, CEN, COL, E, F, FI, G, G-DC, HEPH, HTO, IAN, IBGE, INPA, K, L, LINN-SM, MBM, MG, MO, MPU, NY, NX, P, P-AD, P-BONPL, P-JJR, P-JU, R, RB, U, UB, UFG, UFMT, UMP, US, and VEN herbaria. Digital images of herbarium specimens were analyzed through the following websites: Jstor Global Plants (https://plants.jstor.org/), Reflora - Brazilian Plants: Historic Rescue and Virtual Herbarium for Knowledge and Conservation of the Brazilian Flora (http://reflora.jbrj.gov.br/reflora/PrincipalUC/PrincipalUC.do?lingua=en), and INCT - Herbário Virtual da Flora e Fungos (http://inct.splink.org.br/).

Pollen observations were made on samples obtained from flower buds of specimens at CAY, F, S, U, and US herbaria. For pollen preparation, nearly mature flower buds, just before anthesis, were extracted from herbarium specimens and softened in 1:200 Agepon solution for 30 minutes. The anthers were then dissected and pollen was isolated by sieving with mesh of width 63 µµi after which they were dehydrated in glacial acetic acid and acetolysed in concentrated sulphuric acid and acetic acid 1:9 for 10 minutes in a heating block at
95°C. Grains destined for LM studies were mounted in Kaiser's glycerin jelly. Values of the length of polar and equatorial axes were based on LM measurements, using an Olympus BX 51 microscope, an Olympus ColorView Soft Imaging System camera and AnalySis software. Pollen images and measurements were made by Iris van der Beeten at the Meise Botanic Garden, Meise, Belgium.

Species descriptions are based on field observations, dried herbarium material, and spirit material. Measurements used in the descriptions were made from dry herbarium specimens. Barcode numbers of herbarium specimens, when available, are cited in square brackets after the herbarium acronym; when the barcode number is not available, the accession number, is cited preceded by "Acc. No." and in square brackets. All specimens cited have been examined, unless indicated by "n.v." (not seen) after the herbarium acronym.

Information about collection dates and localities of specimens gathered by Martius in Brazil were obtained from the text and the maps available in Spix and Martius (1976). Pohl's collection dates and localities in Brazil were obtained by Pohl's (1976) travel diary.

Coordinates from collecting sites in French Guiana, when not indicated on specimen labels, were obtained from Hoff and Cremers (1996).

A conservation status assessment of each taxon studied was made using the IUCN Red List Categories and Criteria (IUCN 2012, 2019).

## SPECIES AND VARIETY CONCEPT

In this study, the taxonomic species concept of Davis and Heywood (1963) was used: "assemblages of individuals with morphological features in common and separable from other such assemblages by correlated morphological discontinuities in a number of features." I also tried to reevaluate with a critical approach many morphological characters that have been historically treated as significant for generic delimitation in the Rubiaceae (e.g., corolla aestivation, heterostyly, fruit dehiscence, placement, vestiture, leaf shapes, stipules, etc.).

Steyermark's publications (1964, 1967, 1972a, 1972b, 1974) represent an important contribution towards the understanding of the members of the tribe Sipaneeae, as the group is mostly centered on the Guiana Shield. He expressed his concepts of infraspecific ranks in a note on *Sipanea pratensis* (Steyermark 1967: 271) in which he recognized numerous varieties and forms: "After a prolonged study of numerous specimens, it is believed in the best interests of taxonomy to render the great variation expressed by the assignment of varietal and for-

mal categories. No subspecies are given, since there does not appear to be any definite geographic range indicated within the variations, and the differences manifests appear to intergrade in various portions of the variable characters." In other words, Steyermark allowed varieties and forms to widely overlap throughout their geographic ranges (i.e., sympatric varieties). However, according to the concepts adopted in the present treatment, only one infraspecific rank is used, the variety, which is defined by a secondary variation with a morphological-geographical correlation, which largely corresponds to Steyermark's subspecies concept. In other words, geographically separated (allopatric) populations correlated with some morphological characters and that are not sufficiently distinct to be accepted as different species; therefore, I opted to use the rank of variety for such populations. This is in accordance with current practice in Neotropical Rubiaceae taxonomy (e.g., Delprete 1999, 2010a, 2010b, 2010c; Persson and Delprete 2017), and is used here to maintain nomenclatural stability.

## GENERAL MORPHOLOGY

### Habit

The habit in the tribe Sipaneeae ranges from annual or perennial herbs, subshrubs, shrubs to treelets. Plants that are basally woody and distally herbaceous are here called subshrubs, for lack of a better term. Therefore, species that are entirely herbaceous at early stage and with woody basal internodes at later stage are described as "herbs or subshrubs (woody at basal internodes)". However, plants that are up to 50 cm tall and entirely woody are also here called subshrubs. The degree of habit variation at the generic level within the Sipaneeae is discussed below.

For non-erect plants, three habits are found in the Sipaneeae for herbs, subshrubs and shrubs. The terminology adopted for these habits follows The American Heritage Dictionary of the English Language (2020) with the following definitions:

1) Decumbent: "Lying or growing on the ground but with erect or rising tips";

2) Prostrate: "Growing flat along the ground";

3) Ascending: "Growing or directing upward from a curved or slanted base".

A summary of the habits found in the genera of the Sipaneeae is presented below.

*Steyermarkia* is exceptional within the tribe by being a subsessile plant with a rosette of large leaves spreading near the ground, and a short, unbranched, woody stem, exceptionally to 18 cm long.
*Dendrosipanea* can be either a shrub or a treelet, 0.5–4 m tall; while *Chalepophyllum*, *Maguireothamnus* and *Neblinathamnus* are woody subshrubs or shrubs, 0.3–4 m tall, usually erect or rarely partially prostrate.

In *Neobertiera* the habit varies from perennial herbs, subshrubs (woody at basal internodes or entirely woody) to shrubs, 0.4–4 m tall, erect or basally decumbent, sparsely branched. *Neobertiera gracilis* Wernham and *N. palustris* range from perennial herbs to subshrubs (woody at basal internodes) to shrubs, 0.5–4 m tall; *N. micrantha* Delprete is a perennial herb, 0.5 m tall; while *N. montedouradensis* Delprete and *N. pakaraimensis* Delprete are shrubs (i.e., entirely woody), 1 m tall and 0.5–4 m tall, respectively.

*Pteridocalyx* is a single-stemmed woody plant, 1–2 m tall, with a central, thin stem, and sparsely branched at the top.

*Sipaneopsis* is a genus endemic to Amazonian white-sand areas, with most species ranging from subshrubs (partially or entirely woody) to shrubs, 0.3–1.6 m tall, erect, ascending, or rarely decumbent (basal portion sometimes prostrate), single-stemmed or with a few to many branches. Two species are exceptional within *Sipaneopsis* by having herbaceous habit: *S. pacimoniensis*, which is a single-stemmed perennial herb 10–12 cm tall, and *S. cururuensis* J.H.Kirkb., which ranges from herb to subshrub (woody at basal internodes) 25–50 cm tall.

Most species of *Sipanea* are herbs, erect, trailing, procumbent or decumbent, often rooting at basal nodes, sometimes mat-forming, or rarely floating on water in inundated areas (*S. biflora*). Several species of *Sipanea* (*S. glomerata*, *S. hispida*, *S. pratensis* var. *dichotoma*, *S. prancei*, *S. wilson-brownei*) range from herbs to sub-shrubs, i.e., completely herbaceous or with stems woody at base and distally herbaceous, 0.3–1.5 m tall, and erect or decumbent. The degree of woodiness of the basal internodes in these species depends on the age of the plant.

The three species of *Limnosipanea* are herbs, either terrestrial, semi-aquatic (amphibious) or aquatic, erect, prostrate or decumbent; short-lived (2–4 months life span) when terrestrial or semi-aquatic, or perennial when growing in permanently flooded areas. *Limnosipanea erythraeoides* is a terrestrial or semi-aquatic (amphibious) herb, prostate or decumbent, with main stems 8–20 cm long, single-stemmed or sparsely branched; with leaves opposite throughout the whole plant or 3–4 per node at basal nodes and opposite at distal nodes. *Limnosipanea palustris* is a terrestrial or semi-aquatic (amphibious) herb, ephemerous (2–4 months life span), erect, 5–40 cm tall, single-stemmed or sparsely branched, with leaves commonly opposite, or sometimes ternate at basal nodes.

*Limnosipanea spruceana* is a polymorphic herb, adapted to terrestrial, seasonally flooded, or permanently flooded environments. Three main habits were detected in this species. In localities seasonally inundated, during full rainy season the water level might reach up to 4–5 m in depth, especially in Amazonian savannas; as the precipitations decrease, the water level gradually diminishes until the soil is still moist but no longer flooded; at this precise moment the terrestrial form of this species appears, sometimes forming large stands, easy to spot from a distance because of the dark red vegetative parts; this terrestrial form is erect, 3.5–25 cm tall, and particularly short-lived, as it can grow, disperse seeds and die within three months. A second form is found in permanently flooded areas, as in localities with natural springs; in this form, the submerged portion of the stem could be up to 40 cm long, not branched, green to whitish-green, with the basal portion leafless, adventitious roots at each node, and the distal submerged portion with 3–6(-8) linear to acicular leaves per node, and without adventitious roots. The aerial portion of these plants is 10–25 cm long (including inflorescences), branched, with stems and rachis red-vinaceous, with 2–5 leaves per node, and blades linear to lanceolate; this form is perennial. A third form is found in seasonally flooded areas, with water 20–30 cm deep during the rainy season; in this environment the plants are seasonally semi-aquatic (amphibious), with dimorphic leaves (i.e., submersed and aerial); at the end of the rainy season, when the water is completely dissipated, the plants become terrestrial and are decumbent, with the portion of stem that was submerged, 20–30 cm long and with 3–6(-8) linear to acicular leaves per node, leaning on the ground, and the distal portion erect, 10–20 cm long (including inflorescences), with 2–5 linear to lanceolate leaves per node; at this stage, the stem, leaves and the rachis are red to reddish, due to sun exposure; this latter form, has a life span of three to four months.

## Stipules

Delprete (1999: 25) proposed three degrees of stipule persistency in Rubiaceae: 1) readily caducous, present only at the vegetative bud, 2) caducous, present during leaf development, but caducous before the leaves fall off, and 3) persistent, present after the leaves of the same node fall off. According to these definitions, stipules are persistent in all Sipaneeae genera.

Stipules in the Sipaneeae are interpetiolar, and can be free or connate at the base or sometimes adnate to
the petioles of the same node. They are very variable and can provide important diagnostic characters for the identification of genera and species.

In *Chalepophyllum*, stipules are broadly triangular or sometimes becoming bifid at apex at older stages (Figure 1A–B). In *Dendrosipanea*, they are free or narrowly connate at the base, deltoid, and acuminate, bifid at apex, or with two small lobes on each side of the stem (Figure 1C–D). In *Limnosipanea*, they are minute to almost obsolete, reduced to a line between the petioles, sometimes with a small mucro or a seta at the center, often withering on the stem, and no abscission layer is formed (Fig. 1E). In *Maguireothamnus*, they are adnate to the petioles (Figure 1F), narrowly triangular or basally triangular and aristate (rarely linear), with a row of 3–7 colleters on each side, inserted just below the margin on the internal side or on the margin of the basal sheath. In *Neblinathamnus* they are adnate to the petioles, minute, broadly to shallowly triangular to truncate, and often bifid at apex, or divided into two lobes on each side of the stem (Figure 1K–L).

In *Neobertiera*, they are ovate to broadly ovate, acuminate or bifid at apex (Figure 1G–H), or narrowly triangular in *N. montedouradensis*. In *Pteridocalyx*, they are ovate to narrowly triangular, entire or bifid at apex (Figure 1I–J); this variation can be present on the same plant, as sometimes the stipules are entire at early stage and remain so at later stage, or they might become bifid at apex in later stages.

*Sipanea* is the largest genus in the tribe, and its stipules are quite variable in shape and size (Figure 2). They can be either free or basally adnate to petioles and vary from truncate to broadly transversally elliptic, broadly to narrowly triangular, suborbicular, subulate, linear, or rarely setaceous or reduced to a line between the petioles. Because of this variation, stipules provide a significant diagnostic characters that can be used to distinguish species within the genus.

In *Sipaneopsis* the stipules can be free or conulate at base, broadly to narrowly triangular, acuminate and bilobed at apex, or bifid with narrowly triangular lobes (Figure 3), or topped by (1-)3-4 linear lobes (*S. morichensis*) or reduce to a line topped by several

lobes (*S. rupicola* (K.Schum.) Steyerm.). In certain species (e.g., *S. foldatsii* Steyerm.) they are triangular and consistently entire (i.e., not lobed). In *S. duckei* Delprete (Figure 3B), stipules are broadly triangular at base and linear at distal portion, or narrowly triangular to narrowly oblong-triangular; also, they can be entire at early stage and remain so at later stages, or they might rarely become bifid at apex on older nodes. In *S. rupicola* they are very variable (Figure 3F–H): they can be triangular, entire and caudate, or triangular at base topped by 2-3 acute lobes, or reduced to a line topped by 6-7 linear lobes or by two long lobes intercalated with shorter lobes.

In *Steyermarkia*, stipules are persistent, free at base, lanceolate to linear-lanceolate, and attenuate or bifid at apex.

## Leaves

In most Sipaneeae genera, the leaves are opposite and homophyllous, with two exceptions. In *Neblinathamnus*, the leaves might be opposite or ternate. In *Limnosipanea*, the leaves are opposite or whorled, and homophyllous or heterophyllous (see discussion below).

Leaf shape and size vary within and among genera, providing several diagnostic characters that can be used to distinguish genera and species.

In *Chalepophyllum*, the leaves are subsessile to short-petiolate, with ovate, obovate, oblong or spathulate, subcoriaceous blades. In *Dendrosipanea*, they are subsessile to short-petiolate, with oblong, spathulate or oblanceolate, subcoriaceous blades.

In *Limnosipanea*, the leaves are sessile, membranaceous or chartaceous, and can be opposite or whorled. They are homophyllous and opposite or ternate in terrestrial plants, or heterophyllous and with a different phyllotaxy in partially or seasonally submerged (semi-aquatic or amphibious) plants, and in permanently submerged (aquatic) plants. *Limnosipanea erythraeoides* is prostate or decumbent herb, terrestrial or semi-aquatic, with homophyllous leaves, which can be opposite throughout the whole plant, or 3-4 leaves at basal nodes and

**Figure 1.** Stipules variation in selected genera of the tribe Sipaneeae. **A–B.** *Chalepophyllum guyanense*, stipule variation on the same branch. **A.** Entire stipule. **B.** Bifid stipule. **C–D.** *Dendrosipanea revoluta*, stipule variation on the same branch. **C.** Entire stipule. **D.** Bifid stipule. **E.** *Limnosipanea erythraeoides*, node with base of two leaves, and extremely reduced stipule with three partially exserted colleters. **F.** *Maguireothamnus tatei*, nodes with permanent, overlapping stipules. **G.** *Neobertiera gracilis*, node with bifid stipule. **H.** *Neobertiera montedouradensis*, node with entire stipule. **I–J.** *Pteridocalyx appunii*, stipule shapes present on the same branch. **I.** Entire stipule. **J.** Bifid stipule. **K–L.** *Neblinathamnus argyreus*. **K.** Shallow, truncate stipule. **L.** Shallow, bilobed stipule. **A–B:** drawn from *Delprete & Araujo 7429* (CAY); **C–D:** drawn from *Wurdack & Adderley 42972* (US); **E:** drawn from *Macedo 5537* (US); **F:** drawn from *Maguire & Politi 28449* (US); **G:** drawn from *Maguire & Fanshawe 22964* (F); **H:** drawn from *Santos 414* (MG); **I–J:** drawn from *Delprete & Benjamin 12813* (CAY). Illustration by Piero Delprete.
<figure><img src="image_5.png" /><figcaption>Figure 1.</figcaption></figure>
opposite at distal nodes. *Limnosipanea palustris* is an erect, terrestrial or semi-aquatic (amphibious) herb, with homophyllous leaves, which are commonly opposite or sometimes ternate at basal nodes.

*Limnosipanea spruceana* is a polymorphic, erect or decumbent herb, adapted to terrestrial and to seasonally or permanently flooded environments. In this species, the leaves are homomorphic, opposite or whorled in terrestrial plants, or whorled and dimorphic in submerged plants. Three main forms were detected in this species. In the terrestrial, short-lived form, found in seasonally inundated localities, the leaves are homomorphic, opposite or 3-5 per node, with linear to lanceolate blades. The second form is perennial, and grows in permanently flooded areas, and has heteromorphic leaves; the basal portion of the submerged portion the stem is leafless and with adventitious roots at each node, while in the distal submerged portion the leaves are whorled, 3-6(-8) per node, linear to acicular blades; and the aerial portion has 2-5 leaves per node, with linear to lanceolate blades. The third form grows in seasonally flooded areas. During the rainy season, the plants are semi-aquatic (amphibious), with dimorphic submerged and aerial leaves, as described for the second form. At the end of the rainy season, when the water is completely dissipated, the portion of stem originally submerged, with whorled leaves (3-6(-8) per node), is laying on the ground, and the distal portion of the stem is erect, with 2-5 leaves per node, and linear to lanceolate blades.

In *Maguireothamnus*, the leaves are sessile, subsessile or short-petiolate, and the blades are ovate, obovate, oblong, oblanceolate to lanceolate, and thinly to thickly coriaceous. *Neblinathamnus* has short-petiolate or subsessil leaves, with elliptic, obovate or oblong, thinly coriaceous blades. In *Neobertiera* and *Pteridocalyx*, they are petiolate, and with elliptic, oblong-elliptic to oblanceolate, chartaceous blades.

In *Sipanea*, the leaves are sessile or subsessile to short-petiolate, rarely with axillary brachyblasts with numerous smaller leaves (e.g., *S. galioides* Wernham); and the blades are ovate, narrowly ovate, rhombic-ovate, elliptic, oblong-elliptic, oblong-lanceolate, or linear-

lanceolate to linear, and membranaceous, chartaceous or thinly subcoriaceous. *Sipaneopsis* has short-petiolate leaves, with ovate, elliptic, lanceolate or linear, and chartaceous or subcoriaceous blades.

*Steyermarkia* is a subsessile plant, with leaves in rosettes spreading near the ground. The leaves are short-petiolate, with large, narrowly obovate to oblanceolate, membranaceous to chartaceous blades.

## Leaf domatia

Leaf domatia in Rubiaceae are commonly tufts of hairs, correlated or not with a pit or a crypt, and present on the abaxial side in the axils of the secondary veins, or rarely in the axils of the tertiary veins. Domatia are commonly associated with presence of mites. Leaf domatia are absent in all genera of the Sipaneae, with the sole exception of the tuft-domatia present in the axils of secondary veins of *Chalepophyllum guyanense*.

## Colleters

Colleters have been defined by Robbrecht (1988) as "pluricellular mucilage-secreting structures occurring inside stipules and on other organs." He also reported that they have previously been called *drusenzotten* (Solereder 1893), shaggy hairs (Solereder, 1908), glandular shaggy hairs (Metcalfé and Chalk 1950), *harzsecerniberende drusen* (Krause 1909), *cérocystes* (Hallé 1967), *squamellae* (Ramaya and Bahadur 1968), and *annexes glanduleuses* (Boiteau and Allorge 1978). Steyermark (1964, 1967, 1974, 1984a, 1984b) called them "glándulas", "glands" or "squamellae". According to modern literature, these minute structures are called colleters (e.g., Esau 1965; Lersten 1974a, 1974b, 1975; Robbrecht 1988; Verdcourt 1976; Rogers 1984, 1987; Delprete 1999; Persson and Delprete 2017). Esau (1965) clarified that the term colleter is "derived from the Greek *Colla* [= glue], referring to the sticky excretion from this structure" and "they frequently produce a mixture of terpenes and mucilage." In Spanish, they are called "coléter" (sing.) or

**Figure 2.** Stipule variation in *Sipanea*. **A.** *Sipanea glaberrima* [Section *Sipanea*], node with stipule and petioles. **B.** *Sipanea glomerata* [Section *Sipanea*], node with sheathing stipule and leaf bases. **C.** *Sipanea pratensis* var. *pratensis* [Section *Sipanea*], node with sheathing stipule and leaf bases. **D.** *Sipanea veris* [Section *Sipanea*], node with sheathing stipule and partially inserted colleters, and leaf bases. **E.** *Sipanea micrantha* [Section *Virecta*], node with sheathing stipule with partially inserted colleters, and petioles. **F.** *Sipanea carrenoi* [Section *Virecta*], node with stipule and petioles. **G.** *Sipanea setacea* [Section *Virecta*], node with setaceous stipule and petioles. **H.** *Sipanea stahelii* [Section *Nudae*], node with stipule and basal portion of petioles. **I.** *Sipanea saxicola* [Section *Nudae*], node with stipule reduced to a line between petioles, inserted colleters, and basal portion of petioles (note long, erect trichomes). **A:** drawn from *Rombouts 223bis* (U, holotype); **B:** drawn from *Williams 13016* (US); **C:** drawn from *Delprete 12882* (CAY); **D:** drawn from *Molina & Barkley 18-V-161* (US); **E:** drawn from *McDowell 3779* (US); **F:** drawn from *Steyermark et al. 115598* (MO); **G:** drawn from *Huber et al. 8245* (NY, holotype); **H:** drawn from *Maguire 24314* (US); **I:** drawn from *Martinelli et al. 7074* (MG). Illustration by Piero Delprete.
<figure><img src="image_6.png" /><figcaption>Figure 2.</figcaption></figure>
<figure><img src="image_7.png" /><figcaption>**Figure 3.** Stipule variation in *Sipaneopsis*. A. *Sipaneopsis cururuensis*, node with stipule and basal portion of petioles. B. *Sipaneopsis duckei*, node with stipule and basal portion of petioles. C. *Sipaneopsis maguirei*, node with stipule and basal portion of petioles. D. *Sipaneopsis paci-moniensis*, node with stipule and basal portion of petioles. E. *Sipaneopsis huberi*, node with sheathing stipule and basal portion of petioles. F-H. *Sipaneopsis rupicola*, nodes with stipule variation. A: drawn from Egler & Raimundo 1265 (MG, isotype); B: drawn from Egler 273 (MG); C: drawn from Delprete et al. 7452 (CAY); D: drawn from Maguire et al. 37570 (NY, holotype); E: drawn from Huber & Medina 5786 (U, isotype); F: drawn from Williams 14897 (US); G-H: drawn from Gutierrez & Schultes 654 (US). Illustration by Piero Delprete.</figcaption></figure>

“coléteres” (pl.), for which Font Quer (2000: 245) offers
the following definition (translated from Spanish) “from
Greek χόλλα, gum, and ουρητηρ, urethra. Hair secreting

mucilage.” Colleters in the Rubiaceae are most commonly present on the internal surface of the stipules, usually at the basal portion, and are also frequently found inside
the calyx, at the base of the calyx lobes or in the sinuses between them.

In most Rubiaceae genera, the colleters are commonly present on the internal side of the stipules and secrete a resinous substance in variable amounts. In certain genera the secretion could be abundant, and sometimes might form a globose unit above the apical stipules (e.g., *Elaeagia* Wedd., *Retiniphyllum* Bonpl.), and/or covering the distal portion of young braches. This exudate is believed to protect the vegetative buds and the young distal internodes against herbivory.

In the Sipaneeae, colleters have been observed on the internal surface of the stipules, sometimes at the axils of terminal branchlets of the inflorescences, at the side of bracteoles, and in the sinuses of calyx lobes. For the presence of colleters in the calyces of Sipaneeae genera, see the Section *Calyx* (below).

The present section deals with the colleters present on the internal (adaxial) side or at the margin, or rarely at the tip of the stipules. Within the Sipaneeae, Steyermark (1964: 195), distinguished *Chalepophyllum* from *Dendrosipanea* by having, among other characters, a "glutinous exudate abundant and obvious in uppermost parts of the branches at the base of the petioles, pedicels, or peduncles" while he wrote that in *Dendrosipanea* the "glutinous exudate of branches [is] lacking or inconspicuous." However, he did not attempt to clarify the origin of the abundant exudate present in *Chalepophyllum* nor described the stipules of this genus.

Seyermark (1974: 384; translated from Spanish) reported that the stipules of *Limnosipanea* are "obsolete, interpetiolar, basal sheath adnate to the petioles and reduced to a seta or a solitary projection, with glands [i.e., colleters] inside." While for *Dendrosipanea*, *Maguireothamnus*, *Neblinathamnus*, *Sipanea*, and *Sipaneopsis*, Steyermark (1974) described only the shape and the external side of the stipules and did not mention the presence of colleters.

In most genera of the Sipaneeae, the stipules are small or reduced to a line between the nodes (*Limnosipanea*), and, aside from *Chalepophyllum*, no resinous secretion has ever been reported. Nevertheless, this does not exclude the production of a resinous exudate by the stipular colleters of genera with minute stipules. A simple explanation could be that, if present, the amount of secretion of minute stipules with a few colleters might be so minor that it has not been observed.

Presence and characteristics of colleters inserted on the internal surface or at the margin or rarely at the tip of the stipules in Sipaneeae genera is presented below.

**Chalepophyllum.** Stipules are free at base, broadly triangular to subtruncate (older stipules sometimes

becoming bifid at apex; Figure 1A-B), with the basal 2/3 covered by numerous dense colleters inside.

**Dendrosipanea.** Stipules are free or basally adnate to petioles, deltoid, acuminate or bifid (Figure 1C-D), with basal 2/3 covered by numerous dense colleters intermixed with hairs inside.

**Limnosipanea.** Stipules are reduced to a line between the petioles, sometimes obsolete, persistent, and withering on the stem with no abscission layer formed. They have 1-3 colleters inserted just below the margin, on the internal side, with the tips exerted beyond the stipule margin (Figure 1E). In stems with obsolete stipules, 1-2 colleters are inserted in the sinuses between the leaf bases. In submersed stems, stipules and colleters are absent.

**Maguireothamnus.** Stipules have a basal sheath adnate to the petioles, with the free portion narrowly triangular to linear (Figure 1F), sometimes with an apical colleter. A row of 3-7 colleters is present on each side, either inserted just below the margin or on the margin of the basal sheath.

**Neblinathamnus.** Stipules are basally adnate to the petioles, minute, broadly to shallowly triangular to truncate, sometimes shallowly bilobed, often bilobed at apex, or rarely constituted of two free lobes on each side of the stem (Figure 1K-L). A row of 7-9 sparse colleters is present at the margin of shallowly triangular to truncate stipules, or a row of 4-5 colleters is present at the margin of each lobe in bilobed stipules or in stipules constituted of two free lobes.

**Neobertiera.** Stipules are basally adnate with the petioles, broadly ovate, ovate, oblong-ovate or narrowly triangular, acuminate or bifid at apex (Figure 1G-H). Their inner side is pubescent and with numerous colleters either in a row or as two groups on each side at medio-basal portion.

**Pteridocalyx.** Stipules are basally adnate to the petioles, ovate to narrowly triangular, acuminate or bifid at apex (Figure 1I-J). The inner side has strigose hairs intermixed with colleters inserted at the medio-basal portion.

**Sipanea.** Stipules are sheathing at base or basally adnate to the petioles, truncate to broadly transversally elliptic, broadly to narrowly triangular, suborbicular, subulate, linear, or rarely setaceous, or reduced to a line between the petioles (Figure 2). Colleters are inserted on the internal side or along the margin; a few to several colleters are inserted on each side or irregularly spread near the base or at the median portion or just below the margin, or inserted along the margin. The presence and position of colleters for each section is described below.

**Sipanea section Sipanea** (corolla mouth with a ring of yellow hairs). In this section, the stipules are basally
adnate to the petioles, sheathing, with 2 colleters on each side of the central lobe in *S. galioides*, or with 3 colleters on each side of the central lobe in *S. glaberrima* (Figure 2A). In *S. glomerata*, 1–5 colleters are present on each side at the base of the central lobe, or sometimes 1–3 colleters are present near the apex of the linear lobe, either on the margins and/or at the tip. In *S. hispida*, the inner side of stipules has 5–6 colleters inserted just below the base of the central lobe, or 6–7 colleters are inserted just below the margin, often with exserted tips. In *S. pratensis*, 2–3 colleters are inserted at the margin on each side of the central lobe. In *S. veris*, 5–6 colleters are inserted along the stipular margin.

**Sipanea section Virecta** (corolla mouth with a ring of white hairs). In this section, stipules are adnate to the petioles, broadly triangular, shallowly obtuse to subacute (or very rarely bifid) at apex, or truncate, or with a central seta or two unequal setae in *S. setacea*, while the internal side and colleters have not been observed. In *S. biflora*, 2–6 colleters are inserted in a row near the base of the stipule. In *S. carrenoi*, 3–5 colleters are inserted on the median portion of the stipule. In *S. gleasonii*, 3–5 colleters are inserted at the median portion, or 7–10 colleters are irregularly distributed on the inner surface of the stipule. In both *S. micrantha* (Figure 2E) and *S. ovalifolia*, 3–5 colleters are inserted just below the margin, with the tips exserted beyond margin.

**Sipanea section Nudae** (corolla mouth glabrous or with sparse white hairs). In this section, stipules are also adnate to the petioles, and subulate, or broadly to narrowly triangular at base and narrowly triangular to linear distally, or very shallowly transversally ovate, or reduced to a line between the petioles. In *S. prancei*, 5–7 colleters are intermixed with a few hairs. In *S. saxicola*, 5–8 colleters are inserted in a row just below the margin (Figure 2I). In *S. stahelii*, 6–9 colleters are inserted in a row just below the margin or are concentrated just below the base of the central lobe. In *S. wilson-brownei*, 3–7 colleters are inserted at the base. In *S. ayangannensis*, the internal side of the stipules and the presence of colleters was not observed.

**Sipaneopsis.** Stipules in this genus are persistent, free or adnate to the petioles, or sometimes basally sheathing. The free portion is broadly to narrowly triangular, or broadly triangular at the base and linear or acuminate distally. They can also be bilobed or bifid at the apex, or topped by 2–4 linear lobes in *S. morichensis* and *S. rupicola* (Figure 3F–H). The colleters are inserted on the internal side at the medio-basal portion or just below the margin with their tips exserted, and range from 1 or 2 to 11. The stipules of *S. cururuensis* have just a few colleters at the base. In *S. duckei*, 4–7 colleters

inserted just below the margin with their tips exserted in the populations on Serra Aracá, or (1-)4–7 colleters inserted at the medio-basal portion in populations of Campos do Ariramba. In *S. maguirei*, 2–3 colleters are inserted just below the margin on each side of the central lobe. The stipules of *S. morichensis* have 6–7 colleters inserted just below the margin with their tips exserted; and those of *S. rupicola* have 10–11 colleters inserted just below the margin with their tips exserted. In *S. foldatsii* and *S. pacimoniensis*, the inner side of the stipules was not studied.

**Steyermarkia.** In this genus, the stipules are persistent, ovate or lanceolate to linear-lanceolate, attenuate or bifid at apex, densely white-hirsute outside. The inner side is covered with long, appressed hairs intermixed with numerous colleters; the colleters are linear, 2–2.3 mm long. In bilobed stipules, 1 colleter is present in the sinus between the lobes.

## Inflorescences

In this treatment, the terminology of inflorescence position and architecture follows the concepts of Troll (1950) and Weberling (1992). In addition, Weberling (1977) published an overview on the typology of inflorescences in the Rubiaceae, which is here followed.

Numerous Rubiaceae genera have terminal inflorescences with secondary branches subtended by leaf-like bracts (i.e., pherophylls). These leaf-like bracts are similar to foliage leaves, and are gradually smaller toward the distal portion of the inflorescence. In several instances, the presence of leaf-like bracts in terminal inflorescences has led some workers to incorrectly describe the inflorescences as lateral and cymose, instead of terminal, paniculate, and frondose. This argument was convincingly made by Troll (1950) and Weberling (1977, 1992). Steyermark (1974) described the inflorescences of *Sipanea* as “axillary or terminal, once or twice dichasially branched…” (Steyermark 1974: 357; translated from Spanish). In this genus, some species have inflorescence with the secondary branches subtended by leaf-like bracts (i.e., pherophylls), which Steyermark interpreted as axillary inflorescences subtended by leaves. In the present treatment, according to the definitions proposed by Weberling (1977, 1992), the inflorescences with secondary branches subtended by leaf-like bracts are treated as terminal and frondose.

Inflorescences in Sipaneeae may be terminal or truly axillary. Inflorescence position is consistent within each genus, and is an important diagnostic character that can be used to distinguish genera within the tribe. Within the Sipaneeae, they are axillary in *Chalepophyllum*,
*Maguireothamnus*, *Neblinathamnus*, and *Steyermarkia*, while they are terminal in the remainder of the genera. A discussion about inflorescence position and architecture by genus is presented below.

In *Chalepophyllum*, the inflorescences are axillary, reduced-cymose, and 1-7 flowered. The flowers of *Maguireothamnus* are solitary, axillary on distal nodes, and subtended by two leaf-like bracts. In *Neblinathamnus*, the flowers are axillary, 1-2 per axil, and subtended by two setaceous bracts. In *Steyermarkia*, the inflorescences are axillary, long-pedunculate, capitate, congested-cymose, with 3 head-like cymules, and 10-12-flowered.

In *Dendrosipanea*, the inflorescences are terminal or terminal on distal axillary branches, cymose, often frondose, and few- to many-flowered.

In *Limnosipanea*, the flowers are terminal and solitary, or in terminal, cymose, 2-4-dichotomous, few- to many-flowered inflorescences.

In *Neobertiera*, the inflorescences are terminal, many-flowered, subcapitate (extremely reduced cymes), densely glomerulate, densely cymose, or laxly cymose; in glomerulate and in densely cymose inflorescences, the lateral branches terminate with flower glomerules, while in laxly cymose inflorescences, the ultimate branches are scorpiod (more evident when fully expanded).

In *Pteridocalyx*, the inflorescences are terminal, cymose, many-flowered, and with scorpiod ultimate branches (more evident when fully expanded).

In *Sipanea*, the inflorescences are terminal, sometimes appearing axillary as a result of a reiteration of the axillary bud subtending the inflorescence, and paniculate, simply or compoundly cymose, or corymbose, usually not frondose, or in a few species they are frondose, with leaf-like bracts (i.e., pherophylls) subtending secondary branches, pauci- to multi-florous, or rarely uniflorous. In several species (e.g., *S. carrenoi*, *S. ovalifolia*, *S. pratensis* var. *pratensis*) the inflorescences are congested-cymose (appearing fasciculate) at initial stages, and either they remain so or they might slightly expand in later stages until fruit maturity. Whereas, in several other species (e.g., *S. hispida*, *S. pratensis* var. *dichotoma*, *S. stahelii*, *S. wilson-brownei*), the inflorescences are initially condensed-cymose (extremely shortly-branched, appearing fasciculate), and during and after anthesis the rachis elongates and the secondary branches expand from subcapitate to scorpiod. Later expansion of the inflorescence is generally treated as a variation at specific level, correlated with different stages of development, therefore not deserving subspecific rank, with the exception of *S. pratensis* (see below). Additional details about the inflorescences in *Sipanea* are discussed below in the three sections recognized in the genus.

In *Sipanea* section *Sipanea* (corolla mouth with a ring of yellow hairs), the inflorescences are cymose, dichotomously or trichotomously branched, or either a single condensed head or trichotomous with three condensed heads in *S. glomerata*, or 1-2-flowered in *S. veris*. In this section, the inflorescences do not expand or expand only slightly after anthesis, with the exception of *S. pratensis*. In this latter species, two varieties with allopatric distribution, and with different infructescences and fruit shapes, are here recognized: var. *pratensis*, with inflorescences that are initially congested-cymose (appearing fasciculate), and secondary branches that do not elongate in later stages, infructescences congested-cymose (appearing fasciculate), and globose, subglobose, ovoid to obovoid capsules; and var. *dichotoma*, with inflorescence axes that are already elongated in early stages or congested in early stages and elongated during and after anthesis, producing a subsecund monochasial cyme of dichasial appearance, often with scorpioid secondary branches, and capsules that are longer than broad, cylindrical-oblong to oblong-narrowly ovoid (See *S. pratensis* for further information).

In *Sipanea* section *Virecta* (corolla mouth with a ring of white hairs), the inflorescences are 1-7-flowered, condensed dichotomous cymes, monochasial, or rarely dichotomous in *S. biflora*, and do not expand or expand only slightly after anthesis.

In *Sipanea* section *Nudae* (corolla mouth glabrous or with sparse white hairs), the inflorescences are 3-32-flowered, cymose, dichomously branched, or modified dichasia, with 1-3 pairs of scorpioid lateral branches, and usually expanded after anthesis.

The inflorescences of *Sipaneopsis* are terminal, few-to many-flowered, congested-cymose in early stages (before anthesis), and slightly or much expanded and dichotomously branched during and after anthesis. In this genus, inflorescences range from reduced cymes of 2-3 flowers to compound dichasia, with scorpiod secondary branches, and from (12-)19-147-flowered. The smallest inflorescences in the genus are those of *S. pacimoniensis* Steyermark (1967: 289), which are 2-3-flowered cymes, and those of *S. maguirei* Steyermark (1967: 287), which are congested, 2-8(-13)-flowered cymes. The largest inflorescences are found in *S. huberi* Steyermark (1984c: 37, fig. 11), which has 31-147-flowered compound dichasia, with 5-9 pairs of secondary branches dichotomously branched.

## Flowers

In the Sipaneeae, flowers are commonly 5-merous. In the whole tribe, calyx lobes, corolla lobes, and sta-
mens are homomerous. In *Maguireothamnus*, flowers are exceptionally 6- or 7-merous. In *Limnosipanea*, a few flowers are exceptionally 4- or 6-merous. In *Sipanea*, flowers are commonly 5-merous, although in *S. galioides* they are exceptionally 6-merous, and in *S. pratensis* they might rarely be 4- or 6-merous. In some species of *Sipaneopsis*, a few flowers are exceptionally 6-merous. *Steyermarkia* is exceptional within the tribe by having flowers consistently 4-merous.

*Heterostyly*

Schumann (1889, p. 247), in *Flora Brasiliensis*, was the first author to report heterostyly in a member of the Sipaneeae by describing *Sipanea* as having “flores actinomorphi pentameri heterostyli.” [flowers actinomorphic, pentamerous, heterostylous]. In the same publication, he also asserted that *Chalepophyllum* and *Limnosipanea* (Schumann 1889, pp. 245 and 252, respectively) are homostylous; however, the former is here shown to be heterostylous, while the latter is here confirmed to be homostylous.

Brown (1901) in the original description of *Chalepophyllum speciosum* N.E.Br. [= *Maguireothamnus speciosus* (N.E.Br.) Steyerm.], described the style as “about as long as the corolla tube, or shorter than the anthers or rarely exserted” and just below explained that “The variation in the length of the style would seem to imply that the flowers are heterostyled, but it may be due to a lengthening at various periods of development.” His explanation is correct, because he described the style at various stages of development, and this species, currently accepted as part of the genus *Maguireothamnus*, is homostylous, and with the style exserted well beyond the corolla mouth when fully expanded and receptive (i.e., with style branches separated from each other).

Verdcourt (1958) confirmed the presence of heterostyly in a genus of the Sipaneeae, by saying that “some species of *Sipanea* have the anthers at different heights in the corolla tube”.

Steyermark (1964: 192–193) in the emended description of *Chalepophyllum guyanense* var. *guyanense* wrote “tubo [corolla] 10–16 mm longo [...] stylis 5.5–13 mm longis; staminibus prope medium vel supra medium corolla insertis [...]” [corolla tube 10–16 mm long, [...] style 5.5–13 mm long; stamens inserted at the middle or above the middle of the corolla tube] and in that of *C. longilobum* Steyermark (1964: 193) wrote “tubo [corolla] 13–14 mm longo [...], filamentis liberis 2 mm longis paullo supra medium corollae tubi insertis ad basin adnatis; stylis 6–13 mm [...].” [corolla tube 13–14 mm long [...], filaments free, 2 mm long, inserted just above

the middle of the corolla tube, adnate at base; style 6–13 mm long, glabrous; [...].

Bremekamp (1966) described the tribe Sipaneeae, where he included *Sipanea*, *Virecta* Vahl [= *Sipanea*], and *Limnosipanea*; however, he did not mention the presence of heterostyly in the tribe. Bahadur (1968: 220) published an overview of heterostyly in the Rubiaceae in which he cited the flowers of *Sipanea* as “dimorphic, Verdcourt (1958).”

Steyermark (1974: 323) in *Flora de Venezuela*, described *Chalepophyllum guyanense* as having filaments inserted at the middle or at the distal ¾ of the corolla tube. In the same publication, Steyermark (1974: 357) described *Sipanea* as having (translated from Spanish) “Stamens 5, included, inserted below or above the middle of the tube, rarely near the mouth” and reported only *S. pratensis* as a heterostylous species of the genus by having “Stamens included, 2/3 to 3/4 of the total length of the [corolla] tube from the base or at the distal part of the tube; anthers linear or linear-fusiform, 2.2–3 mm long; filaments 0.4–1.5 mm long, glabrous, inserted on tube at 3.5–8 mm below the [corolla] mouth. Style 5–19 mm long, glabrous.” (Steyermark 1974, p. 371, translated from Spanish). Therefore, although Steyermark (1964, 1974) reported for both *Chalepophyllum* and *Sipanea* that the stamens are inserted at different heights on the corolla tube and the style is either included or exserted, he did not explicitly state that these genera are heterostylous.

Robbrecht (1988, fig. 48) in the bubble diagram illustrating his Rubiaceae classification, indicated that heterostyly is present in the Sipaneeae, probably referring to the distyly reported in *Sipanea* by previous authors (Verdcourt, 1958; Bahadur, 1968; Steyermark, 1974).

As a result of recent studies, Delprete (2015a, 2018, 2019a, 2019b) observed that in the Sipaneeae, heterostyly is present in several genera. In addition, presence or absence of heterostyly is consistent in all the genera, and can be used as a diagnostic character to distinguish them. Within the tribe, the genera *Limnosipanea*, *Maguireothamnus*, *Sipaneopsis*, and *Steyermarkia* are consistently homostylous, with exserted or partially exserted style when fully elongated and receptive (i.e., branches spread apart from each other).

Within the Sipaneeae, the genera *Chalepophyllum*, *Dendrosipanea*, *Neobertiera*, *Pteridocalyx* and *Sipanea* are heterostylous. In *Dendrosipanea*, *Neobertiera*, and *Sipanea*, most species were observed to be distylous, although in a few of them only the long-styled or the short-styled flowers were examined, due to lack of available material. However, it was assumed that the five above-cited genera are entirely heterostylous. The heterostylous genera of the Sipaneeae are discussed below.
In *Chalepophyllum*, the short-styled flowers have stamens inserted at the upper portion of the corolla throat and are included, and the style is short and included. While in long-styled flowers, the stamens are inserted at medio-basal portion of corolla throat and are included, and the style is exserted well beyond corolla mouth.

The distylous condition of *Dendrosipanea* was first observed by Delprete (2018) in both *D. revoluta* and *D. spigelioides*. In short-styled flowers of these two species, the stamens are included, with filaments inserted at the distal portion of corolla throat and linear anthers, while the style is much shorter than the corolla tube. In long-styled flowers, the stamens are also included, although the filaments are inserted at the distal portion of the corolla throat and the anthers are also linear, while the style is barely exserted, with only the branch tips exserted beyond the corolla mouth. Ducke (1935) in the original description of *Dendrosipanea* wrote that the filaments are inserted at the middle of the corolla tube and the style is as long as the corolla tube; therefore, he based the original genus description on long-style flowers of the type specimen of *D. spigelioides*.

Steyermark (1964: 198, fig. 72a-g) described *Dendrosipanea wurdackii* Steyerm. as having the style 3-3.5 mm long with branches 2-2.5 mm long. He distinguished it from *D. spigelioides* by other characters, a "much shorter style not reaching the height of the anthers." Therefore, Steyermark's description of *D. wurdackii* is based on the short-styled flowers of the type gathering (Maguire & Wurdack 35558), and, in agreement with Delprete and Steyermark (2004a), these two taxa are conspecific.

Delprete (2018) recently described *Dendrosipanea prancei* Delprete from three collections. In all of them the style is barely exserted beyond the corolla mouth, and the stamens are inserted the basal portion of the corolla tube, with the anthers presented at the medio-distal portion of the corolla tube. As the other two species of the genus are distylous, the three collections of *D. prancei* were interpreted as long-styled, and this species is also distylous.

Wernham (1917) described *Neobertiera* with a sole species, *N. gracilis* Wernham, using a single specimen (Jenman 2388, BM). He assumed that its flowers are homostylous and wrote "Stamina 4 [sic, 5], infra corollae fauces inserta; anthereae in tergo prope basin tamen in filamentum latum longiusculum fixae, lanceolato-oblongae" [Stamens 4 [sic, 5], inserted at corolla mouth; anthers dorsally attached on long filaments, oblong-lanceolate]. The flowers of the holotype specimen correspond with Wernham's description in having stamens inserted at the medio-distal portion of the

corolla, with rather long filaments and anthers presented near the corolla mouth. Following Wernham's original description, *Neobertiera* has been reported by Sandwith (1931) and Steyermark (1967) as monospecific and homostylous. However, Delprete (2015a, 2019b) recently described four additional species in *Neobertiera*, and stated that out of the five species in the genus, four are distylous and one is tristylous. The heterostyly in each species of this genus is discussed below.

The distyly of *Neobertiera gracilis* has been observed in numerous herbarium specimens. In long-styled flowers, the filaments are short and inserted at the medio-basal portion of the corolla tube and, the style is about the same length or slightly longer than the corolla tube (Delprete, 2015a, fig. 6E). In short-styled flowers, the filaments are long and inserted at the medio-distal portion of corolla tube, and the style is much shorter than the corolla tube (Delprete, 2015a, fig. 6D). Therefore, Wernham's original description of this species was made studying the short-styled flowers of the holotype specimen.

*Neobertiera palustris* is the only species observed by Delprete (2015a, as *N. glomerata* Delprete) to be tristylous in the Sipaneeae. One form of long-styled flowers has stamens inserted at about the middle of corolla tube, with narrowly sagittate anthers, and the style is slightly shorter than the corolla tube (Delprete 2015a, fig. 3C). In the other form of long-styled flowers, the stamens are inserted near the base of corolla tube, also with narrowly sagittate anthers, and the style is about as long as the corolla tube, with the branch tips barely exserted (Delprete 2015a, fig. 3D). In short-styled flowers, the stamens are inserted above the middle of the corolla tube, with linear anthers, and the style is much shorter than the corolla tube (Delprete 2015a, fig. 3E).

In *Neobertiera micrantha* Delprete, *N. pakaraimensis* Delprete, and *N. montedouradensis* Delprete, only the long-styled flowers were observed (Delprete 2015a, 2019a), as these species are only known by the type specimens (*Cremers & Granville 14097*, Henkel et al. 1449, and *Santos 414*, respectively). In these specimens, the stamens are inserted at about the middle of the corolla tube, and the anthers are narrowly sagittate in *N. micrantha* and *N. pakaraimensis* or linear in *N. montedouradensis*, while the style is about as long as the corolla tube in the former two species, or slightly longer, with the branch tips barely exserted, in *N. montedouradensis*. Because the stamen insertions and the proportion of the style with the corolla tube of these three species resemble the long-styled flowers of *N. palustris* and *N. gracilis* and are assumed to be distylous, although the short-styled flowers have not yet been observed.
Delprete (2019a, fig. 1), as a result of field observations of natural populations and the study of numerous herbarium specimens, concluded that *Pteridocoxyx* is distylous. In long-styled flowers the stamens are included and inserted near the base of corolla tube, with anthers 1.8–2 mm long, and the style is about the same length as the corolla tube (with the tip of branches barely exserted) or exserted just beyond corolla mouth. In short-styled flowers, the stamens are inserted at the distal portion of corolla tube, included, and with anthers 2.5–2.7 mm long, and the style is about half the length of the corolla tube.

*Sipanea* is the most diverse and most widely distributed genus of the tribe, and displays the widest variation in corolla shape and dimensions. In *Sipanea*, most species were observed to be distylous, although in a few species only the long-styled or only the short-styled flowers were examined, due to the lack of available material. Generally, in long-styled flowers the stamens are inserted near the base or at the middle of the corolla tube, and the style is as long as the corolla tube or exserted. In short-styled flowers the stamens are inserted at the middle or at the medio-distal portion of the corolla tube, and the style is shorter than the point of insertion of the stamens. The term medium-styled flowers is here introduced, observed in *S. hispida*, for flowers that have the stamens inserted in lower-median portion of the corolla tube, just below the tips of the style branches, and the style is about half the length of the corolla tube, equal in height with the middle or upper tip of the anthers. Three sections are here recognized within *Sipanea*, and the various aspects of distyly are discussed below under each section.

*Sipanea* section *Sipanea* is characterized by flowers with a ring of yellow hairs at the corolla mouth. Within this section, *S. galioides*, *S. glomerata*, *S. pratensis* and *S. veris* were observed to be distylous. In the long-styled flowers of these species, the stamens are inserted about the middle of the corolla tube, and the style is exserted beyond the corolla mouth. While in short-styled flowers the stamens are inserted at the distal portion of the corolla tube, and the style is much shorter than the point of insertion of the stamens.

In *Sipanea hispida*, a member of section *Sipanea*, in short-styled flowers, the stamens are inserted at medio-distal portion of the corolla tube, just above or at the same height as the tips of the style branches, and the style is shorter than the stamen insertions on the corolla tube. Whereas, in medium-styled flowers the stamens are inserted below the tips of the style branches, at about the middle of the tube, and the fully elongated style equal in height to the middle or upper tips of the

anthers, which are inserted at the median portion of the tube.

For five species of *Sipanea* section *Sipanea*, distyly remains to be confirmed, due to the lack of available material. In *S. glaberrima* (Bremek.) Steyerm., known only from the type, only short-styled flowers were observed, with stamens inserted just below the corolla mouth, and a short, included style. In *S. micrantha* Sandwith (1928: 378), known from three collections, only long-styled flowers were observed, with stamens inserted near the base of corolla tube, and the style about as long as the corolla tube. In *S. setacea* Steyerm., also know only from the type, only long-styled flowers were examined, with stamens inserted at medio-distal portion of tube, and style slightly exserted beyond the corolla mouth.

Species of *Sipanea* section *Virecta* are characterized by a ring of white hairs at the corolla mouth. Within this section, only *S. biflora* and *S. ovalifolia* are here confirmed to be distylous, following the observations of numerous specimens from throughout their distribution range. In both species, the long styled flowers have stamens inserted at the lower portion of the corolla tube, and style about as long as corolla tube (tip of branches exserted) or exserted beyond corolla mouth. In short-styled flowers the stamens are inserted at the distal portion of the corolla tube, and the style is much shorter than the corolla tube.

Within *Sipanea* section *Virecta*, only the long-styled flowers of *S. carrenoi* Steyerm., known only from the type, *S. micrantha*, known from three collections, and *S. setacea*, known only from the type, were observed, due to the paucity of material available. In these three species, the flowers observed have the stamens inserted at the basal (*S. micrantha*) or medio-distal (*S. carrenoi* and *S. setacea*) portion of the corolla tube, and the style is about the same length as corolla tube or exserted beyond the corolla mouth. In *Sipanea gleasonii* Steyerm., also know only from the type, only short-styled flowers were observed, with stamens inserted just below the corolla mouth, and the style much shorter than the corolla tube.

Species of *Sipanea* section *Nudae* are characterized by the corolla mouth glabrous or with a few sparse white hairs. Within this section, only *S. stahelii* Bremek. and *S. wilson-brownei* Cowan were observed to be distylous, based on analyses of numerous herbarium specimens. In both species the long-styled flowers have stamens inserted at the basal portion of corolla tube, and the style is about the same length or slightly longer than the corolla tube. While in short-styled flowers the stamens are inserted at distal portion of corolla tube, and the style is much shorter than the corolla tube. Within this sec-
tion, for *S. ayangannensis* Steyerm., only known from the type, and *S. saxicola* J.H.Kirkbr., known from a few collections, only short-styled flowers are known, which have stamens inserted at medio-distal portion of the corolla tube, and the style much shorter than the corolla tube.

In *Sipanea prancei* Steyerm., also of *Sipanea* section *Nudae*, only the flowers of three collections were analyzed, due to the paucity of material available. In these flowers, the stamens are inserted at about the middle (1/2 or 3/5 from the base) of the corolla tube, and the style is slightly longer than the point of insertion of the stamens. However, in all of them the style is not completely elongated and the branches are still appressed against each other (i.e., not opened). Therefore, additional specimens with styles completely elongated are needed, to confirm the distyly of this species.

## Flowering modality

In all genera of the Sipaneeae, except for *Sipaneopsis* (see below), the corolla lobes open after the corolla tube is completely elongated, and the reproductive parts are subsequently available to pollinators. In all genera of the tribe, the flowers are protandrous, with the anthers maturing, dehiscing, and releasing pollen before the style is completely elongated. After the pollen has been released, the style expands to full length and the branches spread apart from each other, exposing the stigmatic surfaces on the adaxial side.

The flowering modality of *Sipaneopsis* is unique within the Rubiaceae and was described in detail by Delprete (2015a, 2017). In Figures 80B–C is an inflorescence of *S. maguirei* with flowers at different developmental stages. During the initial stage of anthesis the flowers are very small but the corolla lobes are already open and erect, although not fully expanded, before tube elongation (Figure 82A–B). At this stage, the triangular appendages present at the base of the corolla lobes are appressed against each other, forming a convex structure at the corolla mouth (Figure 82A–B), obstructing the entrance of any visitors or pollinators. During successive stages of anthesis, the corolla tube and lobes elongate, and the corolla lobes remain erect and the corolla lobe appendages are still appressed against each other (Figure 82C–F), continuing to obstruct the entrance of any visitors or pollinators. At the final stage of anthesis, the corolla lobes reflex and become perpendicular to the tube, corolla hypocrateriform, and the corolla lobe basal appendages become erect, not touching each other (Figure 82G–H), allowing visitors and pollinators to access the corolla tube and nectar disk. More details about the

flowers modality of this genus are discussed and illustrated in *Sipaneopsis* (see below).

## Hypanthia

All genera of the Sipaneeae, as in most Rubiaceae genera, have an inferior ovary. Following Radford et al. (1974: 99), the hypanthium is “the fused or coalesced basal portion of floral parts (sepals, petals, stamens) around the ovary.” Therefore the external portion surrounding the ovary (i.e., below the calyx) should be called the hypanthium, although some specialists erroneously call this external portion the “ovary”.

In the Sipaneeae, hypanthia vary in shape from globose, obovoid, narrowly obovoid, obconical, turbinate or rarely subcampanulate-urceolate (in one species of *Sipaneopsis*), and are considerably variable in dimensions (see below).

Vestiture of hypanthia in this tribe is also quite variable, as they can be glabrous, or minutely puberulent, densely pubescent, strigillose, strigose, hispidulous, hispid, or sericeous. Trichomes are most commonly simple (i.e., not basally tuberculate) in most species of the tribe. Exceptionally, hairs are basally tuberculate in several species of *Sipanea* (e.g., *S. hispida*, *S. gleasonii*, *S. ovalifolia*, *S. stahelii*, and *S. wilson-brownei*), and in *Neobertiera montedouradensis*. In these species, the tubercle is multicellular, and surrounds the base of the central hair.

In *Chalepophyllum*, the hypanthia are obconical or turbinate, 1–1.5 × 1–1.3 mm, and glabrous or minutely puberulent. In *Dendrosipanea*, the hypanthia are obconical, turbinate to narrowly obovoid, 1.5–3 × 1.2–2.5 mm, and glabrous or strigillose. In *Limnosipanea*, the hypanthia are narrowly ellipsoid to narrowly obovoid, 0.3–1 × 0.2–1.3 mm, and densely hispid. In *Maguireothamnus*, the hypanthia are oblong-obconical, obconical, narrowly obconical to narrowly obovoid, 2–6 × 1.5–5 mm, and glabrous, minutely puberulent, densely pubescent, antrorse-hispidulous, antrorse-hispid to densely spreading strigose. In *Neblinathamnus*, the hypanthia are obovoid, oblong-ovoid, turbinate or narrowly obovoid, 1.8–2.5 × 1.4–2 mm, and sparsely to densely hirtellous.

In *Neobertiera*, the hypanthia are globose, broadly obovoid to obovoid, 0.5–1.5 × 0.5–1.5 mm, with appressed-strigose, simple trichomes (i.e., not basally tuberculate) in most species. *Neobertiera montedouradensis* is unique within the genus by having hypanthia and fruits with trichomes basally tuberculate.

In *Pteridocalyx*, the hypanthia are oblong-obovoid, 1.5–2 × 1.1–1.3 mm, and appressed strigose-pubescent.

In *Sipanea*, the hypanthia display a wide range of size, shape and vestiture. In most species the trichomes
on the hypanthia are simple (i.e., not basally tuberculate. In a few species, in each of the three sections, the hypanthia have trichomes with basal multi-cellular tubercules. Hence, size, shape, vestiture and kind of trichomes of the hypanthia offer an important set of diagnostic characters, and these features are discussed below within each of the three sections recognized in the genus.

In *Sipanea* section *Sipanea* (corolla mouth with a ring of yellow hairs), the hypanthia are obconical, obovoid, turbinate to narrowly obovoid, 0.7–5 × 0.5–2.5 mm, glabrous or sparsely to densely antrorse setose-strigulose, appressed pubescent, densely antrorse hispid sericeous or densely appressed-strigillose; the hairs are simple (i.e., not basally tuberculate).

In *Sipanea* section *Virecta* (corolla mouth with a ring of white hairs), the hypanthia are subglobose, broadly to narrowly obovoid or obconical, 0.7–2.5 × 0.7–1.5 mm, glabrous or with a few appressed hairs, sparsely appressed-strigillose on the distal half and glabrous below, appressed-strigillose throughout or densely antrorse hispid-strigose. In most species of this section, the trichomes on the hypanthia are simple (i.e., not basally tuberculate), with the exception of *S. gleasonii* and *S. ovalifolia*, which have hypanthia with basally tuberculate trichomes.

In *Sipanea* section *Nudae* (corolla mouth glabrous or with sparse white hairs), the hypanthia are globose, subglobose, broadly turbinate, narrowly obconical, narrowly ovoid to obovoid, 0.7–2 × 0.5–2 mm, densely antrorse-strigose, densely antrorse-pubescent, densely erect-sericeous, densely antrorse-pubescent, or appressed strigose-pubescent. Within this section, *S. stahelii* and *S. wilson-brownei* are exceptional in having hypanthia with basally tuberculate trichomes.

In *Sipaneopsis*, the hypanthia are subglobose, globose, broadly turbinate, turbinate, subcampanulate-urceolate, broadly-obovoid, obovoid-turbinate, obconical or oblong-obovoid, 1–2 × 0.8–1.7 mm, scabrous, densely hispid, densely hispidulous strigillose, densely to sparsely strigose, sericeous-strigose or sericeous.

In *Steyermarkia*, the hypanthia are turbinate, 1.5–2 × 1–1.5 mm, and densely antrorse-hispid. The hairs are long, white, and simple (i.e., not basally tuberculate).

## *Calyces*

In the Sipaneeae, the calyx lobes are commonly free, with an extremely reduced the calyx tube, or sometimes shallowly connate at the base, and persistent on the fruit or sometimes breaking off in old fruits.

Regarding calcine colleters in Rubiaceae, Robbrecht (1988) wrote that “The inside of the calyx is beset

with colleters of the same type of those of the stipules. Colleter number and position is diverse. They may cover the entire inside or only a part of it, occur in a ring all around the inside of the calyx-base, or be limited to small groups (sometimes isolated colleters) on the inside between or at the margin of the lobes.” Additional information about colleters is available in the section *Colleters*.

In all genera of the Sipaneeae, one to several colleters are inserted at the calyx lobe sinuses, either on both sides of the lobe bases or at the middle of the sinuses, usually just below the margin of each sinus, on the internal side. Hooker (1868) was probably the first specialist to report calcine colleters in members of the Sipaneeae, as he described the calyx lobes of *Limnosipanea* as “lanceolate, subfoliaceis, intus basi glandulose, persistentes” and in figure 4 of plate 1050, of the same publication, is depicted a dissected flower with colleters at the base of the calyx lobes.

Schumann (1889), in *Flora Brasiliensis*, also reported calcine colleters in several members of the Sipaneeae. He wrote that the calyx of *Sipanea* is “fere ad basin in lacinias elongates basi denticulo glandulose solitario interpositas divisus persistens, tubo intus eglandulosus” [with a solitary small glandular tooth inserted approximately near the base at sinus of calyx lobe, tube non glandular inside], and that the calyx of *S. pratensis* and *S. biflora* have a “denticulo solitario glanduloso interjectas diviso.” [a solitary small glandular tooth at sinus between calyx lobes] (Schumann, 1889, pp. 247–251). For *Limnosipanea*, he stated that the calyx lobes have a “denticulo solitario glanduloso interposita, inferne breviter coadunate persistentia intus eglandulosa.” [a solitary small glandular tooth at lobe sinus, lobes basally connate, inner side non glandular] (Schumann 1889, p. 252). He also reported calcine colleters in *Sipaneopsis rupicola* (K.Schum.) Steyerm. (as *Rondeletia rupicola* K.Schum.) by describing its calyx as “fere ad basin in lacinias ovarium paulo superantes subulatas inaequialongas denticulis solitaris vel binis interpositas extus ad nervam medianum pilosulas ciliolatas divisa” [calyx lobes connate at base, slightly longer than the “ovary” [hypanthium], unequal, with one or two small teeth at sinus, with a pilose-ciliolate middle vein] (Schumann 1889: 222 [incorrectly numbered “224”]).

Steyermark (1967, 1974, 1984a, 1984b, etc.) reported the presence of colleters at the calyx lobe sinuses in the species descriptions of *Neobertiera*, *Sipanea*, and *Sipaneopsis*, and called them “glándulas”, “glands”, “glandulae”, “squamellae” or “esquamelas”. The latter two terms are rather awkward for describing colleters, as the proper Spanish term for these secretory structures is “coléteres”
(Font Quer 2000), whereas squamellae are small scales without secretory function (Stearn 1995).

Steyermark (1967: 284–289), along with the emended description of *Neobertiera*, distinguished this genus from *Sipanea* by, among other characters, “The calyxine squamellae [i.e., colleters] do not arise at the sinus [in *Sipanea*] but at the base on either side of the calyx-lobe, thus two squamellae are evident between the calyx-lobes.”

The variation in calyx lobe size and shape, as well as number, point of insertion, and characteristics of the colleters at lobe sinuses, provide a significant set of diagnostic characters that can be used to distinguish genera and species in the Sipaneeae. These characters are discussed below for each genus.

In *Chalepophyllum*, the calyx lobes are subequal to unequal, oblong-triangular, ovate-lanceolate, oblong-lanceolate, lanceolate, or elliptic to oblong-spathulate, 2–17 × 1–3.5 mm; just below each lobe sinus, on the internal side, is inserted a fascicle of 3–5, oblong to linear, 0.25–0.5 mm long colleters.

Ducke (1935: 69; liberal translation from Latin) described the calyx of his new genus *Dendrosipanea* as “persistent, short, divided to the base into erect-patent lobes, with fascicles of minute glands [i.e., colleters] alternate to the lobes.” In fact, in *D. spigelioides* Ducke, the calyx lobes are deltoid to narrowly triangular, with fascicles of 2–4 colleters at each lobe sinus. In *Dendrosipanea*, currently recognized as a genus of three species (Delprete 2018), the calyx lobes are subequal to unequal, deltoid, narrowly triangular, oblong, narrowly oblong, lanceolate, or spathulate, 1–9 × 0.7–3.5 mm, and at each lobe sinus there are 1–4 colleters, linear, 0.3–0.5 mm long.

In *Limnosipanea*, the calyx lobes are subequal, oblong, lanceolate to linear, 1.5–5.5 × 0.3–0.6 mm, aristate at apex (arista caducous) or not. On the internal side, in each calycine sinus, there is one colleter broadly conical to conical, 0.05–0.1 mm long.

In *Maguireothamnus*, the calyx lobes are subequal or unequal, large, elliptic, narrowly-elliptic, oblong, narrowly lanceolate to linear, 8–23 × 1.5–7 mm, attenuate, acute or acuminate at apex; in each calycine sinus, there is a fascicle of 5–7 colleters, narrowly-lanceolate to oblong-lanceolate, 0.4–0.7 mm long.

In *Neblinathamnus*, the calyx lobes are equal to subequal, spathulate, lanceolate, linear-acuminate, or linear-spathulate, 4–7 × 0.3–1 mm, acuminate, subacute to obtuse at apex; at each lobe sinus, there are 2 or 3 colleters, linear, 0.2–0.3 mm long.

Wernham (1917) in the original description of *Neobertiera* did not mention the presence of calycine

colleters. Steyermark (1967: 289) emended the description of the genus, and, among other characters, added “inter lobos basi intus utriusque lateris glandulis duabus interpostis.” In *Neobertiera*, the calyx lobes are commonly unequal, narrowly-lanceolate, linear-lanceolate to narrowly lanceolate, 1.5–5 × 0.2–1.1 mm, acute at apex. In each calycine sinus, there are 1 or 2 colleters, oblong, 0.1–0.25 mm long.

In *Pteridocalyx*, one or two calyx lobes per flower are expanded, petaloid (i.e., calycophylls), stalked, with blades ovate to narrowly ovate, white, and palmately-veined (see Section Calycophylls, below); while the not-enlarged calyx lobes are subequal, small, linear to linear-lanceolate, 2–4.5 × 0.4–0.7 mm long, and acute at apex. Wernham (1911, 1913) did not mention the presence of calycine colleters in his descriptions of the two species of *Pteridocalyx*. This genus is currently treated as monospecific (Delprete 2019a), and on the calyx there are 1 or 2, oblong, 0.15–0.2 mm long colleters at each lobe sinus.

*Sipanea* is the most diverse and geographically most widespread genus of the Sipaneeae. Accordingly, calyx lobes in *Sipanea* display a wide variation in shape and size. They can be equal, subequal or unequal, and sometimes they vary within the same species from oblong-lanceolate, lanceolate, subulate, linear to setiform, 1.3–13 × 0.1–1.2 mm, and are acute or acuminate at the apex. The smallest calyx lobes in the genus are found in *S. micrantha*, 1.3–1.7 × 0.2–0.3 mm, and the largest ones are those of *S. glomerata*, 7–13 × 0.7–1.2 mm, expanding to 15–17 mm long on the fruits. The shape and size of calyx lobes provide some useful diagnostic characters to identify several species within the genus.

Steyermark (1967) indicated the presence of a solitary colleter in calycine sinuses, using the term “glandula” in the Latin descriptions of several *Sipanea* species: in *S. cowanii* Steyerm. [= *S. biflora* (Rottb.) Cham. & Schltdl.] as “inter lobos in sinus glandula solitaria subovoida obtusa 0.05–0.1 mm longa disco breviori interposita” (Steyermark 1967: 265), in *S. gleasonii* Steyerm. as “inter lobos in sinus glandula solitaria ca. 0.1 mm longo interposita” (Steyermark 1967: 266), in *S. stahelii* Bremek. as “inter lobos in sinus glandula solitaria subulata 0.1–0.2 mm longa disco breviori interposita” (Steyermark 1967: 269), in *S. glaberrima* (Bremek.) Steyerm. as “inter lobos glandula solitaria subulata 0.4–0.5 mm longa apicem disci aequanti interposita” (Steyermark 1967: 270), and in *S. pubinoda* Steyerm. [= *S. pratensis* var. *dichotoma*] as “inter lobos in sinus glandula solitaria 0.2 mm longa interposita” (Steyermark 1967: 278). Steyermark (1974) also cited the presence of calycine colleters in the descriptions of several species of *Sipanea* in the *Flora de Venezuela*, where he called them, in Spanish,
"esquamelas" (see comments about the use of this term in section *Colleters*, above). In all species of *Sipanea*, in each calycine sinus there are 1 or 2 colleters 0.1 to 0.5 mm long, which vary in shape from conical (obtuse at apex), narrowly conical (acute at apex), linear to setiform.

In *Sipaneopsis*, the calyx lobes are equal or subequal, and vary from ovate, narrowly ovate, narrowly lanceolate to linear-lanceolate, 1.5-3 × 0.2-0.7 mm, acute at the apex. Calyx lobes in *Sipaneopsis* do not have an ample range of shape and dimensions, and, aside from their vestiture, do not provide any useful characters for the identification of the species.

Steyermark (1967) reported the presence of calycine colleters (as "glandula" or glandulae"; see comments about the use of this term in section *Colleters*, above) in all the species of *Sipaneopsis* known to him, as follows (translated from Latin): 1 colleter, lanceolate, acute, 1/5 of calyx lobes length in each calycine sinus of *S. rupicola*; 1 or 2 colleters, lanceolate, ca. 1/10 calyx lobes length in each calycine sinus in *S. morichensis*; 1 colleter, 0.1 mm long, in each calycine sinus of *S. maguirei*; 1 colleter, 0.1 mm long, on each side of each calyx lobe of *S. wurdackii*; 1 colleter on each side of the calyx lobes of *S. foldatsii*; and 1 colleter, 0.1-0.2 mm long, in each calycine sinus of *S. pacimoniensis*.

Following recent detailed observations, in all species of *Sipaneopsis*, in each calycine sinus, there are 1 or 2 colleters, 0.2-0.3 mm long, which vary in shape from narrowly conical, ellipsoid, narrowly ellipsoid, narrowly oblong to narrowly cylindro-conical, and acute at apex.

In *Steyermarkia*, the calyx tube is extremely reduced, 0.5-1 mm long, and the lobes are erect, narrowly ovate-lanceolate to linear-lanceolate, 10-15 × 1-1.5 mm. In each calycine sinus there is one linear colleter, 0.7 mm long.

## Calycophylls

Calycophylls are enlarged calyx lobes that serve to attract pollinators and/or function as an aid for seed dispersal (Delprete 1996a, 1996b, 1996c, 1997, 1998a, 1998b, 2019a). A succinct overview of Rubiaceae genera with calycophylls was presented by Delprete (2019a). In flowers with semaphyllous calycophylls, calyx lobes are fully expanded during anthesis and have the function of attracting pollinators, and can be of various colors, ranging from white to greenish-white, yellow, pink, orange, red to purplish-red. They commonly lose their pigmentation when still present after anthesis, or change or rarely maintain their pigmentation after anthesis, and they may fall off before seed dispersal. Semaphyllous cal-

ycophylls, when persistent after anthesis and associated with dehiscent capsules, might have a secondary function of helping to shake the capsules, therefore contributing to the dissemination of wind-dispersed seeds.

In flowers with pterophyllous calycophylls, one, several or all calyx lobes are small or slightly larger during anthesis (sometimes functioning as semaphylls) and expand during fruit ripening, and are associated with indehiscent fruits, e.g., *Cosmocalyx* Standl., *Jackiopsis* Ridsdale, *Nematostylis* Hook.f., and some species of *Alberta* E.Mey. At fruit maturity they are fully expanded and form a wind-dispersed unit with the indehiscent fruit, and therefore they are not analogous to semaphyllous calycophylls.

*Pteridocalyx* is the only genus with calycophylls in the Sipaneeae. A detailed account on the calycophylls of this genus was presented by Delprete (2019a). In *Pteridocalyx*, 1 or 2 calyx lobes per flower are expanded, petaloid, and palmately veined (i.e., calycophylls). Regular small calyx lobes, as well as the calycophylls, are pure white when fresh, and turn cream-white to beige on dried specimens. Calycophylls in *Pteridocalyx* can vary in size and shape on the same inflorescence or even on the same calyx (Figures 36, 37, 39). The smaller calycophylls (Figure 39C-E) do not have a distinguishable stalk, and are linear, narrowly oblanceolate to narrowly oblong-oblanceolate, 4.5-9.5 × 0.8-1.5 mm, and are 1-3-veined, including the midrib. The larger calycophylls (Figure 39A-B) have stalks 2-5 mm long and blades narrowly elliptic elliptic to ovate, 4-13 × 5-9 mm, which can be acute, obtuse to round at base, and acute to obtuse at apex, and are palmately-veined, with 5-7 veins (including midrib). During anthesis, they are pure white and act as an aid for pollinator attraction, hence, they are semaphyllous calycophylls. After anthesis and during fruit development, they turn cream-white to yellowish-white. As they dry on the fruit, they commonly break off before capsule dehiscence, or might persist on the capsule, hence helping in seed dispersal by shaking the capsules.

## Corollas

Corollas in the Sipaneeae display a wide range of dimensions. Corolla shape and dimension supply an important set of diagnostic characters to differentiate genera in the tribe. Also, as corolla size, shape and proportions between corolla tube and lobes are variable among species of the same genus, they are a helpful set of characters that can be used to differentiate species.

Corollas in the Sipaneeae are actinomorphic. The most common corolla shape in the tribe is hypocrateri-
form, except several species of *Sipanea* section *Virec-
ta*, and *Chalepophyllum* (see below). Corolla lobes are
left-contorted in all genera, except for a few species of
*Sipaneopsis*, which might have imbricate aestivation (see
below).

In *Chalepophyllum* (1 sp.), the corollas are infun-
dibuliform, 17–31 mm long, white to cream-white,
sometimes with tube reddish or greenish at base. The
tubes are obconical, 10–16 mm long, much wider at
the mouth, externally strigose, internally pubescent
throughout or only at the mouth, densely yellow-pubes-
cent at the mouth inside. The lobes are ovate, narrowly
ovate to oblong-elliptic, 7–15 × 4–5.5 cm, round, obtuse,
acute or short-acuminate at apex.

Corollas in *Dendrosipanea* (3 spp.) are hypocrateri-
form, 17–30 mm long, white to cream-white, sometimes
with the tube green. The tubes are narrowly infundibuli-
form, 11–20 mm long, glabrous, sparsely appressed-strig-
ulose or hirtellous outside, basal portion glabrous and
medio-distal portion villous inside, with a dense ring
of yellow hairs at mouth inside. The lobes are subequal,
sometimes slightly asymmetrical and of slightly different
width on the same corolla, ovate, narrowly ovate, oblong
to ovate-oblong, 7.5–16 × 4–7.5 mm, and obtuse to acute
at apex.

In *Limnosipanea* (3 spp.), the corollas are hypocra-
teriform, 3–16(–18) mm long, white, cream-white, pink-
ish-white, pink to lilac. The tubes are narrowly cylin-
drical, 2–9 mm long, externally glabrous or strigose,
internally villous, with a pubescent ring at the orifice;
and the lobes are left-contorted, ovate or oblong-ovate,
1–8 × 0.5–4 mm, obtuse to round at apex. The shape
and dimensions of the corollas are important diagnos-
tic characters to distinguish the three species of the
genus. The largest flowers in the genus are those of *Lim-
nosipanea erythraeoides* K.Schum., which has corollas
11.5–16(–18) mm long (tubes 7–9 mm long, lobes 4.5–8
× 2–4 mm). Whereas, the corollas of *L. palustris* are 5.7–
10 mm long, with the tubes 3.5–6.5 mm long and lobes
2.2–3.5 × 0.7–0.9 mm, and in *L. spruceana* Hook.f., the
corollas are 3–5.5 mm long, with the tubes 2–2.5 mm
long and lobes 1–3 × 0.5–0.7 mm.

*Maguireothamnus* (3 spp.) has the largest flowers
in the tribe. The corollas are hypocrateriform, 8–17 cm
long, with the tube pale green, greenish-yellow, cream-
white to pale yellowish-green, sometimes reddish at
base and white lobes. The tubes are long-cylindrical and
slightly wider at mouth, 6.5–13 cm long, externally gla-
brous, internally puberulent, with a pubescent ring at
orifice inside, and the lobes are ovate, lanceolate, oblong,
oblong-ovate to obovate, 0.7–5 × 0.3–1.5(-2) cm, and
round, obtuse, acute or acuminate at apex. The largest

flowers in the genus (and in the tribe) are found in *M. speciosus*, which has corollas 9–17 cm long, with tubes (6.5-)8–13 cm long and lobes 2.3–5 cm long.

In *Neblinathamnus* (2 spp.), the corollas are hypo-
crateriform, 15–22 mm long, green to yellowish-green,
or with a red tube and yellowish or greenish lobes. The
tubes are narrowly cylindrical and slightly wider at
mouth, 9–16 mm long, externally glabrous or hirtellous,
internally puberulent throughout or pubescent at mouth,
the portion corresponding with the anthers with vermi-
form/multicellular hairs, and a pubescent ring at orifice
inside. The lobes vary from ovate, narrowly ovate, ellip-
tic to oblong, 5–6 × 2.5–5 cm, and are obtuse or round
at the apex.

Corollas in *Neobertiera* (5 spp.) are hypocrateri-
form, 3.9–15.5 mm long, white. The tubes are narrowly
cylindrical and slightly wider at mouth, 3–9 mm long,
appressed strigose-sericeous outside, puberulent inside,
with a narrow line of sparse yellow moniliform hairs
at mouth. Corolla lobes are thickened at base, narrowly
oblong or oblong-ovate, 0.9–6 × 0.5–2.7 mm, and round
or acute at apex. The smallest corolla in the genus are
those of *N. micrantha*, which has corollas 3.9–4.2 mm
long, and the largest are those of *N. gracilis*, which has
corollas 9.5–15.5 mm long.

In *Pteridocalyx* (1 sp.), the corollas are hypocrateri-
form, 14–19 mm long, with the corolla tube pale brown
or white and brownish at medial portion, and pink lobes
with a basal white triangle of glandular hairs inside. The
tubes are narrowly cylindrical, slightly wider at mouth,
10.5–13.5 mm long, and the lobes are oblong-ovate to
ovate, 3.5–5.5 × 1.7–3 mm, and obtuse to acute at apex.

*Sipanea* (17 spp.) is the largest and most widespread
genus in the tribe, and has a wide variation in corolla
shape, size, and color. The corollas vary from hypocra-
teriform, narrowly infundibuliform, narrowly campan-
ulate to campanulate, and can be white, pinkish-white,
cream-white, pink, or pale purple, or sometimes the
lobes are pink and with a white basal triangular area
forming a star shape at mouth, with the five lobes. The
tubes can be glabrous, puberulent, short-pubescent or
hirsute, or with the lower half glabrous and the distal
portion pubescent outside, and glabrous, puberulent or
pubescent at the stamen insertion and the rest glabrous,
or puberulent or pubescent throughout inside. In the
present treatment three sections are recognized within
*Sipanea*, which are characterized by the internal vesti-
ture of the corolla mouth: 1) Section *Sipanea*, with a ring
of yellow hairs; 2) Section *Virecta*, with a ring of white
hairs; 3) Section *Nudae*, glabrous or with sparse white
hairs. The variation of corolla shape and size for each
section is discussed below.
In *Sipanea* section *Sipanea*, the corollas are consist-
ently hypocrateriform and with a dense ring of yellow
hairs exserted beyond the mouth. The corollas range
from (8–)8.5 to 27.5(–28) mm in length, with tubes nar-
rowly cylindrical and slightly wider towards the mouth,
6–18 mm long, and with (4)5(6) lobes varying from
round, broadly obovate, broadly elliptic, elliptic, oblong-
elliptic, obovate to oblanceolate, and 2.5–10.5 × 1.5–8
mm. Corolla color in this section varies from pink, pale
pink, whitish-pink, or with tube pink and lobes white,
while in *S. glomerata* is consistently white, and in *S.
veris* is pale to intense pink, turning paler after anthe-
sis, with lobes basally white (non-glandular), forming a
white ring at mouth. The smallest corollas in this section
are found in *S. hispida*, which has corollas 8.5–15(–16.5)
mm long, with the tubes 6–10(–12.5) mm long and lobes
2.5–5 × 1.5–3 mm, and in *S. pratensis*, which has corol-
las 14–28 mm long, with the tubes (8–)10–17 mm long
and lobes (2.5–)4–11 × (2–)2.5–7 mm. The largest corol-
las are found in *S. galioides*, which has corollas (18.5–)
22.5–27.5(–28) mm long, with the tubes (13–)15–18 mm
long and lobes (5.5–)7.5–10.5 × 3–6(–7.5 mm), and also
in *S. pratensis*, which has corollas 14–28 mm long, with
the tubes (8–)10–17 mm long and lobes (2.5–)4–11 ×
(2–)2.5–7 mm. In *S. galioides*, *S. pratensis* and *S. veris*,
the corollas are very variable in size throughout their
geographic range, sometimes varying in size within the
same population or even on the same individual, and
with lobes sometimes unequal or of slightly different
shapes within the same corolla. Corolla lobes in *Sipanea
galioides* vary from broadly ovate or obovate to elliptic-
ovate, (5.5–)7.5–10.5 × 3–6(–7.5 mm), and subobtuse to
acute at the apex. In *Sipanea pratensis*, lobes vary from
round, broadly elliptic, elliptic, obovate, oblong-elliptic
to oblanceolate, and can vary in shape and size within
the same population, or sometimes they may be unequal
or of slightly different shape on the same corolla, (2.5–)
4–11 × (2–)2.5–7 mm, and round, obtuse to acute,
rarely apiculate when subobtuse or acute, or indented
when obtuse or round at the apex. In *S. veris*, the lobes
vary from obovate to round, 6–10 × 4.5–8 mm, and are
obtuse to subacute at the apex.

*Sipanea* section *Virecta* is characterized by a ring of white hairs at the corolla mouth. Contrary to the other two sections, the corolla shape in this section is quite variable, being hypocrateriform in *S. biflora* and *S. carrenoi*, narrowly infundibuliform in *S. gleasonii* and *S. setacea*, and campanulate or narrowly campanulate in *S. micrantha* and *S. ovalifolia*. The corolla color is also more variable in this section. In *S. gleasonii*, the corollas vary from pale pink to white, at the end of anthesis, and in *S. micrantha* and *S. ovalifolia* is consistently white. In

*S. biflora* the corollas vary from pink, deep pink to pale purple, and the lobes have a narrowly triangular basal area with white glandular hairs, forming a star-like pattern with the five lobes. In *S. carrenoi*, a species only known by the type specimen, the corollas are pink, and in *S. setacea*, also known only by the type, the corolla is reported to be purple (fide specimen label of *Huber et al. 8246*). Corollas in this section are also more variable in size, ranging from 4 to 21(–29) mm long, with tubes 2.5–13(–15) mm long and lobes varying from round, broadly ovate, ovate, oblong-obovate, obovate to narrowly oblong, and 1.5–8.5(–14) × 1–5.5(–7) mm. The smallest corollas in this section are those of *S. micrantha*, which are campanulate, 4–6.5 mm long, with the tubes 2.5–3.5 mm long and lobes 1.5–3 × 1–1.5 mm. The largest corollas in section *Virecta* are found in *S. biflora*, which has corollas very variable in size throughout the geographic range, often varying in size within the same population or even within the same individual; they are hypocrateriform, and ranging from (8–)15 to 21(–29) mm long, with the tubes 5–13(–15) mm long and lobes 3–8.5(–14) × 2–5.5(–7) mm.

In *Sipanea* section *Nudae*, all species have hypocra-
teriform corollas, glabrous or with a few sparse white
hairs at mouth. Corollas of this section are entirely pink,
or with a pale green to greenish-white or red tube, and
the lobes are pinkish-white, pink or lavender. *Sipanea
wilson-brownei* differs from the other species of this sec-
tion by having corolla lobes pink often with a median
linear white area, microscopically glandular, at the base,
forming a white star-like pattern with the five lobes. In
this section the corollas vary from 8.5 to 27.5 mm in
length, with tubes narrowly cylindrical and slightly wid-
er towards the mouth, or slightly wider at median por-
tion in *S. prancei*, and from 5.7 to 18 mm long. Corolla
lobes in this section vary from elliptic, narrowly elliptic,
oblong-obovate, narrowly obovate, obovate to ligulate,
2.7–9.5 × 1.4–4.7 mm, and are round, obtuse or acute at
apex. The smaller corollas in this section are those of *S.
prancei*, which are 8.5–11 mm long, with the tubes 5.7–
7.5 mm long and lobes 2.7–3.5 long). The largest corollas
in this section are found in *S. ayangannensis*, which has
corollas 25–27.5 mm long, with the tubes 17–18 mm long
and lobes 8–9.5 long, and in *S. wilson-brownei*, which
has corollas 13–28 mm long, with the tubes (7–)10–15
mm long and lobes 4–8.5(–14) long.

*Sipaneopsis*, a genus endemic to Amazonian white-
sand areas, has a unique flowering modality within the
Rubiaceae, which was discussed and illustrated by Del-
prete (2015a, 2018; see discussion in *Flowering Modal-
ity*). In this genus, the corollas change shape and size
as they go through subsequent flowering stages (Fig-
ures 80, 82). At the initial and intermediate stages, the corollas are small, campanulate, with a short tube, with lobes already opened and erect, with basal appendages appressed against each other and obstructing the corolla mouth. At the final stage of anthesis, the corollas expand becoming much larger and hypocrateriform, with the tube narrowly cylindrical, the lobes reflexed and perpendicular to the tube, and the appendages become erect, allowing access to visitors and pollinators into the corolla. The corollas in *Sipaneopsis* are pink during anthesis and turn pinkish-white to white at final stage. The corolla lobes in *Sipaneopsis* are commonly left-contorted, or they might exceptionally be irregularly imbricate, with 1-3 interior lobes, in *S. cururuensis* and *S. rupicola*.

Because in *Sipaneopsis* the corollas change shape and size during the flowering process, and because the corolla lobes are already open before anthesis, corolla dimensions have sometimes been reported from flowers not yet fully expanded (e.g., Steyermark, 1967, 1974, 1984). In the present treatment, shapes and sizes are reported only from fully expanded corollas, i.e., when the lobes are perpendicular to the tube. In *Sipaneopsis*, the fully expanded corollas are hypocrateriform and range from 13 to 30 mm long, with tubes cylindrical and slightly wider at mouth, 9.5 to 22 mm long. Fully expanded corollas lobes vary in shape from round, ovate, oblong-ovate elliptic to obovate, 4.2-9 × 1.8-4 mm, and are round, obtuse or acute at the apex. In addition, fully expanded corolla lobes are often slightly unequal, and may vary in shape and size on the same plant or the same corolla. The smallest corollas in the genus are those of *S. huberi*, which are 13-14 mm long, with the tubes 9.5-10 mm long, and lobes 4-4.5 × 2.5-3 mm, when fully expanded. The largest corollas are found in *S. pacimoniensis*, only known from a single fully expanded corolla on the type specimen, 27.5-28.5 mm long, tube 19 mm long, lobes 8.5-9.5 × 4.5-5.5 mm, and in *S. maguirei* Steyerm., which is the most widespread species in the genus, with corollas 21-30 mm long, corolla tubes 15-22 mm long, and lobes 4.5-9 × 3-4.2 mm, when fully expanded.

*Steyermarkia* is exceptional within the tribe by having consistently 4-merous flowers. Its corollas are pink, hypocrateriform, with a cylindrical tube 3.5-4.5 cm long, and broadly ovate lobes, 1.4-2 × 0.9-1.3 cm.

## Stamens

In the genera of this tribe the filaments are free at the base, and equal or subequal. The anthers are dorsi-fixed near the base or at the middle of the corolla, and dehisce by longitudinal slits.

Within the Sipaneeae, the genera *Limnosipanea*, *Maguireothamnus*, *Sipaneopsis*, and *Steyermarkia* are homostylous. The stamens of these genera are discussed below.

*Limnosipanea* is only genus of the tribe with well-exserted stamens. In this genus, the filaments are glabrous and inserted near the mouth of the corolla tube, and the anthers are narrowly elliptic or oblong, dorsi-fixed near the middle. In all other genera of the tribe the stamens are included, except for those of the short-styled flowers of *Dendrosipanea*, which may have partially exserted anthers.

In *Maguireothamnus* the filaments are inserted near or just below the corolla mouth and short. The anthers are subsessile, elongate and dorsi-fixed near the base.

In *Sipaneopsis* the filaments are extremely short, inserted at the middle of the corolla tube. The anthers are subsessile, linear and dorsi-fixed near the base.

In *Steyermarkia* the filaments are inserted on the upper part of the corolla tube, short, and glabrous. The anthers are subsessile, elongate and dorsi-fixed near the base.

The genera *Chalepophyllum*, *Dendrosipanea*, *Neblinathamnus*, *Neobertiera*, *Pteridocalyx* and *Sipanea* are heterostylous. Aside from the stamens inserted at different heights on the corolla tube, the anthers may also differ in shape and size in the long-styled and the short-styled flowers of the same species.

In *Chalepophyllum*, the filaments of short-styled flowers are inserted at the upper portion of corolla throat, and the anthers are narrowly oblong. In long-styled flowers, they are inserted at the medio-basal portion of the corolla throat, and the anthers are also narrowly oblong.

In *Dendrosipanea*, the stamens of short-styled flowers are included or partially exserted, with filaments inserted at distal portion of corolla throat, and the anthers are linear, and the style is included. In long-styled flowers, the stamens are included, with filaments also inserted at basal portion of corolla throat, and anthers are also linear, while the style is barely exserted, with the branch tips presented just beyond corolla mouth.

In *Neblinathamnus*, the stamens of short-styled flowers are included, with extremely short filaments (anthers subsessile) inserted on the distal most portion of the corolla throat with the anther tips at corolla mouth or barely exserted, and the anthers are linear. The stamens of long-styled flowers are included, with extremely short filaments (anthers subsessile) inserted at upper portion of corolla throat with the anther tips much below the corolla mouth, and the anthers are narrowly oblong.
rowly elliptic, much shorter than those of short-styled flowers.

In *Neobertiera*, the filaments of short-styled flowers are inserted at about the middle or at the distal portion of the corolla tube and anthers are linear. Those of long-styled flowers are inserted near the base or at the middle of corolla tube, and the anthers are linear or narrowly sagittate.

In *Pteridocalyx*, the filaments of short-styled flowers are inserted at the distal portion of corolla tube, and the anthers are linear. The filaments of long-styled flowers are inserted near the base of the corolla tube, and the anthers are also linear.

*Sipanea* is the most diverse genus of the tribe, and is here subdivided into three sections. The characteristics and points of insertion of the stamens are discussed by section. In section *Sipanea*, the filaments of long-styled flowers are inserted near the base, at about the middle, or at medio-distal portion of the corolla tube, and the anthers are narrowly oblong-elliptic to linear. The filaments of short-styled flowers are inserted at the distal portion of the corolla tube, and the anthers are narrowly oblong-elliptic, very narrowly lanceolate or linear. In the medium-styled flowers of *Sipanea hispida* the filaments are inserted at 3/10 to 1/2 from the base of the corolla tube, just below the tips of the style branches, and the anthers are linear.

In *Sipanea* section *Virecta* and section *Nudae*, the filaments of long-styled flowers are inserted near the base or at medio-distal portion of the corolla tube, and the anthers are narrowly oblong to linear; while the filaments of short-styled flowers are inserted at the distal portion of the corolla tube, and the anthers are linear.

## Pollen

In all the genera of the Sipaneeae, pollen grains are released in monads and are colporate. The number of colpi are either 3 or 4. In most genera the number of colpi are consistently 3 or 4, which represent a good diagnostic character for the identification of genera. In a few genera, the colpi are commonly 3 or exceptionally 4, or vice versa. Dimensions and descriptions of pollen grains in the Sipaneeae are presented below, organized by genus.

*Chalepophyllum*. (Figure 4AB). Pollen grains are 32.37–33.83 × 26.50–29.52 µm, and are the second largest in the tribe, after those of *Maguireothamnus*, which corresponds with the corolla tubes 1.7–3.1 cm long, which are also the second largest in the tribe. The number of colpi is commonly 4 or exceptionally 3. The external surface (sexine) is foveolate-reticulate.

*Dendrosipanea*. (Figure 4C–D). Pollen grains are 18.68–29.53 × 18.50–25.42 µm, which are average dimensions for most genera of the tribe. They are consistently 4-colporate in all the species. External ornamentation is either foveolate or foveolate-reticulate.

*Limnosipanea*. (Figure 4E–F). Pollen grains are 20.27–30.38 × 20.45–27.06 µm, which are average dimensions for most genera of the tribe. They are 3-colporate in all the species, although they could exceptionally be 4-colporate in *L. palustris*. Their external ornamentation is shallowly foveolate, without perforations in *L. erythraeoides* and *L. spruceana* var. *spruceana*, or either without perforations or finely perforate in *L. palustris*.

*Maguireothamnus*. (Figure 4G–H). Pollen grains are the largest of the tribe, by being 69.11–75.38 × 54.60–67.84 µm. The large size of the pollen corresponds with the long-tubular corollas, with corolla tubes 6.5–13 cm long, which are also the largest in the Sipaneeae. Grains are commonly 3-colporate, although they may be 3- or 4-colporate in *M. speciosus*. The external wall in this genus is either smooth or finely foveolate.

*Neblinathamnus*. (Figure 4I). Pollen grains are 17.28–23.17 × 18.14–25.12 µm, consistently 3-colporate, and foveolate-reticulate. There is a difference in size between the 2 species recognized in the genus: 20.52–23.17 × 21.61–25.12 µm in *N. argyreus*, and 17.28–19.58 × 18.14–20.42 µm in *N. brasiliensis*. Pollen size corresponds with the length of the corolla tubes, which are 10.5–14.5(-16) mm long in *N. argyreus*, and 9–12 mm long in *N. brasiliensis*.

*Neobertiera*. (Figure 4K). A genus of 5 species of perennial herbs, subshrubs or shrubs endemic to the Guiana Shield. One these species, *N. micrantha* Delprete, is only known from the type specimens, and the other two are only known by three collections, *N. montedouradensis* Delprete, *N. pakaraimensis* Delprete. The only species of *Neobertiera* studied, *N. gracilis*, has pollen

**Figure 4.** SEM images of pollen grains of Sipaneeae genera. **A–B.** *Chalepophyllum guyanense* A. side view. **B.** polar view. **C.** *Dendrosipanea prancei*, side view. **D.** *Dendrosipanea prancei*, polar view. **E–F.** *Limnosipanea spruceana* var. *spruceana* E. side view. **F.** detail of exine cerebriform sculpturing. **G–H.** *Maguireothamnus speciosus*. **G.** side view, with smooth exine. **H.** polar view. **I.** *Neblinathamnus brasiliensis*, side view. **J.** *Neobertiera gracilis*, side view. **K.** *Neobertiera palustris*, polar view. **L.** *Pteridocalyx appunii*, side view. **A–B:** from Delprete & Benjamin 12860 (CAY); **C–D:** from Prance et al. 16199 (F); **E–F:** from Delprete et al. 7433 (CAY); **G–H:** from Steyermark 59801 (F); **I:** from Silva & Brazão 60907 (F); **J:** from Grenwald & Persaud 110 (U); **K:** from Delprete 11860 (CAY); **L:** from Delprete & Benjamin 12860 (CAY). All scale bars are 1 µm, except G–H that are 10 µm. Images made by Iris van der Beeten.
<figure><img src="image_8.png" /><figcaption>Figure 4.</figcaption></figure>
grains 13.14–15.43 × 14.15–17.58 µm, 3-colporate, and foveolate.

*Pteridocalyx*. (Figures 4L, 5A–B). A monospecific genus endemic to central Guyana, in the Potaro River Basin. Pollen grains are 13.13–15.06 × 13.55–16.85 µm, 3-colporate. The exine is foveolate-reticulate and with a rugulate surface.

*Sipanea*. (Figure 5C–H). A genus of 17 species, with the widest geographic distribution and the highest diversity in the Sipaneeae. The five species studied in this genus have 3-colporate pollen grains, 15.75–23.77 × 14.49–22.25 µm, and with foveolate-reticulate or finely foveolate external ornamentation. Three sections are here recognized in the genus: 1) section *Sipanea*, with a ring of yellow hairs at corolla mouth, 2) section *Virecita*, with a ring of white hairs at corolla mouth, and 3) section *Nudae*, with a corolla mouth glabrous or a few sparse hairs. Pollen grains dimensions and external ornamentation are amply overlapping and do not offer any diagnostic characters for these sections. The possible pollen dimorphism in distylous species was observed only in *S. pratensis* var. *pratensis*. In both forms pollen grain dimensions and external ornamentation, foveolate-reticulate, are similar, and it seems that at least in this species there is no pollen dimorphism.

*Sipaneopsis*. (Figure 5I–J). *Sipaneopsis* is a genus of 8 species endemic to white-sand savannas of the Amazon Basin. Two species are known only from the type specimens and 3 from a few collections, and flower buds of these specimens could not be extracted for palynological studies. Two species, *S. duckei* and *S. maguirei*, known from numerous collections, were studied. They have 4-colporate, 18.85–25.85 × 17.70–25.40 µm, shallovely foveolate pollen grains.

*Steyermarkia*. (Figure 5K–L). One collection with several duplicates (*Hammel et al. 15637*), with several flowers on each specimen, allowed the extraction of one flower bud. Pollen grains are 27.98–35.48 × 26.72–31.34 µm, 3-colporate, and externally foveolate.

An article dedicated to the pollen morphology of this tribe, with LM and SEM images, discussions, and vouchers cited, is being prepared and will soon be submitted for publication (Delprete, van der Beeten and De Block, in progress).

## Styles

The styles in the Sipaneeae are included or exserted, and have two style branches. On the adaxial side of each style branch there is a minutely papillose stigmatic surface, which becomes receptive after the style branches have spread apart from each other. The genera *Limnosipanea*, *Maguireothamnus*, *Sipaneopsis*, and *Steyermarkia* are homostylous. In *Limnosipanea*, the style is exserted, glabrous, and with oblong or ovate branches. In *Maguireothamnus*, the style is exserted well beyond the corolla mouth, antrorse-papillose at distal portion, and with elliptic branches. In *Sipaneopsis*, the style is included or barely exserted, with the branch tips exserted, glabrous, and with lanceolate to narrowly lanceolate branches. In *Steyermarkia*, the style is included, and has oblong branches.

The genera *Chalepophyllum*, *Dendrosipanea*, *Neblinathamnus*, *Neobertiera*, *Pteridocalyx* and *Sipanea* are heterostylous. Aside from the variation in length of the style, the style branches may also be of different shape and size in the long-styled and short-styled flowers of the same species.

In *Chalepophyllum* and *Dendrosipanea*, the style is much shorter than the corolla tube in short-styled flowers, or is exserted well beyond corolla mouth in long-styled flowers. The style branches are oblong in both forms.

In *Neblinathamnus*, the stamens are included, with short filaments inserted at distal portion of corolla throat, and the anthers are linear. In short-styled flowers, the style is included and with linear branches. In long-styled flowers, the stamens are also included with short filaments, but they are inserted at medio-basal or median portion of corolla throat; the anthers are narrowly oblong or linear; the style is as long as corolla tube with the style branches barely exserted beyond corolla mouth or exserted, with narrowly ovate, narrowly lanceolate or linear branches.

In *Neobertiera*, the style is much shorter than the corolla tube, with narrowly oblong or elliptic branches, in short-styled flowers; or is about the same length of the corolla tube with the tips of the branches barely exserted or exserted beyond the corolla mouth, with narrowly
<figure><img src="image_9.png" /><figcaption>Figure 5.</figcaption></figure>
oblong, narrowly lanceolate to linear branches in long-
styled flowers. In *Pteridocalyx*, the style is much short-
er than the corolla tube and with narrowly lanceolate
branches in short-styled flowers; while it is as long as the
corolla tube with the tips of the branches barely exerted
or exerted just beyond the corolla mouth and with lin-
ear branches in long-styled flowers.

*Sipanea* is the most diverse genus of the tribe,
and is here subdivided into three sections. In section
*Sipanea* (corolla mouth with a ring of yellow hairs), the
style of long-styled flowers is as long as the corolla tube
with the tips of branches exerted or exerted beyond
the corolla mouth, with oblong or obovate branches
(0.6–)1–1.3 mm long. In short-styled flowers, it is much
shorter than the corolla tube, and with linear branches
2–3 mm long. In the medium-styled flowers of *Sipanea
hispida*, the style is about half the length of the corolla
tube and corresponds with the middle or the upper tips
of the anthers (stamens inserted at 3/10 to 1/2 from the
base of the corolla tube, and has linear branches, 1–3
mm long. In section *Virecta* (corolla mouth with a ring
of white hairs), the style of long-styled flowers is as long
as the corolla tube with the tips of the branches exerted
or exerted beyond the corolla mouth and has obovate,
very narrowly lanceolate or linear branches 0.6–2 mm
long. In short-styled flowers, it is much shorter than the
corolla tube, with linear branches 1–1.6 mm long. In sec-
tion *Nudae* (corolla mouth glabrous or with sparse white
hairs), the style of long-styled flowers is as long as corol-
la tube with the branches obovate, very narrowly lanceo-
late or linear to filiform, 0.6–2.5 mm long, branch tips
exerted. In short-styled flowers, the style is much short-
er than the corolla tube and with the branches narrowly
ovate, narrowly lanceolate or linear, 1–3.5 mm long.

Ovaries

In the Sipaneeae, the ovaries are inferior, bilocular,
with axile placentation, and with many ovules per loc-
ule. In most genera, the placenta has a stalked exten-
sion inserted at the middle, medio-basal, or distalmost
portion of the septum near the roof of the locule. *Den-
drosipanea* is exceptional in the tribe by having a fleshy
placental extension adnate along the entire length of the
septum. In *Chalepophyllum*, *Limnosipanea*, *Maguire-
othamnus*, *Neblinathamnus*, *Neobertiera*, *Sipaneopsis*
and *Steyermarkia*, the placental stalk is inserted at the mid-
dle of the septum, and terminates with a hemi-ellipsoid,
oblong-ellipsoid, or hemi-elliptic extension, or with a
globose extension in *Sipaneopsis*.

In *Sipanea*, the placental stalk is inserted at the mid-
dle or medio-basal portion of the septum, and termi-

nates with an oblong or hemi-elliptic extension, with the
ovules inserted on the placental extension. In some spe-
cies of this genus, the stalk of the young ovaries is very
short, giving the impression that the ovules are inserted
directly on the central septum.

*Dendrosipanea* is unique within the tribe in having a
fleshy placental extension adnate along the entire length
of the septum, with the ovules irregularly peltate on the
longitudinal placental extension.

Delprete (2019) described the placenta of *Pteridoca-
lyx* as longitudinally adnate along the central septum.
However, additional anatomical studies revealed that
this genus is unique within the tribe by having a placen-
tal stalk inserted at the distalmost portion of the sep-
tum, near the roof of the locule, with a pendulous, nar-
rowly cylindrical extension almost as long as the locule,
and the ovules are inserted on the cylindrical extension.

Fruits

Most genera of the Sipaneeae have persistent,
bilocular, multi-seeded, basipetally dehiscent capsules
with a central placenta in each locule, which dehisce
and release the wind-dispersed seeds. *Neobertiera* and
*Sipaneopsis* are exceptional within the tribe, by having
indehiscent, crustaceous fruits that fall off as dispersal
units, leaving a tiny round scar and subtending bracts
on the infructescence branches.

Shape and dimensions of capsules are rather consist-
ent within each genus, with the exception of *Sipanea*,
the most diverse genus in the tribe, with fruits varying
in size and shape. They vary among genera, offering a
good practical aid for generic distinction. In *Chalepo-
phyllum*, capsules are ovoid to ellipsoid, 7–17 × 5–7 mm;
in *Dendrosipanea*, turbinate to oblong-turbinate, (5–)7–
11.5 × 3–5.7 mm; in *Limnosipanea*, are globose or ovoid
to subglobose, 2.5–4 × 1.5–3 mm; in *Maguireothamnus*
are obovoid, ovoid to ellipsoid, 10–27 × 8–15 mm; in
*Neblinathamnus* are subturbinate, obovoid-subglobose
to broadly obconical, 4–5 × 3–4 mm; in *Pteridocalyx* are
oblong-ellipsoid to narrowly oblong, 6–14 × 2–3 mm; in
*Sipanea* are globose, subglobose, broadly ovoid, ovoid to
narrowly ovoid, obovoid, ellipsoid, oblong-ovoid, oblong,
narrowly oblong-elliptic, oblong-turbinate or cylindrical-
oblong, 2.5–11 × 1.5–5.5 mm; and in *Steyermarkia* are
subglobose, 6.5–8 mm in diam.

The indehiscent fruits of *Sipaneopsis* and *Neobertiera*
are quite similar in shape and size, being globose or sub-
globose, rarely urceolate in *Sipaneopsis*, 3–5 in diam. in
the former, and globose, 1.2–4 mm in diam. in the latter.

Capsular dehiscence is a valuable diagnostic charac-
ter to identify genera within the Sipaneeae. They are sep-
ticidal in *Chalepophyllum*, *Dendrosipanea* and *Pteridocalyx*, and loculicidal in *Limnosipanea*, *Maguireothamnus*, *Neblinathamnus*, *Sipanea*, and *Steyermarkia*.

The term secondary dehiscence (Delprete 1999) refers to the distal splitting of the valves that occur in advanced stages of capsule maturity, usually after and perpendicular to the primary dehiscence. In the Sipaneeae, secondary dehiscence was observed only in the old capsules of *Chalepophyllum*.

## SYSTEMATIC TREATMENT

### Description of the tribe Sipaneeae

Tribe **Sipaneeae** Bremek. (as "Sipaneae"). Rec. Trav. Bot. Neerl. 31: 253. 1934

Type: *Sipanea* Aubl.

**Herbs**, subshrubs or shrubs, rarely treelets; generally terrestrial, or semi-aquatic (amphibious) or free-floating herbs in *Limnosipanea* and a few species of *Sipanea*; wood, when present, whitish, yellowish or red-dish. **Raphides** absent. **Stipules** interpetiolar, entire or bifid, or entire when young and becoming bifid when older, rarely with several linear lobes in *Sipaneopsis*, with colleters on the adaxial side secreting a resinous substance, persistent or caducous. **Leaves** opposite and decussate, ternate, or rarely in whorls of 3-6(-8) leaves per node in *Limnosipanea*, sessile, subsessile or petiolate; blades chartaceous, papyraceous, subcoriaceous to coriaceous; domatia commonly absent, or tuft-domatia on leaves of *Chalepophyllum*. **Inflorescences** terminal (*Dendrosipanea*, *Limnosipanea*, *Neobertiera*, *Pteridocalyx*, *Sipanea*, and *Sipaneopsis*) or axillary (*Chalepophyllum*, *Maguireothamnus*, *Neblinathamnus*, and *Steyermarkia*), simple, capitate, condensed, or cymose, congested or short- to long-branched, with 2-8 orders of branching, pauci- to multi-florous or uniflorous. **Flowers** actinomorphic or subzygomorphic in *Maguireothamnus*, bisexual, 4-5(-6)-merous, protandrous, homostylous (*Limnosipanea*, *Maguireothamnus*, *Sipaneopsis*, and *Steyermarkia*) or heterostylous (*Chalepophyllum*, *Dendrosipanea*, *Neblinathamnus*, *Neobertiera*, *Pteridocalyx*, and *Sipanea*). **Calyx** persistent (crowning the fruit); tube extremely reduced or absent, with lobes free; lobes often minute, equal or subequal, rarely foliose, or with 1 or 2 lobes per flower expanded into white to cream-white calycophylls in *Pteridocalyx*. **Corolla** commonly hypocrateriform, or narrowly infundibuliform, infundibuliform, narrowly campanulate to campanulate, white (sometimes

tube pale green), cream-white, pinkish-white, pink, rarely lilac (*Limnosipanea*), or corolla tube red with yellowish or greenish lobes in *Neblinathamnus*; aestivation contorted or rarely irregularly imbricate (1-3 lobes internal in two species of *Sipaneopsis*). **Stamens** as many as corolla lobes, inserted near the base, or at the medial zone, or near the corolla mouth, sometimes all positions present in di- or tri-stylous species; anthers included or exserted, oblong to narrowly elliptic to button-shaped, 2-locular, dehiscing by longitudinal slits, dorsifixed near the base or around the middle, introrse. **Pollen** released in monads, 3-4 colporate, exine reticulate or foveolate. **Style** included or exserted; style branches 2, with stigmatic surface smooth or glandular. **Ovary** inferior, 2-locular, placentation axile, with a stalked placental extension; the stalk commonly inserted at the middle or medio-basal portion of the septum, terminating in a hemi-ellipsoid, oblong-ellipsoid or hemi-elliptic extension, or with a globose extension in *Sipaneopsis*; or the stalk inserted at the distalmost portion of the septum (i.e., near the roof of the locule) with a pendulous, narrowly cylindrical extension in *Pteridocalyx*; or with a fleshy placental extension adnate along the entire length of the septum in *Dendrosipanea*. **Fruits** capsular, loculicidal (*Limnosipanea*, *Maguireothamnus*, *Neblinathamnus*, *Sipanea*, *Steyermarkia*) or septicidal (*Chalepophyllum*, *Dendrosipanea*, *Pteridocalyx*), persistent, opening basipetally, woody or crustaceous, or indehiscent, crustaceous, falling off as dispersal units (*Neobertiera* and *Sipaneopsis*), with persistent calyx. **Seeds** globose, ovoid or irregularly tetrahedral; wings absent or extremely reduced and concentric in *Maguireothamnus*.

The tribe Sipaneeae, as here delimited, includes the genera *Chalepophyllum* (1 sp.), *Dendrosipanea* (3 spp.), *Limnosipanea* (3 spp.), *Maguireothamnus* (3 spp.), *Neblinathamnus* (2 spp.), *Neobertiera* (5 spp.), *Pteridocalyx* (1 sp.), *Sipanea* (17 spp.), *Sipaneopsis* (8 spp.), and *Steyermarkia* (1 sp.), for a total of 44 species.

## KEY TO THE SIPANEEAE GENERA

Some of the genera of this tribe have variable habit (i.e., herb, subshrub or shrub) and/or phyllotaxy (i.e., leaves opposite, ternate or whorled, e.g., *Limnosipanea*); these genera are found in multiple entries in this key.

1. Plant acaulescent or nearly so, sometimes with a woody stem to 18 cm long; leaves in basal rosettes, crowded at the apex of a short stem; flowers 4-merous (southern Mexico (Chiapas) and Guatemala; on rock walls, in rain forest understory) .................................................... 10. *Steyermarkia*
1. Plants with a well-developed stem; cauline leaves regularly spaced along the stem, not in basal rosettes; flowers (4)5(6)-merous .................................................................................. 2

2. Prostrate, decumbent or erect herbs.................................................................................. 3

3. Subshrubs (plant basally woody and distally herbaceous, or shrubs less than 50 cm tall), shrubs or small trees................ 7

4. Leaves whorled, 3-6(-8) per node (Panama, Colombia, Venezuela, Guyana, Brazil and Bolivia; ephemerous herb, terrestrial or semi-aquatic; periodically inundated open fields, margins of small water courses, and swamps)........ 3. *Limnosipanea*

5. Leaves opposite (opposite or ternate in *Neblinathamnus*).... 4

6. Plant semi-aquatic, amphibious or terrestrial; flowers homostylous; stamens exerted well beyond the corolla mouth.... .................................................................................. 3. *Limnosipanea*

7. Plant terrestrial; flowers homostylous or heterostylous; stamens included, or exerted just beyond the corolla mouth in short-styled flowers of some species of *Sipanea*.................. 5

8. Fruit a loculicidal capsule, persistent (flowers distylous; corolla lobes without a glandular area at base) (Nicaragua, Costa Rica, Panama, Colombia, Venezuela, Guianas, Peru, Brazil, Bolivia and Paraguay; open savannas, forest undercanopy, and rocky outcrops).................................................. 8. *Sipanea*

9. Fruit indehiscent, falling off as dispersal unit; plant erect. 6

10. Flowers homostylous; corolla mouth with 5 thickened triangular projections at base of each corolla lobe, covered with erect brushy white hairs at base of corolla lobes; corolla lobes glabrous on adaxial side, opening before complete elongation of the corolla tube (Guayana Shield: Colombia, southern Venezuela, northern Brazil, N of the Amazon River, except for *S. cururuensis* and *S. maguirei*, found S or the Amazon River; white-sand savannas, mostly lowlands or moderate elevations) ................ 9. *Sipaneopsis*

11. Flowers distylous or exceptionally tristylous; corolla mouth without thickened triangular projections at base of each corolla lobe; corolla lobes opening after complete elongation of the corolla tube, with glandular triangular area at base (Guyana, Suriname, French Guiana, northern Brazil (Pará); forest undercanopy, usually near creeks) .................... 6. *Neobertiera*

12. Some flowers of the inflorescence with 1 or 2 calyx lobes expanded and petaloid (calycophylls), white (Guyana: Upper Potaro River).................................................................................. 7. *Pteridocalyx*

13. Flowers without expanded, petaloid, calyx lobes.................. 8

14. Corolla 9-17 cm long, tube 5-13 cm long (Endemic to the tepuis of the Guayana Shield: Venezuela, Guyana and northern Brazil; on exposed sandstone outcrops, open scrub formations, *Bonnetia roraimae* forests, shrubby savannas, and open wet savannas, in sandy soils, at 1300-2600 m altitude) .................................................. 4. *Maguireothamnus*

15. Corolla < 5 cm long, tube < 3.5 cm long .................................................................................. 9

16. Inflorescence axillary, 1-7-flowered (Endemic to Guayana Shield, at 300-1900 m altitude).................................................................................. 10

17. Inflorescence terminal, many-flowered .................................................................................. 11

18. Leaves opposite; inflorescence 1-7-flowered; corolla infundibuliform, white to cream-white (sometimes the tube red-dish or greenish at base outside), lobes 7-15 × 4-5.5 mm; capsules septicidal, ovoid to ellipsoid, 7-17 × 5-7 mm, the valves secondarily splitting at apex (Guiana Shield: Venezuela, Guyana and northern Brazil, at 300-1430 m altitude).................................................................................. 1. *Chalepophyllum*

19. Leaves opposite or ternate; inflorescence 1-2-flowered or cymose, (2-3)3-5-flowered; corolla hypocrateriform, green to yellowish-green, or tube red and lobes yellowish- or whitish-green, lobes 4.5-6 × 2.5-3 mm; capsules loculicidal, subturbinate to obovoid-subglobose, 4-5 × 3-4 mm, the valves not secondarily splitting at apex (Sierra de la Neblina Massif, Venezuelan and Brazilian sides, at 1300-1900 m altitude) .................................................. 5. *Neblinathamnus*

20. Fruit indehiscent, falling off as dispersal unit; flowers homostylous; corolla mouth with 5 thickened triangular projections at base of each corolla lobe, covered with erect brushy white hairs at base of corolla lobes; corolla lobes glabrous on adaxial side, opening before complete corolla elongation (Guayana Shield: Colombia, southern Venezuela, northern Brazil, N of the Amazon River, except for *S. cururuensis* and *S. maguirei*, found S or the Amazon River; white-sand savannas, mostly lowlands or moderate elevations) .................................................................................. 9. *Sipaneopsis*

21. Fruit capsular, or indehiscent in *Neobertiera*; flowers distylous or tristylous; corolla mouth without triangular projections; corolla lobes with or without a basal triangular area with glandular hairs on adaxial side, opening after corolla tube complete elongation .................................................................................. 12

22. Shrubs or small trees; placenta with a fleshy extension adnate along the entire length of the septum (i.e., not stalked), with the ovules irregularly peltate on the longitudinal placental extension (Amazonian Colombia (Guianía), Venezuela (Amazonas), and Brazil (Amazonas); white-sand savannas).................................................. 2. *Dendrosipanea*

23. Subshrubs (plant basally woody and distally herbaceous, or shrubs less than 50 cm tall), or shrubs; placenta stalked, with the stalk inserted at the middle or medio-basal portion of the septum and an oblong hemi-elliptic or hemi-elliptic extension, with the ovules inserted on the placental extension .................................................................................. 13

24. Fruit indehiscent, falling off as dispersal unit; plant erect; flowers distylous or tristylous; corolla lobes linear-oblong to narrowly lanceolate, or ovate and with a white-glandular triangular area at base in *N. montedouradensis* (Guyana, French Guiana, Brazil (Pará); forest undercanopy, usually near creeks).................................................. 6. *Neobertiera*
13. Fruit a loculicidal capsule, persistent; plant erect, trailing or decumbent; flowers distylous; corolla lobes round, broadly ovate, obovate, elliptic-ovate or lanceolate, commonly without a white-glandular area at base, or sometimes with a median linear white area microscopically glandular at base, forming a white star-like pattern (with the 5 lobes) in S. wilson-brownei (Nicaragua, Costa Rica, Panama, Colombia, Venezuela, Guianas, Peru, Brazil, Bolivia and Paraguay; open savannas, forest undercanopy, and rocky outcrops) 8. *Sipanea*

## 1. CHALEPOPHYLLUM

*Chalepophyllum* Hook.f. in Benth. & Hook.f., Gen. Pl. 2: 50. 7-9 Apr 1873.

Hook.f. in Hooker's Ic. Pl. 12: 43-44, tab. 1148. Apr. 1873; K.Schum. in Martius et al., Fl. Brasil. 6(6): 245-246, tab. 111, fig. 4. 1889; Steyerm. in Mem. New York Bot. Gard. 10: 192-194, fig. 70A-F. 1964; Steyerm. in Lasser & Steyermark, Fl. Venezuela 9(1): 322-326, fig. 52. 1974; Delprete et al. in Steyermark et al., Fl. Venezuela 8: 541-542, fig. 437. 2004.

Type: *Chalepophyllum guyanense* Hook.f.

*Subshrubs* to *shrubs*; distal internodes, base of petioles and base of peduncles often covered by a resinous exudate produced by stipular colleters. *Stipules* free at base, broadly triangular to subtruncate, older stipules sometimes becoming bifid at apex, with the basal 2/3 covered by dense colleters inside. *Leaves* opposite, sessile to short-petiolate; blades ovate, obovate, oblong or spathulate; subcoriaceous; domatia in tuft of hairs, or absent. *Inflorescences* axillary, reduced-cymose, 1-7 flowered. *Flowers* heterostylous, 5-merous, fragrant. *Hypanthium* obconical or turbinate. *Calyx* tube extremely reduced, lobes subequal to unequal, large, oblong-triangular, ovate-lanceolate, oblong-lanceolate, lanceolate, elliptic to oblong-spathulate, with 3-5 minute colleters at each lobe sinus. *Calycophylls* absent. *Corolla* infundibuliform, white to cream-white, sometimes with the tube pale green outside; tube obconical, externally strigose, internally pubescent throughout or only at mouth, with a pubescent ring at orifice inside; lobes left-contorted, ovate, margin entire, round, obtuse, acute or short-acuminate at apex. *Pollen* (3)4-colporate; exine foveolate-reticulate, perforate. *Ovary* with a stalked placenta; stalk inserted at the middle of the septum, terminating with a narrow oblong-ellipsoid extension; ovules dorsoventrally peltate on the placental extension. *Short-styled flowers*: stamens

included, inserted at upper portion of corolla throat; filaments short; anthers narrowly oblong; style included, short, style branches oblong. *Long-styled flowers*: stamens included, inserted at medio-basal portion of corolla throat; filaments short; anthers narrowly oblong; style exerted well beyond corolla mouth, style branches oblong. *Fruits* capsular, dehiscing septicidally, thinly woody, the valves secondarily splitting at apex. *Seeds* many, vertical, 3-5-angular, irregularly elliptic or irregularly oblong to fusiform in outline, compressed, wings extremely reduced and concentric, or absent.

**Notes about publication dates:** Joseph Dalton Hooker (1873) published the genus *Chalepophyllum* in Bentham & Hooker's *Genera Pantarum*, vol. 2, page 50. In this work he only published the genus name, followed by the citation "*Hook. f. Ic. Pl. t. 1148*", and after the description he wrote that it has one species from Guyana, without citing the species name. The title page of volume 2 of *Genera Plantarum* states the publication date of 1873. Stafleu and Cowan (1976: 179) indicated that the part where page 50 is included was published on 7-9 April 1873.

Hooker published the name *Chalepophyllum guyanense* Hook.f. on page 43 and on plate 1148 of volume 2 of his *Icones plantarum*. The title page of this volume states the publication date as 1876. Below this binomial Hooker cited "Chalepophyllum, *Hook. f. in Benth. and Hook. f. Gen. Pl. ii. 50.*" Stafleu and Cowan (1979: 294-296) gave several publication dates of Hooker's *Icones plantarum* for volume 2 and plate 1148. On page 294, they gave the date of publication of plate 1148 as 1876 (as stated in the title page). Then on page 296, they gave the publication date of plate 1148 as April 1873. Above the dates of publication on page 296, they stated "...those [dates] of the parts of volumes 11-13 are cited here from manuscript annotations in the copies of the libraries at the Royal Botanical Gardens, Kew, and of the Botany Department of the British Museum (Natural History), London."

Therefore, both *Genera plantarum* and *Icones plantarum* must be cited for the name *Chalepophyllum* as places of publication, as it is impossible to know which of these publications was published first.

**Distribution and ecology:** Guayana Shield in Venezuela, Guyana and northern Brazil; scrub formations in sandy savannas, wet savannas with *Stegolepis* and Raptaceae, white-sand savannas, open dwarf *Bonnettia* forests, and sandy valleys, at 300-1430 m altitude. Only one species is here recognized.
1-1. *Chalepophyllum guyanense* Hook.f., Ic. Pl. 12: 43, tab. 1148. 1873. (Figures 4A-B, 6-9).

Type: GUYANA. Without locality, s.d., R.H. Schomburgk s.n. (holotype K [without barcode; see details below]; photo-K at NY).

*Chalepophyllum guyanense* var. *guyanense* in Mem. New York Bot. Gard. 10: 192. 1964

(=) *Chalepophyllum guyanense* var. *cuneatum* Steyerm, Mem. New York Bot. Gard. 10: 193. 1964.

Type: VENEZUELA. Bolívar: Ilu-Tepui, Gran Sabana, near Kavanayén, 1300 m, 30 Mar. 1952 (fl, fr), B. Maguire 33700 (holotype NY [barcode 00131039]; isotypes G [barcode G00389737], GH [barcode GH00095916], K [without barcode], P [barcode P02273576], US [barcode US00137690]).

(=) *Chalepophyllum longilobum* Steyerm, Mem. New York Bot. Gard. 10: 193. 1964.

Type: GUYANA. Pakaraima Mountains, Mount Ayanganna, occasional at forest edges between Ayanganna and Chinowiang, 1000-1200 m, 7-8 Feb. 1955, B. Maguire, W.M.C. Bagshaw & C. Maguire 40637 (holotype NY [barcode 00131041]; isotypes US [barcode 00137691], VEN [Acc. No. 49511]).

*Subshrubs* to *shrubs* 0.4-4 m tall; branches puberulent. *Stipules* broadly triangular to subtruncate, 2-5(-6) × 2-3 mm, shallowly obtuse when young or sometimes becoming bifid at apex when older, glabrous or puberulent outside, glabrous at distal portion and with the basal 2/3 covered by dense colleters inside. *Leaves* with petioles 3-7 mm long, 1-1.5 mm thick, glabrous; blades round, broadly elliptic, elliptic to obovate, 2-10 × 1.3-5.5 cm, obtuse to acute at base, truncate, obtuse or round at apex, coriaceous, dark green and shiny above, pale green below, drying brown to olive-green; glabrous above, densely puberulent below, margin sometimes minutely revolute, veins densely puberulent; secondary veins 7-13 each side, tertiary venation densely reticulate, impressed above and evident below; tuft-domatia always present. *Inflorescences* subsessile to long pedunculate, reduced-cymose, 1-7-flowered; peduncle 0.2-5.7 cm long; distal

bracts orbicular to broadly triangular, 1-5 × 1-3.5 mm; bracteoles scaliform or absent. *Flowers* with pedicels 1-3 mm long, glabrous to minutely puberulent. *Hypanthium* obconical or turbinate, 1-1.5 × 1-1.3 mm, glabrous or minutely puberulent. *Calyx* tube extremely reduced or absent; lobes subequal to unequal, oblong-triangular, ovate-lanceolate, oblong-lanceolate, lanceolate, elliptic to oblong-spathulate, 2-17 × 1-3.5 mm, glabrous to sparsely puberulent, with 3-5, oblong to linear, 0.25-0.5 mm long, colleters at each lobe sinus. *Corolla* infundibулiform, white to cream-white sometimes with tube red-dish or greenish at base, 17-31 mm long; tube infundibулiform, 10-18 mm long, 1-1.4 mm wide at base, 3-4.5 mm wide at mouth, glabrous outside, densely yellow-pubescent at mouth inside; lobes ovate, narrowly ovate to oblong-elliptic, 7-15 × 4-5.5 cm, round, obtuse, acute or short-acuminate at apex, glabrous outside, basally yellow-pubescent inside. *Short-styled flowers* (*Delprete & Benjamin 12860D*; tube 18 mm long, lobes 11 mm long): stamens included, inserted at 3 mm below corolla mouth; filaments 0.7 mm long; anthers narrowly oblong, 3 × 0.2-0.3 mm, acute at both ends; style included, about half the length of the corolla tube, 5.5-6.5 mm long, glabrous, style branches oblong, 1 mm long. *Long-styled flowers* (*Steyermark 59670*; tube 12 mm long, lobes 8 mm long): stamens included, inserted at 5-7 mm from base of corolla; filaments 0.5-0.7 mm long; anthers narrowly oblong, 2.5-3 × 0.2-0.3 mm, round to acute at base, acuminate at apex; style exerted well beyond corolla mouth, 11-18 mm long, style branches oblong, 1.2 mm long. *Capsules* ovoid to ellipsoid, 7-17 × 5-7 mm, obtuse to acute at base, rounded at apex, dark brown, appressed-puberulent, to sparsely pubescent. *Seeds* 2.5-4 × 2-3 mm.

**Notes:** Joseph Dalton Hooker (1876: 43-44, pl. 1148), along with the description of *Chalepophyllum guyanense*, cited "Hab. British Guiana, Schomburgh [Sic!]" without indicating the herbarium of deposit. A specimen at K has the handwritten label "12 last smallest, Remijia? British Guiana, Schomburgk." On the sheet of the specimen are drawn beautiful pencil sketches of flowers in anthesis, dissected corolla, young ovary and seeds that are almost identical to those illustrated in Plate 1148. This specimen is the holotype and, at the time I studied it, it did not have a barcode.

Steyermark (1964) distinguished *Chalepophyllum longilobum* Steyerm. from *C. guyanense* by the corolla

**Figure 6.** *Chalepophyllum guyanense.* A. Branch with inflorescences. B. Inflorescences with flowers in anthesis and flower buds. C-D. Stipule variation on the same branch. C. Entire stipule. D. Bifid stipule. E. Dissected long-styled flower. F. Dissected short-styled flower. G. Capsule. A-D: drawn from *Delprete & Araujo 7429* (CAY); E: drawn from *Steyermark 59670* (F); F: drawn from *Delprete & Benjamin 12860D* (CAY); G: drawn from *Delprete & Araujo 7428* (CAY). Illustration by Piero Delprete.
<figure><img src="image_10.png" /><figcaption>Figure 6.</figcaption></figure>
lobes 14–15 mm long (vs. 6–12 in *C. guyanense*) and the seeds 2.8–3 mm long (vs. 3–4 mm long). In the same publication, he also published *Chalepophyllum guyanense* var. *cuneatum* Steyerm., which he differentiated from the typical variety by having leaf blades obovate and acute at base (vs. oblong-obovate, rounded or narrowed at base). Recent collections demonstrated that the characters used by Steyermark to distinguish these three taxa are morphologically and geographically overlapping (Delprete et al. 2004), and they are here treated as synonymous. Also, Steyermark (1964, 1974) and other authors wrote the specific epithet as “guianense”, but it was originally published by J.D. Hooker (1873) as *guyanense* and must be maintained as such.

**Distribution and ecology:** Endemic to the Guiana Shield, in Venezuela, Guyana and northern Brazil (Fig-

ure 9); growing in scrub formations in sandy savannas with Rapateaceae Melastomataceae, Piperaceae and *Drosera*, wet savannas with *Stegolepis* and *Drosera*, white-sand savannas, open dwarf *Bonnettia* forests, and sandy valleys, at 300–1430 m altitude.

**Phenology:** Flowering and fruiting throughout the whole year.

**Suggested conservation status:** Least Concern (LC). This species is known from many localities in Venezuela, Guyana and northern Brazil. The size of the populations in all the localities is unknown. Personal observations in its natural environment were made in Venezuela in 2000, and in Guyana in 2016; the populations in these two localities were healthy, with more than 50 individuals, and with no immediate threats. In addition, this species

<figure><img src="image_11.png" /><figcaption>**Figure 7.** *Chalepophyllum guyanense.* A. Branch with inflorescences and infructescences. B. Detail of leaf blade abaxial side, showing reticulate-foveolate surface, and high magnification detail of depressed areoles. C. Seeds and detail of the testa. D. Dehisced capsule. E. Dissected corolla of short-styled flower, and detail of multicellular present at corolla mouth. Illustration by Bruno Manara (Reproduced with permission from Flora de Venezuela vol. 9(1), fig. 52. 1974).</figcaption></figure>
<figure><img src="image_12.png" /><figcaption>**Figure 8.** *Chalepophyllum guyanense*. A. Habit. B. Detail of inflorescence with flower buds and flowers in anthesis. C. Detail of distal portion of branches with flower buds and flowers in anthesis (note leaf revolute margin). Photos taken by Piero Delprete on June 2016, in the Kaieteur National Park, Guyana (plants not collected).</figcaption></figure>

grows in several protected areas, and in at least in three
national parks: the Canaima National Park, Venezuela,
the Kaieteur National Park, in Guyana, and the Monte

Roraima National Park, in northernmost Brazil. There-
fore, taking into account the numerous sites of occur-
rence, including many remote and preserved areas, and
its healthy populations, this species is here treated as Least Concern (LC) following IUCN criteria (IUCN 2012, 2019).

**Specimens exmined:** **VENEZUELA: Bolívar:** Gran Sabana, ca. km 167, S of El Dorado along hwy to Santa Elena, 24 km S of La Ciudadella, 1300 m, 4 Dec. 1973 (fl), G. Davidse et al. 4825 (MO, NY); 2 km N of San Rafael de Kamoiren, km 174, area seasonally inundated with whitesand soil, dominated by Melastomataceae, Rapateaceae, Piperaceae, Drosera, 5°39'N, 61°24'W, 1300 m, 27 Dec. 2000, P.G. Delprete & A.C. Araujo 7424 (imm fr) (CAY, NY, UFG, VEN), 7426 (imm fr) (CAY, L, MO, US), 7428 (fl, fr) (CAY, GB, NY, UFG, VEN), 7429 (fl, imm fr) (BR, F, NY, P, UFG, VEN); Piar, extremo N de la Gran Sabana, Carretera El Dorado-Santa Elena de Uirén, ca. 100 km S of El Dorado, 5°40'N, 61°30'W, 1300 m, 3 Apr. 1985 (fl), B.K. Holst et al. 2158 (MO); Distr. Roscio, Sabana ca. 10 km N del Kamá-meru, mano derecho de la Carretetra Sta. Elena de Uirén-Luepa, 5°29'N, 61°18'W, 1180 m, 4 Mar. 1983 (fr), O. Huber et al. 7330 (P, US); Dtto. Piar, sabana arbustiva ubicada en el paso entre Ptari-tepui y Soropán-tepui, al N de Kavanayén, 5°42'N, 61°45'W, 1370 m, 28 Jun. 1983 (fl, fr), O. Huber & C. Alarcon 7713 (NY [2 sheets], US, VEN); Dtto. Piar, sabanitas ubicadas sobre altiplanicie al NE del Aprada-tepui, ca. 40 km al ENE de Urimán, 5°30'N, 62°20'W, 930 m, 12 Dec. 1984 (fl, fr), O. Huber et al. 9904 (NY, US, VEN); ibid., 5°40'N, 62°50'W, 900 m, 12 Dec. 1984 (fl, fr), O. Huber et al. 9918 (NY, VEN); Dtto. Roscio, sabanas y arbustales en la cuenca superior meridional del Río Kamurán, ca. 20–25 km al NW del Ilu-tepui, 5°37'N, 61°13'W, 1000 m, 18 Jun. 1985 (fl, fr), O. Huber & C. Alarcon 10616 (NY, VEN); Dtto. Sifontes, sabana arbustiva sobre planicie ubicada a la ribera izquerda (Sur) del Río Yuruaní medio, ca. 5 km al franco Sur del Wadakaoué-tepui, 5°17'N, 60°53'W, 1050 m, 5 Sep. 1986 (fl, imm fr), O. Huber 11765 (NY, US, VEN); Mun. Gran Sabana, [Canaima National Park], Sierra de Lema, 70 km NNE de Kavanayén, 1650 m, 30 Jan. 1988, O. Huber 12497 (US, VEN); Mun. Gran Sabana [Canaima National Park], herbazal y arbustal tepuyano en el sector occidental de la Sierra de Leme, a lo largo de un afluente oriental del Río Carrao alto, ca. 70 km al NNE de Kavanayén, 5°58'N, 61°37'W, 1250 m, 31 Jan. 1988 (fr), O. Huber 12518 (INPA, U, US); ca. 1 km S of Military Base, just N of turnoff to Kavanayen by VEN-10, 24 Jul. 1983 (fl), R. Kral & Á.C. González 70383 (MO); Gran Sabana, ca. 1 km E of Kavanayen, 26 Jul. 1983 (fl, fr), R. Kral & A.C. Gonzalez 70500 (NY); Guayana venezolana, Kavanayen, 28 May 1945 (fl), T. Lasser 1824 (NY, VEN); Gran Sabana, km 137 along El Dorado-Santa Elena rd, 1420 m, open savanna, 16 Nov. 1978 (fl, fr), J.L. Luteyn et al. 6278 (NY); Ilu-Tepui, Gran Sabana, between Urupata and Enemasic, 1000 m, 8 Feb. 1952 (fl, young fr), B. Maguire

33244 (NY, US, VEN); Ilu-Tepui, Gran Sabana [Canaima National Park], Mesa Grande, savanna thickets and bush islands, area dominated by Stegolepis and Bonnetia, 1600 m, 12 Mar. 1952 (fl), B. Maguire 33357 (NY, P, VEN); Ptari-tepui, SW slop forest and savanna, 1500 m, 17 Dec. 1952 (fl), B. Maguire & J.J. Wurdack 33922 (IAN, NY, US, VEN); Ptari-tepui, slopes and rocks in vicinity of “Cave Rock,” below S face of mountain, savanna S of Ptari-tepui, 1.5 hours from “Cave Rock” by foot, soil moist with scattered shrubs, 1600–2000 m, 14–19 Aug. 1970 (fl), H.E. Moore Jr. et al. 9731 (F, NY); Gran Sabana, treeless wet savanna, ca. 16 km E of the mission at Kavanayén, 1340 m, 19 Dec. 1979 (fl, fr), J. Pruski & J.A. Steyermark 1417 (NY); Gran Sabana, Parque Nacional Canaima, Carrettera Fuerte, Luepa-Santa Helena, km 168, 19 Mar. 1993 (fl), N. Ramírez 3552 (MO), 3553 (MO); Gran Sabana, Parque Nacional Canaima, Carrettera Fuerte, Luepa-Santa Heleña, 20 Mar. 1993 (fl, fr) N. Ramírez 3742 (MO); Gran Sabana, Parque Nacional Canaima, Carrettera Fuerte, Luepa-Kavanayén, desvio hacia Rinoroíto, 23 Mar. 1993 (fl, fr) N. Ramírez 4077 (MO); Gran Sabana, between Mission of Santa Teresita de Kavanayén NW to Río Karuai, on large mesa, 1220 m, 26 Oct. 1944 (fl), J.A. Steyermark 59359 (F, NY, US, VEN); Ptari-tepui, dry sandy and rocky sandstone exposure on level ground adjacent to swamp on plateau-portion of SE facing slopes, 1600 m, 1 Nov. 1944 (fl), J.A. Steyermark 59670 (F, NY, US, VEN); vicinity of Misia Kathy Camp, on mesa between Ptari-tepui and Sororopán-tepui, 1615 m, 15–17 Nov. 1944 (fl, fr), J.A. Steyermark 60233 (F, NY, US); Uei-tepui, between SE slope and summit, between Luepa and Cerro Venamo, 1100–1300 m, 19 Apr. 1960 (fl), J.A. Steyermark & S. Nilsson 60348 (F, NY, US, VEN); near rd Campamento 150, at 150 km in valley of savanna of Río Uarama below Uarama-tepui, NE of Luepa, 1220 m, 24–25 Apr. 1960 (fl), J.A. Steyermark & S. Nilsson 60644 (NY, VEN); Gran Sabana [Canaima National Park], altiplanicie de suelo arenoso, formación Roraima, drenaje de las cabeceras del Río Aponguao, sabana pantanosa entre Río Arautá-parú (km 148–150 S de El Dorado), 1350–1400 m, 20 Dec. 1970 (fl), J.A. Steyermark et al. 104111 (NY, P, VEN).

**GUYANA:** Upper Mazaruni River Region, Karowtigu Mountain, E end of mountain, 1000 m, 21 Apr. 1987 (fl), B.M. Boom & D. Gopaul 7604 (MO, NY); Cuyuni-Mazaruni Region, Utshi River, trail to Santa Elena (Venezuela), 5°39'N, 61°9'W, 980 m, 31 Jan. 1996 (fl), H.D. Clarke 918 (BRB, MO, NY, U); Paruima, 20 km W, wet savanna on Waukauyengtipu, 5°49'58"N, 61°14'5"W, 1430 m, 17 Jul. 1997 (fl), H.D. Clarke et al. 5809 (BRB, MO, NY, U, US); Potaro-Siparuni Region, Mount Ayanganna, camp on summit plateau, 2040 m, 23 Jun. 2001 (fl), H.D. Clarke et al. 9490 (US); Kaieteur Plateau, near
Kaieteur Falls, ca. 426 m, savanna and low savanna-
forest, boggy area in savanna margin, 25 Feb. 1962 (fl,
fr), R.S. Cowan & T.R. Soderstrom 1945 (NY, US, VEN);
Potaro-Siparuni Region, Upper Potaro River, Chenapou
Village, Aklapanan Savanna, motorbike trail from
Chenapou Creek mouth towards Paramakatoi Village,
eight hills from creek mouth (ca. 10 km), then small trail
to the left, crossing a small waterfall, savanna frequently
burned with Pteridium arachnoides (fern) and Brochinia
micrantha (Bromeliaceae), bordered by trees 2-3 m tall,
on white-sand soil, 4°55'28"N, 59°34'33"W, 510 m, 16
Jun. 2016 (fl), P.G. Delprete & P. Benjamin 12860D (BRG,
CAY, GB, NY); Kaieteur National Park, between air-
strip and escarpment, ENE of airstrip, 5°11'N, 59°29'W,
450 m, 29 Mar. 1989 (fl), L.J. Gillespie & H. Persaud 916
(BRB, MO, NY, U, US); Kaieteur National Park, savanna
along airstrip, 5°10'30"N, 59°29'W, 420-450 m, 7 May

1989 (fl), L.J. Gillespie et al. 1349 (MO, NY, US); Potaro-
Siparuni Region, Kaieteur Falls National Park, 5°12′N,
59°29′W, 500 m, 7 May 1988 (fl), W. Hahn et al. 4092
(BRB, CAY, MO, NY, P, U, US); Potaro-Siparuni Region,
Kaieteur Falls National Park, 5°10′N, 59°29′W, 500 m, 12
Apr. 1988 (fr), W. Hahn et al. 4461 (BRB, MO, P, U, US);
Potaro-Siparuni Region, Kaieteur plateau, 3 km WNW
from Falls along Kaieteur-Kuribrong trail, seepage bog
and xeromorphic scrub forest mosaic on pink sand with
frequent sandstone outcrops, 5°12′N, 59°30′W, 540 m, 22
Jul. 1993 (fl, fr), T.W. Henkel & R. Williams 2357 (MO,
NY, U, US); Cuyuni-Mazaruni Region, Pakaraima Mts.,
base camp 11.4 km NE Imbaimadai Partang R., 1 km E,
5°48′N, 60°14′W, 675-700 m, 25 May 1992 (fl). B. Hoff-
man et al. 1849 (CAY, F, MO, NY, U, US); Pakaraima
Mountains, between Koatse River and Chenoweing Vil-
lage, 5°27′N, 60°04′W, 700-800 m, 12 Nov. 1992 (fl), B.

<figure><img src="image_13.png" /><figcaption>**Figure 9.** Distribution of *Chalepophyllum guyanense*.</figcaption></figure>
Hoffman & T. Henkel 3356 (BRB, MO, US); Potaro-Siparuni Region, Kaieteur Falls National Park, around airstrip, 5°10'N, 59°29'W, 300 m, 16 Jul. 1993 (fl), C.L. Kelloff et al. 972 (BRB, MO, U, US); Potaro-Siparuni Region, Kaieteur Falls, vicinity of Kaieteur airstrip, 5°11'N, 59°29'W, 450 m, 8 Oct. 1987 (fl, fr), L.P. Kvist et al. 101 (MO, NY, U, US); Pakaraima Mountains, Mount Aymatoi (sandstone), 5°55'N, 61°0'W, 1150 m, 15 Oct. 1981 (fl), P.J.M. Maas et al. 5716 (MO, NY, P, U, US); Kaieteur Plateau, 3 May 1944 (fl, fr), B. Maguire & D.B. Fanshawe 23169 (F, MO, NY, P, RB, U, US); Upper Mazaruni River, occasional in savanna, Samwarakna-tipu (Holitipu), 1100 m, 10 Nov. 1951 (fl, fr), B. Maguire & D.B. Fanshawe 32559 (NY, RB); Cuyuni-Mazaruni Region, Mt. Holitipu, on eroded sandstone and white sand, forrested creek below peak, 5°56'N, 61°05'W, 1150-1240 m, 1 Jun. 1990 (fl, fr), T. McDowell & D. Gopaul 3023 (F, MO, NY, P, US); E of Arabaru Creek, Kobadai Savanna, 5°27'N, 60°39'W, 500 m, 16 Jul. 1991 (fl), T. McDowell 4597 (BRB, MO, U, US); Potaro-Siparuni Region, Kaieteur National Park, Upper Mure Mure Basin, savanna on trail to Menzies landing, 5°15'27"N, 59°30'40"W, 480 m, 28 Mar. 2014 (fl, fr), F.A. Michelangeli 2565 (NY); Pakaraima Mountains, Ireng River at Kurutuik Falls, 5°05'N, 59°59'W, 670 m, 23 Oct. 1994 (fl), P. Mutchnick et al. 188 (BRB, MO, US); Cuyuni-Mazaruni Region, vicinity of Chinoweng Village, savanna and mixed forest, also Bonnetia-Moronobea associations along creeks, 5°32'N, 60°7'W, 650 m, 21 Feb. 1987 (fl, fr), J.J. Pipoly et al. 10478 (CAY, NY, US); Ayanganna Plateau, ca. 3 km N of Koatse River, due S of mountain central depression, 5°38'N, 60°4'W, 650-670 m, 27 Feb. 1987 (young fr), J.J. Pipoly & G. Samuels 10739 (F, MO, NY, U, US); Ayanganna Plateau, N of mountain center, 5°28'N, 60°4'W, 650-700 m, 1 Mar. 1987 (young fr), J.J. Pipoly & G. Gharbarran 10846 (BRB, MO, NY, U, US); Kako River vicinity, above Kako Village, near Camp 3, ca. 22 km air distance E of Tulameng Summit, 5°33'27"N, 60°59'35"W, 520 m, 26 Jul. 2010 (fl, young fr), K.M. Redden et al. 7089 (F, MO, US); Kaieteur Savannah, in thickets among Brochinia, by Indian trail, ca. 400 m, 4 Sep. 1934 (fl, fr), N.Y. Sandwith 1346 (K, NY, U); Kaieteur Savanna, sandy and gravelly place, 370 m ["1100 ft"], 30 Aug. 1933 (fl, fr), G.T. Tutin 676 (BM, RB, U, US); Potaro-Siparuni Region, Boy Scout Lookout & Johnsons Lookout, 5°10'46"N, 59°29'1'W, 466 m, 30 Aug. 2006 (fr), K.J. Wurdack et al. 4195 (P, U); Cuyuni-Mazaruni Region, Kato River, 490 m, 19 May 2009 (fl, fr), K.J. Wurdack et al. 5073 (US); Cuyuni-Mazaruni Region, below 1st escarpment (of four) of Kamakusa Mt., Partang Airstrip (presently non-operational) and vicinity, 734 m, 19 May 2012 (fl, fr), K.J. Wurdack et al. 5672 (US).

**BRAZIL. Roraima:** Uiramutã, Parque Nacional do Monte Roraima, Monte Caburaí, vegetação herbácearabustiva com afloramento e campos de Rapateaceae, 5°10'22"N, 60°13'57"W, 1322 m, 6 Nov. 2014 (fl, fr), R. Forzza et al. 8128 (INPA, RB); Uiramutã, Parque Nacional do Monte Roraima, Monte Caburaí, campos arbusativos com rapateaceae, 5°10'22"N, 60°13'57"W, 1320 m, 6 Nov. 2014 (fl, fr), G. Martinelli et al. 18392 (MG, NY, RB); Uiramutã, Parque Nacional do Monte Roraima, Monte Caburaí, campos de Rapateaceae intercalados com floresta ambrófila, 5°10'22"N, 60°13'57"W, 1322 m, 6 Nov. 2014 (fl, fr), M. Nadruz et al. 2861 (RB); Uiramutã, Parque Nacional do Monte Roraima, Monte Caburaí, imediações do marco de fronteira B-BG/11A, 5°10'22"N, 60°13'57"W, 1400 m, 6 Sep. 1998 (fl, fr), L.A. Pessoni 335 (UFRR).

## Excluded Species

*Chalepophyllum coriaceum* Gleason in Gleason & Killip, Brittonia 3: 192. 1939.

Type: VENEZUELA. Bolívar: Mount Auyan-Tepui, 2200 m, Dec. 1937 (fl, fr), G.H.H. Tate 1179 (holotype NY [barcode 00131038]; isotype VEN [not found]).

(=) *Maguireothamnus speciosus* (N.E.Br.) Steyerm. (see below).

*Chalepophyllum latifolium* Standl., Publ. Field Columbian Mus., Bot. Ser. 7: 379. 1931.

Type: VENEZUELA. Amazonas: Summit of Mount Duida, s.d. (fl, fr), 1320 m, G.H.H. Tate 730 (holotype NY [barcode 00131040]; isotype F [Acc. No. 603528]).

(=) *Maguireothamnus tatei* (Standl.) Steyerm. (see below).

*Chalepophyllum pungens* Standl. & Steyerm., Fieldiana, Bot. 28: 568. 1953.

Type: VENEZUELA. Amazonas: On open granitic rocks at Puerto Ayacucho, 100 m, 18 May 1940 (fr), Ll. Williams 12970 (holotype F [Acc. No. 1078932]; isotypes F [Acc. No. 1609002], US [barcode 00137692], VEN [Acc. No. 15136]).

(=) *Acanthella sprucei* Hook.f. in Bentham & J.D.Hooker (1867: 749; Melastomataceae).
Standley and Steyermark (1953: 568, 570) described *Chalepophyllum pungens* Standl. & Steyerm., using specimens with open capsules and seeds, and cited as the type *Llewelys Williams 12970* at F. There are two sheets of *Williams 12970* at F, which are kept together in the same folder. Sheet with Accession No. 1078932 is annotated in Standley's handwriting "Type. Chalepophyllum pungens Standl. & Steyerm." and that with Accession No. 1609002 is annotated in Standley's handwriting "Iso-Type. Chalepophyllum pungens Standl. & Steyerm."

*Chalepophyllum speciosum* N.E.Br., Trans. Linn. Soc. London II, 6: 33. 1901.

Type: VENEZUELA. Bolívar: F.V. McConnell & J.J. Quelch 653 (first-step lectotype, designated by Steyermark (1964: 223), **second-step lectotype** K [without barcode, with label "New York Botanical Garden Neg. No. N.S. 3240 (1953)"], **here designated**; isotype type BM [barcode BM000614299].

(=) *Maguireothamnus speciosus* (N.E.Br.) Steyerm.
(see below).

Brown (1901: 33) described *Chalepophyllum speciosum* and cited three syntypes "McConnell & Quelch 100, 305, 653." Steyermark (1964: 223) among the specimens studied for this species cited "McConnell & Quelch 653 (photo of holotype of *Chalepophyllum speciosum*, from K at NY)." Although Steyermark cited this collection as holotype, according to Art. 7.11 and 9.10 of the *Code* (Turland et al. 2018) is a correctable error, and it is here treated as an inadvertent first-step lectotypification of *McConnell* & *Quelch 653* at K because there are two specimens of *McConnell* & *Quelch 653* at K. At the time they were studied, these specimens did not have barcodes. The specimen with the label "New York Botanical Garden Neg. No. N.S. 3240 [1953]," which has eight branchlets with flowers is here designated the second-step lectotype of this taxon. The other specimen with three branchlets with flowers, and without the NYBG label, is an isotype type.

*Chalepophyllum tatei* Standl., Publ. Field Columbian Mus., Bot. Ser. 7: 380. 1931.

Type: VENEZUELA. Amazonas: Mount Duida, summit of Peak N. 7, 2130 m, Aug. 1928-Apr. 1929 (fl, fr), *G.H.H. Tate* 623 (holotype NY [barcode 00131042]; isotype F [Acc. No. 603541]).

(=) *Maguireothamnus tatei* (Standl.) Steyerm. (see below).

## 2. DENDROSIPANEA

*Dendrosipanea* Ducke, Arch. Inst. Biol. Veg. 2(1): 69. 1935 Emend. Steyerm. in Mem. New York Bot. Gard. 10: 195-199, fig. 71. 1964; Steyerm. in Lasser & Steyermark, Fl. Venezuela 9(1): 326-330, fig. 53. 1974; Delprete & Steyerm. in Steyermark et al., Fl. Venez. Guayana 8: 571, fig. 454. 2004; Delprete, Phytotaxa 382(1): 125-135. 2018.

Type: *Dendrosipanea spigelioides* Ducke

*Shrubs or treelets. Stipules* free or basally adnate to petioles, deltoid, acuminate or bifid, with basal 2/3 covered by dense colleters intermixed with hairs inside. *Leaves* opposite, subsessile to short-petiolate; blades oblong, spathulate or oblanceolate, subcoriaceous; doma-tia absent. *Inflorescences* terminal or terminal on distal axillary branches, cymose, sometimes frondose, few- to many-flowered. *Flowers* distylous, 5-merous. *Hypanthium* obconical, turbinate to narrowly obovoid. *Calyx* funnel-shaped, tube extremely reduced or absent with lobes free at base, persistent; lobes subequal to unequal, deltoid, nar-rowly triangular, oblong, narrowly oblong, lanceolate, or spathulate, with 1-4 minute colleters each lobe sinus. *Caly-cophylls* absent. *Corolla* hypocrateriform, actinomorphic, white to cream-white, sometimes with tube green; tube narrowly infundibuliform, glabrous or sparsely appressed-strigulose or hirtellous outside, basal portion glabrous and medio-distal portion villous inside, with a dense ring of yellow hairs at mouth inside; lobes left-contorted, some-times asymmetrical, ovate, narrowly ovate, oblong to ovate-oblong, margin entire, obtuse to acute at apex. *Pol-len* 4-colporate; exine foveolate or foveolate-reticulate, per-forate. *Short-styled flowers:* stamens included or partially exserted, inserted at distal portion of corolla throat; filaments short; anthers linear; style included, much shorter than corolla tube, style branches oblong. *Long-styled flow-ers:* stamens included, inserted at basal portion of corolla throat; filaments short; anthers linear; style barely exserted (only branch tips beyond corolla mouth), style branches oblong. *Ovary* with a fleshy placental extension adnate along the entire length of the septum; ovules irregularly peltate on the longitudinal placental extension. *Fruit* caps-sular, dehiscing septicidally, thinly woody. *Seeds* antrorsely peltate along the central placenta, minute, 3-5-angular or irregularly-shaped; testa reticulate.

**Taxonomic observations:** Ducke (1935) published the new genus *Dendrosipanea* Ducke, positioned it in the Ron-deletieae, and described it as having loculicidal capsules. Steyermark (1964: 195-196) corrected Ducke's error, as its capsules are septicidal. *Dendrosipanea* is most similar to