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Research Article
New Piper species from the eastern slopes of the Andes in northern South America
expand article infoWilliam Trujillo‡, Edwin Trujillo Trujillo§, Fausto Andrés Ortiz-Morea§, Diego A. Toro§, M. Alejandra Jaramillo|
‡ Grupo Investigaciones territoriales para el uso y conservación de la biodiversidad. Fundación La Palmita, Bogotá, Colombia
§ Universidad de la Amazonia, Florencia, Colombia
| Universidad Militar Nueva Granada, Bogotá, Colombia

Corresponding author: William Trujillo ( williamtrujilloca@gmail.com )

Academic editor: Elton John de Lirio
© 2022 William Trujillo, Edwin Trujillo Trujillo, Fausto Andrés Ortiz-Morea, Diego A. Toro, M. Alejandra Jaramillo.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Trujillo W, Trujillo ET, Ortiz-Morea FA, Toro DA, Jaramillo MA (2022) New Piper species from the eastern slopes of the Andes in northern South America. PhytoKeys 206: 25-48. https://doi.org/10.3897/phytokeys.206.75971
Open Access

Abstract

We describe four new species of Piper from the Amazonian slopes of the northern Andes. Piper hoyoscardozii is distinguished from similar climbing species, P. dryadum and P. flagellicuspe, by its longer peduncles. The Amazonian species Piper indiwasii is distinguished from P. scutilimbum from Panama and northern Colombia by the narrowly spatulate leaf base extension. Piper nokaidoyitau is characterised by the presence of larger leaves and longer spikes than similar species, P. anonifolium and P. hostmannianum. Finally, P. velae is characterised by cordulate leaf bases in all nodes, petioles 0.8–1.5 cm long and pubescent fruits, which easily distinguish it from the related species, P. holdridgeanum.

Keywords

Colombia, Ecuador, north-western Amazon, Peru, Piper hoyoscardozii, Piper indiwasii, Piper nokaidoyitau, Piper velae, Piperaceae

Introduction

Piper L. is the most diverse and representative genus in Piperaceae, encompassing ca. 2600 species (Callejas-Posada 2020). Piper represents an extraordinary diversification amongst early diverging angiosperms. It is a Pantropical group (Jaramillo and Manos 2001) and its highest diversity lies in the Neotropics (ca. 1800 species; fide Ulloa-Ulloa et al. 2018 onwards). The growth forms of the genus are very variable and are most commonly perennial shrubs and suffrutices, growing mainly in the understorey of rainforests. Additionally, other Piper species are lianas, rarely caulescent herbs, hemi-epiphytes or trees not taller than 15 m (Callejas-Posada 2020). Piper is characterised by simple, alternate leaves and jointed stems with enlarged nodes; many species produce pearl bodies on the leaves or stems (Tepe et al. 2004), but the most distinctive morphological feature of the genus is the production of solitary spikes, upright or pendant, which contain dozens to thousands of apetalous flowers. Many Piper species are rich in essential oils, which can be found in many tissues and organs, including the fruits, seeds, leaves, branches, roots and stems (Salehi et al. 2019). Although very few species have significant global economic value, many are locally important for their use by native populations for medicinal and culinary purposes (Colvard et al. 2006; Cáceres and Kato 2014).

Piper has an extensive history of taxonomic and nomenclatural instability. The leading causes for that uncertainty are the challenges of interpreting morphological characteristics and the limited geopolitical circumscription of taxonomists’ work (Ramírez-Amezcua 2016; Callejas-Posada 2020). Piper flowers are small and morphologically homogeneous and the number of stamens and their position, characters of diagnostic importance, are challenging to see or interpret. Not all stamens develop at anthesis (Tucker 1982a, b) and the anthers, articulated at the filaments, fall off quickly after anthesis (Valentin-Silva et al. 2018). Many Piper species present foliar dimorphism and many specimens do not include leaves of both monopodial and sympodial axes. Description of new species, based on incomplete specimens, has led to the publication of superfluous names that later need to be submerged in synonymy (Ramírez-Amezcua 2016). Furthermore, because floristic treatments are often limited to specific countries, many species are given several names across borders (Ramírez-Amezcua 2016). Extensive fieldwork and comparisons with collections (including digitised collections) are essential to improve the taxonomy of this species-rich genera.

Observing species in the field is imperative to ensure detailed descriptions and complete specimens that support an excellent Piper taxonomy. Numerous essential characters cannot be included or are lost in dry specimens. Fortunately, in the last decade, W. Trujillo has collected and studied more than one thousand (1000) specimens from the Amazonian slopes of the Colombian Andes. Some of them have become type specimens of recently-described taxa (Trujillo and Callejas 2015; Trujillo and Jaramillo 2019, 2021). Continued work by the authors will bring to light more diversity in the future.

The present contribution describes four new Piper species from the Amazonian slopes of the Andes in Colombia, Ecuador and Peru. We use the nuclear ribosomal internal transcribed spacer (ITS) to determine their phylogenetic relationships within Piper. We increase to 419 the number of Piper species known from Colombia (Bernal et al. 2015).

Materials and methods

Fieldwork was conducted along the Amazonian slopes of the Andes in southern Colombia, in the Department of Caquetá, during 2010–2020. We collected silica gel-dried leaf tissue samples for DNA extractions. Detailed observations in the field and examination of available herbarium collections were used to describe growth habits and phenological stages accurately. We deposited botanical specimens in COAH, COL, HUAZ and HUA (acronyms according to Thiers 2019). Detailed comparisons with morphologically similar species allowed us to recognise the four new species. Besides reviewing the literature (Trelease 1936; Trelease and Yuncker 1950; Brako and Zarucchi 1993; Jørgensen and León-Yánez 1999; Jørgensen et al. 2014; Jardim Botânico do Rio de Janeiro 2020), we examined specimens through visits to Herbaria COAH, COL, HUA, HUAZ, GH, NY, PMA, RSA and US and digitised plant specimens available on the web (e.g. JSTOR Global Plants, https://plants.jstor.org/). Measurements included here were taken from specimens collected in Colombia. To describe leaf architecture, we used terminology proposed in the Manual of Leaf Architecture (Ellis et al. 2009). To assess conservation status, we calculated area of occupancy (AOO) and extent of occurrence (EOO) using R and the package ConR (Dauby et al. 2017).

We extracted DNA from all the new species (Table 1) using a CTAB method (Doyle and Doyle 1987). We amplified the nuclear ribosomal internal transcribed spacer (ITS) according to Jaramillo and Manos (2001) and aligned sequences using previous alignments as a guide (Jaramillo et al. 2008). First, we included the new sequences in our 900+ Piper ITS alignment, to determine the relationships of the new Piper species. This preliminary analysis (not shown) served to select representatives of each major clade of Piper (Jaramillo et al. 2008) for the analysis presented here. Forty-two species of Piper, 35 from the Neotropics and seven from Asia were selected to provide comparisons with the new taxa. Maximum Likelihood (ML) phylogenetic and bootstrap (100 replicates) analyses were conducted using RAxML (Stamatakis 2014) using species from the Asian tropics to root the phylogeny.

Table 1.
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GenBank accessions for new species and reference taxa. Other GenBank accessions are available in original manuscripts (Jaramillo et al. 2008). New species in bold.

Taxon Voucher GenBank Accession ITS Collection * Publication
Piper abalienatum Trel. MAJ 552 EU581075 DUKE Jaramillo et al. (2008)
Piper abbreviatum Opiz MAJ 203 EU581076 DUKE Jaramillo et al. (2008)
Piper aduncum L. MAJ 76 AF275157 DUKE Jaramillo & Manos (2001)
Piper alatabaccum Trel. & Yunck. AL 1177 KJ930372 INPA Molina-Henao et al. (2016)
Piper albispicum C. DC. MAJ 388 AY572317 DUKE Jaramillo & Callejas (2004)
Piper albozonatum C. DC. MAJ 697 AY326195 DUKE Jaramillo & Callejas (2004)
Piper amalago L. MAJ 561 AF215186 DUKE Jaramillo & Manos (2001)
Piper amplum Kunth MAJ 804 EU581096 RB Jaramillo et al. (2008)
Piper anonifolium Kunth AL 1242 EU581084 MG Jaramillo et al. (2008)
EJT 527 EU581101 MU Jaramillo et al. (2008)
Piper arboretum Aubl. MN 1565 EU581106 RB Jaramillo et al. (2008)
Piper biolleyi C DC. CD 10896 EU581128 SRP Jaramillo et al. (2008)
Piper brachypodon (Benth.) C. DC. MAJ 757 AY326198 DUKE Jaramillo & Callejas (2004)
Piper breviamentum C.DC. MAJ 221 EU581134 DUKE Jaramillo et al. (2008)
Piper callosum Ruiz & Pav. MJK 161 EU581142 SPF Jaramillo et al. (2008)
Piper candollei Sodiro EJT 1449 EF056237 MU Jaramillo et al. (2008)
Piper capense L. CD 11004 EU581143 SRP Jaramillo et al. (2008)
Piper cavendishoides Trel. & Yunck. MAJ 70 AF275153 DUKE Jaramillo & Manos (2001)
Piper cinereum C. DC. MAJ 66 AF275190 DUKE Jaramillo & Manos (2001)
Piper cocornarum Trel. & Yunck. RC 12493 AY326203 HUA Jaramillo & Callejas (2004)
Piper cordulatum C. DC. BCI-EL EU581167 Jaramillo et al. (2008)
Piper darienense C. DC. MAJ 103 AF275181 DUKE Jaramillo & Manos (2001)
Piper dilatatum Rich. MAJ 858 EU581179 RB Jaramillo et al. (2008)
Piper dryadum C. DC. EJT 1047 EU581186 MU Jaramillo et al. (2008)
Piper excelsum G. Forst. N. V. EF635476 Jaramillo et al. (2008)
Piper filistilum C. DC. MAJ 157 AF275155 DUKE Jaramillo & Manos (2001)
Piper flagellicuspe Trel. & Yunck. MAJ 65 AF275154 DUKE Jaramillo & Manos (2001)
Piper hartwegianum (Benth.) C. DC. MAJ 781 AY326207 DUKE Jaramillo & Callejas (2004)
Piper hispidum Sw. MCS 304 EU581241 RB Jaramillo et al. (2008)
Piper holdridgeanum W. C. Burger CD 10865 EU581247 SRP Jaramillo et al. (2008)
JF 9128 EU581248 MO Jaramillo et al. (2008)
Piper hostmanianum C. DC. SM 25228 EU581251 NY Jaramillo et al. (2008)
EJT 573 EU581249 MU Jaramillo et al. (2008)
Piper hoyoscardozii WT 4127 OK235346 UMNG This study
WT 4004 OK235347 UMNG
WT 4099 OK235348 UMNG
Piper imberbe Trel. & Yunck. AB 983 EU581255 SEMO Jaramillo et al. (2008)
Piper indiwasii ET 7254 OK235342 JBB This study
EJT 1438 EU581390 MU Jaramillo et al. (2008)
Piper maxonii C. DC. EJT 370 EF056270 MU Jaramillo et al. (2008)
Piper multiplinervium C. DC. MAJ 139 AF275168 DUKE Jaramillo & Manos (2001)
Piper nokaidoyitau WT 4171 OK235339 COAH This study
WT 4258 OK235340 COAH
ET 7249 OK235341 COAH
Piper novogranatense C. DC. MAJ 71 EU581317 DUKE Jaramillo et al. (2008)
Piper peltatum L. MAJ 564 EU581335 DUKE Jaramillo et al. (2008)
Piper retrofractum Vahl. MAJ 395 AF275196 DUKE Jaramillo & Manos (2001)
Piper sanctum (Miq.) Schltdl. ex C. DC. AB 744 EU581382 SEMO Jaramillo et al. (2008)
Piper scutilimbum C. DC. WT 4151 OK235343 UMNG This study
Piper scutifolium Yunck. MAJK 281 EU581389 SPF Jaramillo et al. (2008)
Piper sorgosonum C. DC. MAJ185 AY572320 DUKE Jaramillo & Manos (2001)
Piper spoliatum Trel. & Yunck. MAJ 60 AF275179 DUKE Jaramillo & Manos (2001)
Piper subscutatum C. DC. EJT 1604 EU581406 MU Jaramillo et al. (2008)
Piper trianae C. DC. MAJ 662 EU581413 DUKE Jaramillo et al. (2008)
Piper truncatum Vell. MAJ 937 EF056291 RB Jaramillo et al. (2008)
Piper tuberculatum Jacq. MAJ 710 AY326225 DUKE Jaramillo & Callejas (2004)
Piper umbellatum L. MAJ 35 EU581433 DUKE Jaramillo et al. (2008)
Piper umbricola C. DC. EJT 1014 EU581435 MU Jaramillo et al. (2008)
Piper velae WT 4058 OK235344 UMNG This study
WT 3995 OK235345 UMNG
Piper viçosanum Yunck. MAJ 809 EU581440 RB Jaramillo et al. (2008)
Piper yanaconasense Trel. & Yunck. MAJ 774 AY326229 DUKE Jaramillo & Callejas (2004)

*Collections: COAHH, Herbario Amazónico Colombiano; DUKE, Duke University Herbarium, UMNG: Herbario Universidad Militar Nueva Granada; HUA, Herbario de la Unviersidad de Antioquia; INPA, Instituto Nacional de Pesquisas da Amazônia; MG, Museu Paraense Emílio Goeldi; MU, Miami University Herbarium; NY, New York Botanical Garden Herbarium; RB, Herbario Jardim Botânico do Rio de Janeiro; SEMO, Southeast Missouri State University Herbarium; SPF, Herbario da Universidade de São Paulo; SRP, Snake River Plains Herbarium (University of Idaho).

Results

Phylogenetic analyses identified the relationships of the new species described here (GenBank accession numbers are provided in Table 1). The ML tree placed Piper hoyoscardozii and Piper nokaidoyitau within the Radula clade, Piper indiwasii species within Oxodium (= Schilleria, Callejas-Posada 2020) and Piper velae forms a clade with Piper holdridgeanum W. C. Burger (1971: 144–145), sister to the Macrostachys clade (Fig. 1).

Figure 1. 

Phylogenetic relationships of species described in this manuscript, based on Maximum Likelihood analysis of nrITS sequences. New species are shown in bold. Species with peltate leaves are underlined. Numbers above branches are ML bootstrap support values (> 80).

Taxonomic treatment

Piper hoyoscardozii W. Trujillo-C & M. A. Jaram., sp. nov.

urn:lsid:ipni.org:names:77303983-1
Figs 1, 2, 3 and 4

Type

Colombia. Caquetá: Florencia, vereda Sucre, 1076 m elev., 1°47'50"N, 75°38'50"W, 18 Oct 2020 [fr], F. Hoyos 049 (Holotype COL, Isotype COAH, HUA, UMNG)

Diagnosis

Piper hoyoscardozii W. Trujillo & M. A. Jaram. is similar to P. dryadum C. DC. (1891:221) and P. flagellicuspe Trel. & Yunck. (1950:59) from which it is easily distinguished by peduncles 2–3 cm long, spikes long-apiculate and fruit with stigmas sessile vs. peduncle 0.5–1 cm long, spikes not-apiculate and fruit with stigmas on a short style in P. flagellicuspe and P. dryadum.

Description

Shrub with sarmentose branches. Internodes (1)3–7 cm long, smooth, green, pubescent, trichomes pluricellular, uniseriate, 1–2.3 mm long, idioblasts not visible. Prophylls caducous, 1.2–1.5 cm long, green-whitish, pubescent, trichomes pluricellular, uniseriate, 0.2–1.0 mm long, dispersed on the abaxial surface, idioblasts not visible. Petioles uniform in size along all axes, 0.5–0.8 cm long, vaginate on the basal half, smooth and pubescent. Leaf-blades membranaceous, drying black, uniform in shape and size on all nodes, (5)6–7 × (13)15–17 cm, elliptic, symmetric, base cordate to rounded, apex acuminate; leaf blade smooth, pubescent on both surfaces, trichomes pluricellular, uniseriate, 0.5–2.3 mm long, dispersed on the adaxial surface, along first and second order nerves and dispersed on the areolas and third order nerves of the abaxial surface, eciliate; pinnately nerved from the lower 1/3, 2–3 nerves on each side, with spacing uniform or decreasing and angle increasing gradually towards the base, eucamptodromous, tertiary veins percurrent. Inflorescence and infructescence a simple spike, erect; peduncle 2–3 cm long, pubescent, green; rachis in flower 4–7 cm long, rachis in fruit 7–9 cm long, rachis with a 10–15 mm long, sterile green apical extension, fruits densely grouped along the rachis. Floral bracts cucullate, reddish in flower, triangular from above, 0.4–0.6 × 0.7–0.8 mm, glabrous on the adaxial surface, margin fimbriate, bracts forming bands around the spike. Flowers with four stamens, filaments 0.6–0.8 mm long, anthers 0.4–0.6 × 0.5–0.7 mm, longitudinally dehiscent, dithecous, with connective not protruding, glabrate, idioblasts not evident, black when dried. Sessile stigmas. Fruits rectangular, laterally compressed, green when alive and black when dry, 0.9–1.2 × 1.5–1.9 mm, pubescent, partially immersed in the rachis, with persistent sessile stigmas, 0.05–0.1 mm. Seeds oblong, laterally compressed, brown, smooth, 0.8–1 × 0.8–1.1 mm.

Distribution and habitat

Piper hoyoscardozii is a shade-loving sarmentose shrub that grows on trees and rocks. It is known from the Amazonian slope of the Andes in southern Colombia and Ecuador, between 1000–1500 m in elevation (Fig. 2).

Figure 2. 

The locality of four new Piper species from the Andes eastern slopes of Colombia, Ecuador and Peru.

Phenology

Flowering specimens were collected in July. Fruiting specimens were collected in August.

Etymology

This species name is dedicated to Fernando Hoyos Cardozo, a great companion during our floristic explorations of the Amazonian foothills and who collected the type specimen of this species in Caquetá.

Conservation status

This species is known from six specimen collections representing two subpopulations. The locations where it occurs are threatened by deforestation and expansion of the agriculture frontier, especially extensive cattle ranching. The extent of occurrence (EOO) of 876 km2 and area of occupancy (AOO) of 16 km2 are small, which, together with the continuing decline in quality of habitat, suggests it is Endangered [EN B1a+B2a].

Phylogenetic relationships

Piper hoyoscardozii belongs to the large clade Radula. A group of medium-size shrubs, mostly self-supporting, but some species are herbs or lianescent shrubs; leaves are plinerved or pinnately nerved. Flowers are densely arranged in spikes forming banding patterns and inflorescences can be erect or distally curved. Furthermore, this species is closely related to the clade of sarmentose shrubs occurring in wet tropical forests in Central America and the western slopes of the west Cordillera in Colombia (the latter corresponds largely to the Chocó Region) that includes P. brachypodon C. DC. (1869:327), P. cavendishioides Trel. & Yunck. (Trelease and Yuncker 1950: 85), P. dryadum, P. flagellicuspe, P. ottoniifolium C. DC. (1866:213), P. oxystachyum C. DC. (1898:255) and P. novogranatense C. DC. (1869:313) (Jaramillo et al. 2008).

Figure 3. 

Piper hoyoscardozii A sympodial branch B magnified view of the infrutescence C floral bract view from above D floral bract side view E anthers and distal portion of the filament F fruit side view G seed H floral diagram. Illustration by Marcela Morales based on F. Hoyos 049 COAH.

Discussion

Piper hoyoscardozii is a sarmentose shrub, a habit not commonly observed amongst Piper species in the study region (eastern slope of the Andes). The phylogeny (Fig. 1) places P. hoyoscardozii sister to other climbing Piper species occurring on the western slope of the Andes and wetter parts of Mesoamerica. Here we provide a comparative table for the climbing Piper species included in the phylogeny (Table 2). P. hoyoscardozii is easily differentiated because its spikes (in flower and fruit) have a long peduncle and a long apiculate apex.

Table 2.
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Comparison of Piper hoyoscardozii with related species of scandent habit.

Species Internodes indument Secondary nerves branch Peduncle length Rachis length Spike a pex Distribution
P. brachypodon (Benth.) C. DC. glabrous from the lower half 1 cm 5–7 cm obtuse Chocó Region
P. cavendishioides Trel. & Yunck. tomentulose from the lower one-fourth or one-third 1 cm 7–8 cm obtuse Chocó Region
P. dryadum C. DC. pubescent from the lower third 0.5–1 cm 5–6 cm obtuse Mesoamerica and Chocó Region
P. flagellicuspe Trel. & Yunck. velvety from the lower half 0.5 cm 4 cm obtuse Chocó Region
P. novogranatense C. DC. glabrous from the lower third 0.5 cm 4 cm obtuse Chocó Region
P. ottoniaefolium C. DC. glabrous near the base 0.5–1 cm 6–8 cm obtuse Chocó Region
P. xanthostachyum C. DC. glabrous from the lower third 0.5–1 cm 5–6.5 obtuse Mesoamerica and western slope of the Andes
P. hoyoscardozii W. Trujillo & M. A. Jaram. pubescent from the lower third 2–3 cm 7–9 cm long apiculate Eastern slope of the northern Andes
Figure 4. 

Piper hoyoscardozii A growth form, scandent shrub B upper leaf surfaces and spike C infructescence D leaf base and prophyll. Photos from F. Hoyos 049 by F. Hoyos

Specimens examined

Colombia: Caquetá, Florencia, vereda Tarqui, monumento Divino Niño, 1570 m elev., 1°50'0.3"N, 75°39'52.8"W, 30 Aug 2020 [fl], W. Trujillo & F. Hoyos 4120 (COAH, UMNG).; vereda Tarqui, quebrada Tarqui, 1530 m elev., 1°50'28"N, 75°39'42"W, 20 Aug 2020 [42], W. Trujillo 4099 (COAH); corregimiento El Caraño, vereda Sucre. 1076 m elev., 1°47'50.8"N, 75°38'50.5"W, 8 Jul 2014 [fl], W. Trujillo 3130 (COAH); vereda Sucre, Finca campamento Sucre. 1°46'52"N, 75°39'5.1"W. 1050 m elev,. 5 Jul 2012 [fl]. W. Trujillo & C. Malambo 2400; vereda Sucre, vía antigua Florencia-Huila, 1°47'50.8"N, 75°38'50.3"W, 1000 m elev., 24 Sep 2020 [fl], F. Hoyos 042 (COAH). Ecuador. Napo, Parque Nacional Sumaco-Galeras, 0°50'S, 77°34'W, 1090 m elev., 27 Oct 2005 [fr], J. Homeier & M.A. Chinchero 2000 (MO).

Piper indiwasii W. Trujillo-C & M. A. Jaram., sp. nov.

urn:lsid:ipni.org:names:77303984-1
Figs 1, 2, 5 and 6

Type

Colombia. Caquetá, municipio de San José del Fragua, ronda de bosque cerca al balneario Villa Collazos sobre el rio Fragua, 1°20'04"N, 75°59'28"W, 395 m elev., 14 May 2020, M. Angulo 1550 (Holotype COL, Isoptype COAH, HUA, HUAZ, UMNG).

Figure 5. 

Piper indiwasii A sympodial branch B lower leaf surfaces and details of the petiole C magnified view of the infructescence D floral bract view from above E floral bract side view F fruit side view G seed side view. Illustration by Marcela Morales based on Angulo 1550, COAH.

Diagnosis

Piper indiwasii W. Trujillo & M. A. Jaram. can be distinguished from P. scutilimbum C. DC. (1920a:242) by many attributes. Piper indiwasii has 1–1.7 cm long petioles, 7–8 pairs of secondary veins and a narrowly spatulate leaf base extension, 0.4–0.9(1.5) cm wide, vs. P. scutilimbum, which has a 4–6 cm long petioles, 10–12 secondary veins and an obtuse and rounded leaf-base extension, 2.5–4 cm wide. Piper indiwasii occurs in the Amazon watershed, on the eastern foothills of the Andes, while P. scutilimbum occurs west of the Andes in Panama and extends to Sierra Nevada de Santa Marta in northern Colombia.

Figure 6. 

Piper indiwasii A sympodial branch upper leaf surfaces B sympodial branch lower leaf surfaces C erect spikes. Photos from E. Trujillo 7249 by G. Delgado.

Description

Shrub , up to 2 m tall. Internodes 2–4(5) cm, canaliculate, green, glabrous. Prophylls not seen. Petioles are uniform in size along all axes, 1–1.7 cm long, vaginate along their entire length, canaliculate, glabrous. Leaf-blades coriaceous, drying grey to brown, uniform in size along all axes, (4.5)6–8.5 × (11)14–18 cm, elliptic, symmetric, leaf-base peltate, symmetric, with a narrowly spatulate extension, 0.4–0.9 × (0.5)1–2.3(2.5) cm, the leaf-base extension covering the petiole on sympodial nodes and orientated towards the axis on monopodial nodes, apex acuminate; leaf-blade glabrous on both surfaces, eciliate; pinnately nerved throughout, the nerves 7–8 on each side, brochidodromous, with spacing decreasing towards the base and angle uniform throughout, tertiary veins random reticulate. Inflorescences and infructescences a solitary spike, erect; peduncle 0.9–1.5 cm long, glabrous, green; rachis length in fruit (5)6–20 cm, fruits loosely grouped along the rachis. Floral bracts cucullate, triangular from above, 0.3–0.5 × 0.5–0.8 mm, glabrous on the adaxial surface, margin eciliate, not forming bands around the spike. Flowers with three stamens, filaments 0.5–0.8 mm long, anthers 0.3–0.5 × 0.2–0.3 mm long, longitudinally dehiscent, dithecous, with connective not protruding, glabrate, idioblasts not evident; stigmas 3, 0.05–1.5 mm long, sessile. Fruits obpyriform, green when alive and brown when dry, 0.6–0.8 × 0.9–1.2 mm, glabrous, partially immersed in the rachis, with stigmas persistent, 0.05–1.5 mm long, sessile. Seeds obpyriform, black.

Distribution and habitat

Piper indiwasii is known from the Amazonian slopes of the Andes in Colombia (Departments of Putumayo, Caquetá and Guaviare), Ecuador (Provinces of Guayas, Napo, Orellana, Pastaza and Sucumbíos) and Peru (Provinces of Amazonas), from 200 to 1,608 m elevation (Fig. 2). It occurs in lowland (sometimes along riverbanks) and lower montane forests. It is a shade-loving species that grows in the understorey and the edges of trails of preserved forests.

Phenology

Fruiting specimens were collected from December to June and August to October. Flowering samples were collected in March, April, May and December.

Etymology

Piper indiwasii is named after the Inga word meaning “House of the Sun”. Ingas or Inganos are an indigenous group belonging to the Quechua linguistic family. The Ingas of the Amazon foothills are made up of migratory groups from the Peruvian and Ecuadorian Amazon, the Mocoas and some survivors of the Andaquíes. The clans are united by their location, cosmovision and the culture of “yajé” (Banisteriopsis caapi) . Furthermore, the type specimen of this species was collected in the Alto Fragua Indi-Wasi National Park, located in San José del Fragua, Caquetá-Colombia.

Conservation status

Piper indiwasii is not endangered. It is known from 11 subpopulations and 12 localities; it has an EOO of 1,478,359 km2 and an AOO of 52 km2. According to IUCN guidelines, it is of Least Concern (LC) as the region where it occurs is threatened by deforestation and its conservation status should be monitored.

Phylogenetic relationships

Piper indiwasii belongs to the Neotropical clade Oxodium. Species in this group are shrubs, sometimes sarmentose. They have plinerved or pinnately nerved leaves, leaf bases are often acute or cordate and they have lax inflorescences with loosely arranged flowers (Jaramillo et al. 2008). Piper indiwasii is closely related to P. scutilimbum. Nucleotide difference between the two Piper indiwasii ITS accession is 5 bp out of 641 (0.8%), while these sequences have a 27 bp (4%) dissimilarity with P. scutilimbum (collected in the type locality). Sequence data and leaf material were available for five species of Neotropical Piper with peltate leaves. P. subscutatum C. DC. (1869:321) and P. imberbe Trel. & Standl. (Standley and Steyermark 1952:303–304) are in the Oxodium clade as P. indiwasii and P. scutilimbum; P. scutifolium Yunck. (1966:123–124) is part of the Ottonia clade; and P. maxonii C. DC. (1920b:16), P. hartwegianum (Benth.) C. DC. (1869: 369) and P. candollei Sodiro (1905:202) are members of the Macrostachys clade. Neotropical Piper species with peltate leaves do not form a monophyletic group and are part of at least four clades: Oxodium, Pothomorphe, Macrostachys and Ottonia (Fig. 1). Further studies are needed to shed light on the convergence of this trait.

Uses by communities

Various common names are used for P. indiwasii amongst indigenous communities in Ecuador: a) “ñahui tapa panga” (closed eye leaf) (D. Irvine & L. Cejua 1125, F, QCA); when a patient is sick and the eyes are closed even when awake, leaves are wrapped around tobacco and the smoke blown over the eyes of the patient; b) “uchi-ampar” a Shuar name, plant used against parasites, leaves and roots are used (Guerrero 171; Herrera 288, MO, QCNE); c) “palu sera aula” or the grandmother of palu sera, which is used for relieving toothache (D. Irvine 959, F, QCA).

Discussion

After reviewing the specimens identified as P. scutilimbum from Panama and northern Colombia vs. specimens from the eastern (Amazonian) Andes slope in Colombia, Ecuador and Perú (Fig. 2), we found a consistent difference in the leaf base shape between collections from both regions. The obtuse and rounded leaf base extension of the type specimen from the Sierra Nevada de Santa Marta coincides with that of specimens collected in Panama in contrast to the narrowly spatulate base extension seen in P. indiwasi. The leaf base shape, combined with other morphological characters and geographical distribution, clearly allows Piper indiwasii to be proposed as a new species. We provide a comparative table of morphological characters for species of Piper with peltate leaves that belong to the Oxodium clade (see Table 3).

Table 3.
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Comparison of Piper indiwasii with species of Piper with peltate leaves belonging to the Oxodium clade.

Species Leaf dimorphism* Leaf base extension width Leaf base extension shape Leaf width Geographic distribution
P. imberbe Trel. & Standley all leaves peltate 1.2–1.5 cm rounded 4.5–8 cm Mesoamerica
P. scutilimbum C.DC. all leaves peltate (2)2.5–4 cm obtuse and rounded 8–14 cm Mesoamerica and northern Andes
P. subscutatum (Miq.) C. DC present 2–4 cm obtuse and rounded 25–28 cm Eastern slope of the northern Andes and Amazonia
P. indiwasii W. Trujillo & M. A. Jaram. all leaves peltate 0.4–0.9 cm narrowly spatulate 4–18 cm Eastern slope of the northern Andes

* Leaves can be peltate or not.

Specimens examined

Colombia. Caquetá, San José del Fragua, ronda de bosque cerca al balneario Villa Collazos sobre el rio Fragua, 1°20'04"N, 75°59'28"W, 400 m elev., 29 Jun 2011 [fr], W. Trujillo et al. 1999 (COAH); Belén de los Andaquies, vereda las verdes, cerro Monserrate, entrada por dos quebradas, 1°36'38"N, 75°53'23"W, 700 m elev., 24 Jun 2011 [fr], W. Trujillo et al. 1990 (COAH); Belén de los Andaquies, Parque Natural Municipal Andaqui, cabeceras del rio pescado, 1°41'52"N, 75°54'15"W, 1608 m elev., 25 Jan 2017 [fr], N. Castaño et al. 8734 (COAH, HUA); Belén de los Andaquies, Parque Natural Municipal Andaqui, sector entre filo seco y la bocana de la quebrada las verdes, 1°37'13"N, 75°53'46"W, 600–800 m elev., 7 Feb 2017 [fr], N. Castaño et al. 9659 (COAH, HUA); Florencia, vereda Damas Arriba, finca el Mirador, 1°37'56"N, 75°41'49"W, 750 m elev., 14 Feb 2002 [fr], M. Correa et al. 2853 (COAH, UDBC); Guaviare, El Retorno, cerca del Retorno, granja de la Corporación Araracuara, zona ligeramente disectada, bosque intervenido, 1 Mar 1994 [fl], P. Stevenson 1168 (COAH); Putumayo, Villagarzón, corregimiento la Castellana, vereda la Pradera, finca el Cairo, bosque intervenido a borde de quebrada, 0°52'23"N, 76°45'27"W, 600 m elev., 10 Dec 1999 [fr], C. Marín & D. Cárdenas 1997 (COAH); Villagarzón, vereda la Kofaina, 1°01'00"N, 77°17'00"W, 550–700 m elev., 2 Sep 1993 [fr], A. Cogollo et al. 6830 (COAH, JAUM, MO); Ecuador. Napo, Estación Biológica Jatun Sacha, 1°04'00"S, 77°37'00"W, 450 m elev., 10 Oct 2007 [fr], J. Homeier et al. 2834 (MO, QCA, QCNE, GOET); Estación Biológica Jatun Sacha, rio Napo, 8 km debajo de Misahualli, 1°04'00"S, 77°36'00"W, 450 m elev., 17 Jan – 6 Feb 1987 [fr], C. Cerón 638 (MO, HUA); Estación Biológica Jatun Sacha, rio Napo, 8 km debajo de Misahualli, 1°04'00"S, 77°36'00"W, 450 m elev., 19–28 Mar 1987 [fr], C. Cerón 1063 (HUA, MO); 9 km rio debajo de puerto Misahualli y 2 km al sur de la cuenca del rio Chinguipino, 1°05'00"S, 77°36'00"W, 430 m elev., 10 Mar 1985 [fr], D. Neill et al. 6054 (ECUAMZ, HUA, MO, NY, QCNE, US); Tena, Estación Biológica Jatun Sacha, rio Napo, 8 km E of puerto Misahualli, 1°04'00"S, 77°36'00"W, 400 m elev., 18 May 1985 [fr], W. Palacios 421 (AAU, HUA, MO, NY, QCNE, US); Tena, Estación Biológica Jatun Sacha, along S bank of rio Napo, 8 km E of puerto Misahualli, 1°04'00"S, 77°36'00"W, 450 m elev., 1 Apr 1992, T. Croat 73366 (HUA, MO) [fr]; along road between Tena and Puyo, 61.5 km N of Puyo, 1°11'36"S, 77°52'34"W, 500 m elev., 22 Dec 1979 [fl], T. Croat 49657 (MO); Archidona, Parque Nacional Galeras a 1.5 km de la comunidad Santa Rosa de Arapino, 00°51'00"S, 77°31'00"W, 1230 m elev., 3 Apr 1996 [fr], H. Vargas & P. Grefa 951 (HUA, MO, QCNE); San José de Payamino 40 km W of Coca, 00°30'S, 77°20'W, 26 Apr 1984 [fl], D. Irvine & H. Jipa 959 (F, QCA); 1 May 1984, D. Irvine & L. Cejua 1125 (F, MO, QCA); Sucumbíos, Dureno, comunidad Cofan al sur del rio Aguarico, 20 km al este de Lago Agrio, 00°05'00"N, 76°40'00"W, 350 m elev., 27 Dec 1988 [fr], C. Cerón et al. 5824 (MO, HUA); Dureno, comunidad Cofan al sur del rio Aguarico, 20 km al este de Lago Agrio, 00°05'00"N, 76°40'00"W, 350 m elev., 27 Dec 1988 [fr], C. Cerón et al. 5827 (MO, HUA); Francisco de Orellana, Orellana, comunidad Shuar Tiguano al sur del Coca por la vía al Pindo, 00°44'58"S, 76°46'55"W, 300 m elev., 6–12 May 2004 [fl], W. Guerrero & A. Herrera 171 (MO, QCNE); Orellana, comunidad Shuar Tiguano al sur del Coca por la vía al Pindo, 00°44'58"S, 76°46'55"W, 300 m elev., 11 May 2004 [fr], A. Herrera & W. Guerrero 288 (MO, QCNE); Parque Nacional Yasuni, Rio Tiputini al noroeste de la confluencia con el Rio Tivacuno, este de la carretera Repsol-YPF, km 32 hacia NPF, Sendero Botánico Guiyero, 00°38'S, 76°30'W, 200—300 m elev., 26 Feb 2002 [fr], G. Villa 1350 (F, QCA, US); Peru. Amazonas, Condorcanqui, Santiago, Cerros Kampankis, Serranía entre los Rios Santiago y Morona, desde Río Marañón hasta frontera con Ecuador, Campamento 1: Pongo Shenin, 03°07'01.52"S, 77°46'55.14"W, 520 m elev., 3 Aug 2011 [fr], I. Huamantupa 15217 (USM, F).

Piper nokaidoyitau W. Trujillo-C & M. A. Jaram., sp. nov.

urn:lsid:ipni.org:names:77303985-1
Figs 1, 2, 7 and 8

Type

Colombia, Caqueta; Florencia, corregimiento el Caraño, vereda Sucre, 01°47'50.8"N, 75°38'50.5"W, 1020 m elev., 25 Oct 2020 [fr], F. Hoyos & W. Trujillo 046 (Holotype COL, Isotype COAH, UMNG, HUAZ, HUA)

Diagnosis

Piper nokaidoyitau W. Trujillo & M. A. Jaram., can be separated from the similar species P. hostmannianum (Miq.) C. DC. (1869:287), by its prophylls up to 2.4 cm long, leaves 12–20 cm long vs. prophylls 2.8–3.5 cm long, leaves 21–26 cm long in P. hostmannianum.

Figure 7. 

Piper nokaidoyitau A sympodial branch B details of the inflorescence C floral bract viewed from above D floral bract side view E flower side view F stamen with glabrous connective G fruit side view H floral diagram. Illustration by Marcela Morales based on F. Hoyos 046 (COL).

Description

Shrub up to 3 m tall; internodes (2.5–)3–4.5 cm long, canaliculate superficially, green, glabrous. Prophylls 2.8–3.2 cm long, green, glabrous, caducous, swollen in the basal portion (observable in live plants). Petioles uniform in size along all nodes, (0.7–)1–1.2(–1.5) cm long, sheathing at the base, smooth, glabrous. Leaf-blades coriaceous, drying black, uniform in shape and size along all axes, (4.5–)5–8 × (18) 21–26 cm, ovate, asymmetric, base rounded, glabrous on both surfaces, eciliate; pinnately nerved throughout, 4–5 ascending nerves on each side, eucamptodromous, with spacing decreasing and angle increasing towards the base, tertiary veins random, reticulate; apex acuminate. Inflorescences simple spikes, erect; peduncle 1–1.5 cm long, glabrous, green; rachis (7.5)10–12 × 0.3 cm in flower, 11–13 × 0.4–0.5 cm in fruit, flowers densely grouped along the rachis, forming bands around the spike. Floral bracts cucullate, heart-shaped from above, 0.2–0.35 × 0.4–0.7 mm, glabrous centrally on the abaxial surface, margin densely fimbriate. Flowers with three stamens, filaments 0.3–0.5 mm long, anthers 0.1–0.25 × 0.2–0.3 mm, transversally dehiscent, dithecous, with connective not protruding, glabrate, idioblasts not evident, colour black when dried; stigmas 3, 0.1–0.25 mm long, sessile. Fruits obpyriform in side view and triangular from above, green when alive, black when dry, 0.5–0.7 × 0.8–0.9 mm, glabrous, partially immersed in the rachis, with stigmas sessile and persistent.

Figure 8. 

Piper nokaidoyitau A sympodial branch, lower leaf surfaces B sympodial branch, upper leaf surfaces and spikes C single infructescence. Photos from F Hoyos & W Trujillo 046 by F Hoyos

Distribution and habitat

Piper nokaidoyitau is known from the lower montane forests in the eastern slopes of the Andes in Colombia, ca. 1,100 m elevation (Fig. 2), the Department of Caquetá. It is a shade-loving species that grows in the understorey of preserved forest.

Phenology

Flowering specimens were collected in September and October. Fruiting specimens in October.

Etymology

Piper nokaidoyitau is named after the Huitoto name for Piper plants, “Nokaido yitau”. It means “the powers of the toucan” because these are sacred and medicinal plants used against fever, body and headaches and as anti-inflammatories.

Phylogenetic relationships

Piper nokaidoyitau belongs to the Radula clade of Neotropical Piper (Jaramillo et al. 2008). Specifically, P. nokaidoyitau is sister to the Isophyllon subclade, within Radula. Isophyllon species are mostly self-standing shrubs with coriaceous leaves, pinnately nerved, acute or obtuse bases and flowers densely arranged in erect inflorescences. Isophyllon species occur in the Atlantic Forest, Central America and the Amazon Region.

Conservation status

This species is known from four specimen collections representing two subpopulations. The locations where it occurs are threatened by deforestation and expansion of the agriculture frontier. The area of occupancy (AOO) of 8 km2 is small, which, together with the continuing decline in habitat quality, suggests it is Endangered [EN B1a+B2a].

Comments

Leaves of Piper nokaidoyitau are pinnately nerved throughout with 4–5 ascending secondary veins on each side. This characteristic is shared by other species belonging to the Radula clade, specifically subclade Isophyllon (Jaramillo et al. 2008). We compared P. nokaidoyitau with similar species that occur on the eastern slope of the northern Andes (Table 4).

Table 4.
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Comparison of Piper nokaidoyitau with related species that have leaves pinnately nerved throughout and occur in the eastern slope of the northern Andes.

Species Prophylls length Leaf shape Leaf base shape Leaf length Infructescence length Geographic distribution
P. anonifolium Kunth 0.5–0.8 cm elliptic cuneate (10)14–17 cm 3–3.5 cm Amazonia
P. hostmannianum C. DC. 1–2 cm elliptic rounded 12–20 cm 10–11 cm Amazonia
P. nokaidoyitau W. Trujillo & M. A. Jaram. 3–3.5 cm ovate rounded 21–26 cm 11–13 cm Eastern slope of the northern Andes
P. mastersianum C. DC. 0.4–0.8 cm ovate rounded 9–12 cm 4–9 cm Amazonia

Specimens examined

Colombia. Caquetá, municipio de Florencia: corregimiento El Caraño, vereda El Caraño, finca Las Brisas, 01°44'14.7"N, 75°40'35.3"W, 1116 m elev., 18 Oct 2013 [fl], W. Trujillo et al. 3005 (COL); Corregimiento El Caraño, finca Las Brisas, 01°44'14.7"N, 75°40'35.3"W, 1116 m elev., 18 Oct 2013 [fl], W. Trujillo et al. 3022 (COL); Municipio de Belén de los Andaquíes: río Pescado, Parque Natural Andaqui, sector sur, 01°36'31"N, 75°55'16"W, 950 m elev., 25 Jun 2013, W. Trujillo et al. 2791 (HUAZ). Cauca. Municipio de Piamonte, corregimiento de Miraflor, vereda La Florida, camino a la reserva La Cristalina, 01°04'59.6"N, 76°28'08.2"W, 1146 m elev., 06 Jan 2021 [fr], E. Trujillo et al. 7249 (CUVC, JBB).

Piper velae W. Trujillo-C & M. A. Jaram., sp. nov.

urn:lsid:ipni.org:names:77303989-1
Figs 1, 2, 9 and 10

Type

Colombia, Caquetá, Belen de los Andaquies, corredor resguardo La Cerinda, PNN Alto Fragua Indiguazi, etnia Embera Katio, 1°36'08.6"N, 75°51'49.1"W, 470 m elev., 03 Oct 2007, W. Trujillo et al. 905 (Holotype COAH, Isotype HUAZ).

Diagnosis

Piper velae W. Trujillo & M. A. Jaram. can be distinguished from the related species P. holdridgeanum W.C. Burger by its elliptic leaves with cordulate leaf bases at all nodes, petioles 0.8–1.5 cm long, fruits cylindrical and pubescent vs. leaves cordate to elliptical with leaf bases that are rounded at fertile nodes and cordate at sterile nodes, petioles that are variable in size from 1–5 cm long, fruits rounded and glabrous in P. holdridgeanum. It can be separated from similar species P. cornifolium Kunth (1815 [1816]:52) because it has leaves pinnately nerved in the lower half of the blade and pubescent fruits vs. leaves pinnately nerved in the lower third of the blade and glabrous fruits in P. cornifolium.

Figure 9 

Piper velae A sympodial branch B magnified view of the infructescence C floral bract view from above D floral bract side view E fruit side view F stamen side view G Seed side view H floral diagram. Illustration by Marcela Morales based on W Trujillo 905

Description

Shrub up to 1.5 m tall. Internodes 2–8.5 cm long, smooth, green, tomentulose, idioblasts not evident. Prophylls 1.2–2 cm long whitish, tomentulose, caducous. Petioles variable along all axes; on monopodial axes 1–1.5 cm long, vaginate to 3/4 of the length, smooth, tomentulose; on sympodial axes 0.8–1.2 cm long, vaginate at the base, smooth, tomentulose. Leaf-blades coriaceous, drying black, uniform in shape and size along all axes, 6–7(11) × 12–15(19) cm, elliptic, symmetric, base cordulate, basal extension asymmetrical; leaf blade smooth, tomentulose on the abaxial surface and glabrous adaxially, eciliate; pinnately nerved from the lower half, 4–5 ascending nerves on each side, festooned brochidodromous, with spacing decreasing and angle increasing towards the base, tertiary veins percurrent; apex acuminate. Inflorescences and infructescence a solitary spike, terminal, erect; peduncle 0.8–1.5 cm long, tomentulose, green; rachis in flower not seen, rachis in fruit 6–8.5 cm long, fruits densely grouped along the rachis. Floral bracts cucullate, triangular from above, 0.15–0.25 × 0.3–0.4 mm, glabrous on the adaxial surface, margin fimbriate, not forming bands around the spike. Flowers with four stamens, filaments 0.2–0.4 mm long, anthers 0.2–0.3 × 0.15–0.25 mm, longitudinally dehiscent, dithecous, shorter than filament, with connective not protruding, glabrate, idioblasts not evident, colour not seen. Stigmas 3, on a short style. Fruits cylindrical, laterally compressed, green when alive and black to brown when dry, 0.8–1.2 × 1–1.3 mm, pubescent on the tip, partially immersed in the rachis, with stigmas persistent, 0.07–0.12 mm long, on a short style, 0.1–0.3 mm long. Seeds 0.4–0.6 × 0.9–1.1 mm, rectangular, laterally compressed, obtuse, black.

Figure 10 

Piper velae A sympodial branch upper leaf surfaces and spike B magnified view of the leaf base and prophyll C magnified view of the spike D magnified view of the prophyll. Photos from W. Trujillo 2039 by William Trujillo.

Distribution and habitat

Piper velae occurs in the eastern slopes of the Andes, from 250–1,500 m in elevation, spreading from wet lowland to wet premontane forests. It occurs in the Colombian Departments of Caquetá, Meta, Cauca and Putumayo. In lowland forests, it occurs in dense terra firme forests. In premontane forests, it grows mostly on moderate slopes, sometimes occurring on steep slopes and rocky substrates. It is a shade-loving species, growing in the understorey and it is also found in forest gaps.

Phenology

Flowering specimens were collected in February, April, May, June, July and October. Fruiting specimens in January, April, June, July, September, October and December.

Etymology

Piper velae is named in honour of Huber Fernando Vela, M.D., a social and environmental leader of Caquetá who was murdered in 2021. Dr Vela and sponsored Piper collections by WT during 2020. Huber Fernando was the leader of the Nature Reserve Romi Kumu, where 30 ha of forest were restored in 2020. The type specimen of P. velae occurs in the region that Dr Vela loved and helped conserve and restore.

Conservation status

This species is known from 41 specimen collections representing 12 subpopulations. It occurs in 18 locations threatened by deforestation. The extent of occurrence (EOO = 40,810 km2, below the EOO to be considered Vulnerable, VU) and area of occupancy (AOO = 96 km2), suggest it is of Near Threatened [NT B1a+B2a].

Phylogenetic relationships

P. velae is sister to P. holdridgeanum and these form a clade sister to Macrostachys (Jaramillo et al. 2008). P. velae and P. holdridgeanum have sheathing petioles to ¾ of their length and tightly-arranged flowers. The marked foliar dimorphism between leaves on sterile (monopodial) and fertile (sympodial) nodes distinctive of P. holdridgeanum have obscured its relationships (Callejas-Posada 2020). Here, we present phylogenetic evidence for its placement sister to Macrostachys. Both species, P. velae and P. holdridgeanum require further study to understand their morphological affinities.

Discussion

Piper velae can be confused with P. cornifolium, because of its cordulate leaf base; however, these taxa are distinguished, based on the leaf venation pattern and fruit pubescence (see Table 5). We also compare P. velae to closely-related P. holdridgeanum; further studies will help us corroborate this relationship and find morphological similarities.

Table 5.
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Comparison of Piper velae with closely-related species P. holdridgeanum and morphological similar species P. cornifolium.

Species Petiole length Leaf shape Leaf base Secondary nerves branched Fruit shape Fruit pubescence Geographic distribution
P. cornifolium Kunth 0.8–1.2 cm obovate-elliptic cordulate from the lower third rounded pubescent Northern Andes
P. holdridgeanum W.C. Burger 1–5 cm cordate to elliptic rounded to cordate from the lower half rounded glabrous Mesoamerica
P. velae W. Trujillo & M. A. Jaram. 0.8–1.5 cm elliptic cordulate from the lower half cylindrical pubescent Eastern slope of the northern Andes

Specimen examined

Colombia: Caquetá: Belén de los Andaquíes: Parque Bosque Microcuenca La Resaca, sendero Alto Sarabando, 800 m elev., 1°27'29"N, 75°53'1.8"W, 26 Oct 2010, D. Cárdenas et al. 40791 (COAH); vereda Las Verdes, río Pescado, margen izq. Parque Natural Municipal Andakí, 700 m elev., 1°36'7.2"N, 75°54'10"W, 28 Oct 2010, D. Cárdenas et al. 40896 (COAH); sector Paramillo, camino entre Acevedo - Belén de Andaquíes, 1400 m elev., 1°40'58"N, 75°54'21"W, 23 Jul 2011, D. Cárdenas et al. 41848 (COAH); cerca del río Pescado, vereda Los Angeles, 1225 m elev., 1°34'49.7"N, 75°54'17"W, 9 Jul 2011, L. Martinez 24 (COAH); río Pescado, Parque Natural Andakí, sector Sur, 950 m elev., 1°36'31"N, 75°55'16"W, 25 Jun 2013, W. Trujillo et al. 2792 (COAH). Cartagena del Chairá: vereda Laguna del Chairá, 240 m elev., 1°15'23.9"N, 74°48'49.8"W, 28 Sep 2007, W. Trujillo et al. 853 (COAH). Florencia: corregimiento El Caraño, vereda Alto Brasil, camino hacia la quebrada Yumal, 321 m elev., 1°39.543'N, 75°36.128'W, 22 Oct. 2012, A. Jimenez et al. 4 (HUAZ); río Hacha, vereda El Caraño, finca Marsella, 500 m elev., 1°41'47"N, 75°37'16"W, 26 Jun 2010, D. Cárdenas et al. 24884 (COAH, HUAZ); vereda El Paraíso, antigua vía Florencia-Neiva, zona de cordillera baja, 756 m elev., 1°45'7.4"N, 75°39'56.9"W, 20 Oct 2010, D. Cárdenas et al. 40568 (COAH); vereda El Paraíso Bajo, vegetación de cordillera baja, 800 m elev., 1°45'0.2"N, 75°37'8.2"W, 22 Oct 2010, D. Cárdenas et al. 40595 (COAH); Centro de investigaciones Macagual, 258 m elev., 1°29'59.8"N, 75°39'22.6"W, 13 Dec 2008, W. Trujillo et al. 1214 (COAH); vereda El Caraño, 1116 m elev., 1°44'14.7"N, 75°40'35.3"W, 18 Oct 2013, W. Trujillo et al. 3002 (COAH). La Montañita: vereda Los Morros, reserva Las Dalias, 300 m elev., 1°29'21.5"N, 75°24'17.6"W, A. Meneses 15 (HUAZ); vereda Itarca, Reserva Natural Itarca, 340 m elev., 1°32'53"N, 75°28'20"W, 30 Oct 2010, D. Cárdenas et al. 40956 (COAH); vereda Itarca, Reserva Natural Itarca, 330 m elev., 1°32'34.5"N, 75°28'19"W, 26 Apr 2011, N. Castaño et al. 3142 (COAH); Reserva Las Dalias, 382 m elev., 1°29'21.6"N, 75°24'17.6"W, 41050, W. Trujillo et al. 2086 (COAH). San Vicente del Caguán: inspección Guacamaya, vereda La Música, margen izquierda del río Caguán, 600 m elev., 2°20'46"N, 74°54'12.4"W, 12 Jul 2015, D. Cárdenas et al. 44401 (COAH). Cauca: Piamonte: La Libertad, 700 m elev., 1°6'41.78"N, 76°28'46.5"W, 22 Feb 2010, W. Trujillo et al. 1271 (COAH). Santa Rosa: Inspección de Santa Marta, vereda Diamante Alto, 1150 m elev., 1°14'N, 76°36'W, 22 Jun 2002, B. Ramírez 16061 (COAH). Meta: San Juan de Arama: sector del chorro Santo Domingo, Parque Nacional Natural Sierra de La Macarena, 520 m elev., 3°15'23"N, 73°57'50"W, 27 Oct 2019, D. Cárdenas et al. 52002 (COAH); vereda Monserrate Bajo, finca El Paraíso, cerca al caño Las Ninfas, 590 m elev., 3°20'33.75"N, 73°57'3.06"W, 4 Apr 2004, L. Carvajal et al. 173 (COAH). Putumayo: Mocoa: vereda Medio Afán, camino Serranía El Churumbelo, sector Nororiental, 900 m elev., 1°10'39"N, 76°38'47"W, 4 Oct 2000, D. Cárdenas et al. 12221 (COAH); vereda San José del Pepino, 1°5'40.17"N, 76°37'49.05"W, 21 Jun 1997, R. López et al. 2514 (COAH); vereda San José del Pepino, 1°5'40.17"N, 76°37'49.05"W, 21 Jun 1997, R. López et al. 2610 (COAH). Orito: Santuario de Flora y Plantas Medicinales Ingui-Ande, vereda Líbano, sector de don Reinaldo, 900 m elev., 0°41.62'N, 77°3.789'W, 1 Oct 2015, D. Cárdenas et al. 45416 (COAH); Santuario de Flora y Plantas Medicinales Ingui-Ande, 1004 m elev., 0°41.627'N, 77°3.801'W, 27 Sep 2015, D. Cárdenas et al. 45454 (COAH); vereda El Líbano, 832 m elev., 0°38'15"N, 77°4'17.9"W, D. Cárdenas et al. 51291 (COAH).

Acknowledgements

We thank Marcela Morales for botanical illustrations and Viviana Vargas for preparing Figures 3, 6, 8 and 10. ET and WT thank Vicerrectoría de Investigaciones and Facultad de Ciencias Básicas of the Universidad de la Amazonia for support in conducting floristic research in Caquetá. We thank Norida Marín from Herbario Amazónico Colombiano (COAH) and Hector García from Herbario Universidad de Magdalena (UTMC) for providing photographs of herbarium specimens.

References

  • Brako L, Zarucchi JL (1993) Catalogue of the flowering plants and gymnosperms of Peru. Monogr. Syst. Bot. Missouri Bot. Gard. 45: 1–1286.
  • Cáceres A, Kato MJ (2014) Importance of a multidisciplinary evaluation of Piper genus for development of new natural products in Latin America. International Journal of Phytocosmetics and Natural Ingredients 1(1): 1–7. https://doi.org/10.15171/ijpni.2014.04
  • Callejas-Posada R (2020) Piperaceae. In: Davidse G, Ulloa C, Hernández-Macías HM, Knapp S (Eds) Flora Mesoamericana. Missouri Botanical Garden Press, Saint Louis.
  • Colvard MD, Cordell GA, Villalobos R, Sancho G, Soejarto DD, Pestle W, Lobo Echeverri T, Perkowitz KM, Michel J (2006) Survey of medical ethnobotanicals for dental and oral medicine conditions and pathologies. Journal of Ethnopharmacology 107(1): 134–142. https://doi.org/10.1016/j.jep.2006.04.005
  • Dauby G, Stévart T, Droissart V, Cosiaux A, Deblauwe V, Simo-Droissart M, Sosef M, Couvreur TL (2017) ConR: An R package to assist large-scale multispecies preliminary conservation assessments using distribution data. Ecology and evolution 7: 1–12. https://doi.org/10.1002/ece3.3704
  • De Candolle C (1866) Piperaceae novae. Journal of Botany. British and Foreign 4: 210–219.
  • De Candolle C (1869) Piperaceae. Prodromus Systematis Naturalis Regni Vegetabilis 16(1): 235–471. [Paris.]
  • De Candolle C (1891) Primitiae Florae Costarricensis. Premier Fascicule, Piperaceae. Bulletin de la Société Royale de Botanique de Belgique 30: 196–235.
  • De Candolle C (1898) Piperaceae novae. Annuaire du Conservatoire et du Jardin Botaniques de Genève 2: 252–287.
  • De Candolle C (1920a) Piperaceae Colombianae et Peruvianae Novae. Annuaire du Conservatoire et du Jardin Botaniques de Genève 21.
  • De Candolle C (1920b) New species of Piper from Panama. Smithsonian Miscelaneous collections 71: 1–17.
  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15.
  • Ellis B, Daly D, Hickey LJ KR J, Mitchell J, Wilf P, Wing S (2009) Manual of leaf architecture. Cornell, New York.
  • Jaramillo MA, Callejas R (2004) A reappraisal of Trianaeopiper Trelease: Convergence of dwarf habit in some Piper species of the Chocó. Taxon 53(2): 269–278. https://doi.org/10.2307/4135607
  • Jaramillo MA, Manos PS (2001) Phylogeny and the patterns of floral diversity in the genus Piper (Piperaceae). American Journal of Botany 88(4): 706–716. https://doi.org/10.2307/2657072
  • Jaramillo MA, Callejas-Posada R, Davidson C, Smith JF, Stevens AC, Tepe EJ, Editor C, Plunkett GM (2008) A Phylogeny of the Tropical Genus Piper Using ITS and the Chloroplast Intron psbJ – petA. Systematic Botany 33(4): 647–660. https://doi.org/10.1600/036364408786500244
  • Jørgensen PM, León-Yánez S (1999) Catalogue of the Vascular Plants of Ecuador. Monograph in Systematic Botany from the Missouri Botanical Garden 75: 1–1181.
  • Jørgensen PM, Nee MH, Beck SG (2014) Catálogo de las plantas vasculares de Bolivia. Jørgensen PM, Nee MH, Beck SG (Eds) Missouri Botanical Garden Press, St. Louis, 1–1744.
  • Kunth CS (1815) [1816] Piperaceae. Nova genera et species plantarum (quarto edn.) 1: 46–74, t. 3–17.
  • Molina-Henao YF, Guerrero-Chacón AL, Jaramillo MA (2016) Ecological and Geographic dimensions of diversification in Piper subgenus Ottonia: A lineage of Neotropical rainforest shrubs. Systematic Botany 41(2): 253–262. https://doi.org/10.1600/036364416X691777
  • Ramírez-Amezcua JM (2016) Piper commutatum (Piperaceae), the correct name for a widespread species in Mexico and Mesoamerica. Acta Botánica Mexicana 116(116): 9–19. https://doi.org/10.21829/abm116.2016.1116
  • Salehi B, Zakaria ZA, Gyawali R, Ibrahim SA, Rajkovic J, Shinwari ZK, Khan T, Sharifi-Rad J, Ozleyen A, Turkdonmez E, Valussi M, Tumer TB, Fidalgo LM, Martorell M, Setzer WN (2019) Piper species: A comprehensive review on their phytochemistry, biological activities and applications. Molecules (Basel, Switzerland) 24(7): e1364. [118 pp.] https://doi.org/10.3390/molecules24071364
  • Tepe EJ, Watson LE, Vincent MA (2004) Phylogenetic patterns, evolutionary trends, and the origin of ant-plant associations in Piper section Macrostachys: Burger’s hypotheses revisited. In: Dyer LA, Palmer AN (Eds) Piper: A model genus for studies of chemistry, ecology, and evolution. Kluwer Academic, Boston MA, 156–178. https://doi.org/10.1007/978-0-387-30599-8_9
  • Thiers B (2019) Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/science/ih/ [accessed 4.12.2020]
  • Trelease W (1936) Piperaceae. In: Macbride JF (Ed.) Flora of Peru. Publications of Field Museum of Natural History, Botanical Serie, Chicago, 3–253.
  • Trelease W, Yuncker TG (1950) The Piperaceae of Northern South America. University of Illinois Press, Indiana.
  • Trujillo W, Jaramillo MA (2019) An emended description of Piper cochleatum and a new species of Piper (Piperaceae) from the Amazonian slopes of the Colombian Andes. Phytotaxa 408(1): 59–68. https://doi.org/10.11646/phytotaxa.408.1.4
  • Ulloa-Ulloa C, Acevedo-Rodríguez P, Beck S, Belgrano MJ, Bernal R, Berry PE, Brako L, Celis M, Davidse G, Forzza RC, Gradstein SR, Hokche O, León B, León-Yánez S, Magill RE, Neill DA, Nee M, Raven PH, Stimmel H, Strong MT JL, Villaseñor J, Zarucchi L, Zuloaga FO, Jørgensen PM (2018) Vascular Plants of the Americas (VPA). http://legacy.tropicos.org/Project/VPA [accessed 25.9.2021]
  • Valentin-Silva A, Batalha MA, Guimarães E (2018) Dynamics of pollen release and stigmatic exposure in neotropical Piper species: A possible pattern for the genus. International Journal of Plant Sciences 179(4): 287–295. https://doi.org/10.1086/696824
  • Yuncker TG (1966) New species of Piperaceae from Brazil. Boletim do Instituto de Botanica 3: 1–370.
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