Synopsis of the genus Peperomia Ruiz & Pav . ( Piperaceae ) in Roraima State , Brazil

(Synopsis of the genus Peperomia Ruiz & Pav. (Piperaceae) in Roraima State, Brazil). Peperomia is the second most diverse genus of Piperaceae, with an estimated 1,600 species and a pantropical distribution. This work aims to present a taxonomic synopsis of the genus in the State of Roraima, in the extreme north of the Brazilian Amazon forest and belonging to the central-south portion of the Guayana Shield. Based on collecting expeditions and analysis of specimens in various herbaria, 23 taxa were recognized, with two new records for the State and one of them, a new record for Brazil. The taxa are differentiated mainly by phyllotaxis, shape and size of their leaves, in addition to habit and fruits. They have been found in areas of lowland, submontane, montane, tepui and floodplain (várzea) forests and mostly show a distribution restricted to the Neotropics. Some species in the state are presently known exclusively from Mount Roraima, and restricted to a few specimens.


Introduction
The Piperaceae family has the largest number of species of the order Piperales.The order comprises four other families, among which Saururaceae is considered the sister group to Piperaceae (APG III 2009).The family includes about 3,600 species in five genera, with a pantropical distribution and its greatest diversity in the Neotropics (Arias et al. 2006, Quijano-Abril et al. 2006, Wanke et al. 2006, Samain et al. 2008).It is divided into three subfamilies, of which Piperoideae Arn., including Peperomia Ruiz & Pav. and Piper L., comprises the core of Piperaceae (Wanke et al. 2006, Samain et al. 2008).
For Brazil, Miquel (1852) recognized 57 species of Peperomia, and later Yuncker (1974) found 163 species for the genus in the country, organized in five subgenera and distinguished mainly by the morphology of the fruit.In both works (Miquel 1852, Yuncker 1974), some of the names listed with an Amazonian distribution are currently synonymized.According to Guimarães et al. (2015), there are 55 species of Peperomia in the Brazilian Amazon, 31 of them are considered endemic, with some restricted to one state.Studies of this area in Brazil have been done only by Costa & Callejas-Posada (1999) and Callejas-Posada (2008a).For the extra-Brazilian Amazon, there are some checklists (Callejas-Posada 1999, Callejas-Posada et al. 2007, Callejas-Posada 2008b), and taxonomic treatments that include Peperomia (Martínez 1997, Görts-van Rijn 2002, Steyermark & Callejas-Posada 2003, Nee 2004, Görts-van Rijn 2007).
The Amazon rainforest is the largest rain forest in the world, covering more than 6 million km² and nine South American countries, where an estimated 40,000 plant species occur, 75% of which are endemic (Mittermier 2003, Silva et al. 2005).In Brazil, the Brazilian Amazon (also known as Amazônia Legal) comprises areas of nine states with a wide range of vegetation types from dense Ombrophylous Forests to Savannas (Veloso et al. 1991, IBGE 2005).Among the vegetation types found, there are tepui, which are areas above 1,000-1,200 m and located in the Guayana Shield (Huber 1988).In Brazil, prominent tepui include the Serra do Aracá and Pico da Neblina, in Amazonas State, Mount Roraima, Serra do Tepequém and Serra dos Surucucus, located in Roraima (Huber 1988).
The objective of this work is to present a taxonomic synopsis of the species of Peperomia found in an area of the extreme north of the Brazilian Amazon, for which collection effort and knowledge of its plant diversity have been lacking.The geographic distribution, habitat, identification key and illustrations of species are also included.

Materials and methods
The area selected for the study comprises the State of Roraima, in the extreme north of the Brazilian Amazon and belonging to the south-central portion of the Guayana Shield (1°18'48"S-5°30'51"N, 58°41'49"W-64°34'33"W), with a total area of 224,301.04 km 2 .It has a border with Venezuela and Guyana to the north and, to the south with the States of Amazonas and Pará (Reis et al. 2003).
The field trips were made from September 2011 to May 2013 in five areas: Estação Ecológica de Maracá, Parque Nacional do Viruá, Mount Roraima, Serra Grande and Serra do Tepequém (figure 1) including various vegetation types (figure 2).The specimens were handled with the usual botanical techniques (Mori et al. 1989), deposited at Herbarium INPA, with duplicates sent to the herbaria UFP and RB (acronyms according to Thiers 2014).The review of existing herbarium collections was done using the collections of the herbaria EAFM, HB, HUAM (Herbário da Universidade Federal do Amazonas), IAN, INPA, MG, MIRR, NY, R, RB and UFRR in addition to the online query of some holdings, specifically B, K and US.
For the species examined, one voucher is cited per municipality or for its entire distribution when scarce.For additional material when necessary, one voucher per state was included.Specimens indicated as coming from Mount Roraima were analyzed and included in this work due to the imprecision of locality (triple border among Brazil, Guyana and Venezuela), and also because it is considered very likely that the taxa occur also on the Brazilian side of the border.

Results
A total of 23 taxa of Peperomia were recognized from the study area, with two new records for the State of Roraima and one of them is a new record for Brazil compared to Yuncker (1974) and Guimarães et al. (2015): P. lancifolia Hook.and P. macrostachya (Vahl) A. Dietr.Most of the taxa found occur in the Neotropics, some of them restricted to areas of higher elevation.There are records of taxa in  3a Terrestrial herbs up to 40 cm tall, stems erect.This species can be differentiated from other species by the leaves with an acuminate apex, in addition to the long spikes (12-30 cm long.).It can be confused with P. alpina, however P. acuminata has membranaceous leaves when dried, the flowers are congested, the rachis is greenish when fresh and the fruits are not prolonged at the apex.
Distributed in Central America, West Indies, Colombia, Venezuela, Brazil, Peru, Ecuador and Bolivia (Steyermark & Callejas-Posada 2003).In Brazil, the species occurs in mountainous areas of the Atlantic and Amazon Forests, where it can be found in the States of Acre, Amazonas and Roraima (Yuncker 1974, Guimarães et al. 2015).In Roraima, it is known only from the region of Mount Roraima, from about 2,100 m up to 2,700 m.
3. Peperomia alpina (Sw.) A. Dietr., Sp. pl. 1: 157.1831.Figures 3e-f Terrestrial herbs up to 40 cm tall, stems erect.This species can be distinguished from others by its size, leaves (6.4-7.5 × 3-4.1 cm) coriaceous when dry, glabrous, long-petiolate (1.5-2.3 cm); spikes paired or grouped in threes, and fruits globoid with a long slender apical beak that may be hooked at the tip.This species can be compared to P. acuminata, but can be differentiated by the lax flowers on the spike, the reddish to orangish rachis when fresh, in addition to the shape of the fruit.
Endemic to Brazil (Yuncker 1974, Guimarães et al. 2015).It occurs in the Atlantic and Amazon Forests, in the states of Roraima, Ceará, Bahia and Minas Gerais (Guimarães et al. 2015).It was found in Montane Forest areas up to 700 m.

Peperomia elongata
It occurs in Colombia, Venezuela, Guyana, Suriname, French Guiana and Brazil (Steyermark & Callejas-Posada 2003).In Brazil, it occurs in Cerrado, Atlantic and Amazon Forests, from Roraima to Mato Grosso (Guimarães et al. 2015).Trelease & Yuncker (1950) and Steyermark & Callejas-Posada (2003) consider there to be three varieties of this species, distinguishable by the size of their leaves and hairiness.However, a strong overlap of characters was detected in the samples of the study area, thus it was not possible to use the proposed taxonomic varieties.The species was found in lowland and alluvial (várzea) forests.3i Lithophytic or terrestrial herbs up to 50 cm tall, stems erect.This species can be differentiated from other species by having verticillate, sessile, oblong leaves (5-11 × 3-5 mm), which are cuneate to rounded at the base, rounded to obtuse apex and globoid fruit.
Distributed from Mexico to South America (Steyermark & Callejas-Posada 2003).In Brazil, it occurs in the Cerrado, Caatinga and Atlantic and Amazon Forests, generally in montane areas of over 1,000 m (Yuncker 1974, Guimarães et al. 2015).In the Brazilian Amazon, the species is registered only from Mount Roraima (Yuncker 1974) 1831.Figure 3j Epiphytic herbs up to 30 cm tall, stems erect.This species is easy to distinguish from other species by the black dots present throughout the plant, in addition to the elliptical to lanceolate leaves (1.5-7.4 × 1-3 cm), with palmate venation, axillary or terminal, arched spikes in number of the 2-3 or rarely solitary, and globoid fruits.It can be confused with P. alata, however the presence of black dots is distinct.
It occurs from Central America, West Indies and South America (Steyermark & Callejas-Posada 2003).In Brazil, it occurs in the Atlantic and Amazon Forests, in the latter biome in the States of Roraima, Amapá, Amazonas, Pará and Acre (Guimarães et al. 2015).It is reported here for Rondônia.According to Steyermark and Callejas-Posada (2003), two varieties can be recognized based on the shape and size of the leaves, however this was not possible for the samples studied due to overlap of the proposed characters.The species is found in mountain and alluvial (várzea) forests.
1841.Figures 4a-b Terrestrial herbs up to 1 m tall, stems erect.It is distinct from other taxa based on its size, habit, stems with quite prominent nodes, leaves (12-16 × 1.5-2.5 cm) with an attenuate base, attenuate to acuminate apex, paired spikes and elliptical fruits (1-1.5 mm long.).It is similar to P. acuminata, however P. lancifolia has leaves with an attenuate base, while P. acuminata has leaves with a rounded, obtuse to cuneate base and always solitary spikes.
It occurs in Mexico, Central America, Colombia, Venezuela, Guyana, Peru, Ecuador and Brazil (Steyermark & Callejas-Posada 2003).Despite the previous authors citing the species for Brazil, Yuncker (1974) and Guimarães et al. (2015) did not mention it for the country.Its occurrence in Brazil is confirmed here.Despite the inaccuracy of locality indicated on collected specimens, it is believed to occur in Montane Forests, as has been cited for other countries (Trelease & Yunker 1950, Steyermark & Callejas-Posada 2003).
1:149.1831.Figures 4c-d Epiphytic herbs up to 50 cm tall, stems decumbent.This species can be differentiated from other species by its elliptical to ovate leaves (3.8-7.1 × 1.8-4.3 cm), with an attenuate to acute apex, sometimes with white patches on the adaxial surface, pinnate venation, eciliate petioles and cylindrical fruits (2-3.5 mm long.).While very similar to P. elongata, P. macrostachya has larger fruits and glabrous petioles.
Distributed from Mexico to Ecuador and Brazil, where it occurs in the Atlantic Forest and widely in the Amazon Forest (Steyermark & Callejas-Posada 2003, Guimarães et al. 2015).The species is registered here for Roraima, where it was found in areas of lowland and Montane Forests.
Material examined: BRASIL.rorAimA: Amajari, Serra do Tepequém, 1-IX-2012 (fr.), A. Melo  12. Peperomia obtusifolia (L.) A. Dietr., Sp. pl.1: 154.1831.Figures 4e-f Epiphytic herbs up to 15 cm tall, stems prostrate.This species can be differentiated from other species by its obovate to rarely elliptical leaves (7.5-11.5 × 4.1-4.8cm), coriaceous when dried, with an obtuse, rounded or rarely emarginate apex, solitary, erect and axillary spikes and elliptical, papillose fruits with an extension at the apex which can form a hook.It can be confused with P. magnoliifolia (Jacq.) A. Dietr., which is not found in the study area, but has hirtose peduncles and petioles and larger and fruits (0.8-1 mm long.).Comparing it to the other species of the area, P. obtusifolia has leaves similar to P. alpina, but can be distinguished by its habit and the shape of the fruits.
Distributed from Mexico to South America (Steyermark & Callejas-Posada 2003), and in Brazil is present in the Caatinga, Cerrado and Amazon and Atlantic Forests (Guimarães et al. 2015).In the Brazilian Amazon, it occurs in the States of Amapá, Pará and Roraima (Yuncker 1974, Guimarães et al. 2015), where it was found only in areas of Montane Forest.Although no records of the species exist for the State of Amazonas, it possibly occurs in montane areas of that State.1923.Figures 4g-h Epiphytic herbs up to 6 cm tall, stems erect and pilose.It is characterized by its small size, elliptical to orbicular leaves (0.7-1.6 cm long) and globose and sessile drupes.It is similar to P. tenuipes, from which it differs by the hairiness of the leaves and stems and the shape of the fruits.It is comparable to P. rotundifolia, however these species differ in the shape of their leaves and the hairiness of the stems.It occurs in Nicaragua, Costa Rica, Colombia, Venezuela, Guyana, Suriname, French Guiana and Brazil, it has been recorded in the Atlantic and Amazon Forests (Görts-van Rijn 2007).It is found in Montane and Tepui Forests (760-2,000 m).P. pilicaulis C.DC. and P. ouabianae are not synonymy according Görtsvan Rijn (2007).These species are similar but differ in indument, leaf shape and size of fruit (Görts-van Rijn 2007).14.Peperomia pellucida (L.) Kunth, Nov. gen. sp. 1: 64. 1815[1816].

Figures 4g
Terrestrial herbs up to 50 cm tall, stems erect.This species can be differentiated from the other species by its habit, by being glabrous, with cordate to rarely deltoid leaves (1-2.5 × 1.5-2 cm), with an acute apex, palmate venation and globoid fruits.From the shape of the leaves, it can be confused with P. serpens (Sw.)Loudon, but it can be distinguished as being terrestrial, usually short-petiolate (0.5-1.5 cm long.), as well as the shape of its fruits.The species can also be confused with P. trinervula C. DC., but it can be distinguished by the shape of its leaves and the coloration of the stem when fresh (greenish in P. pellucida and reddish in P. trinervula).

Figure 4h
Epiphytic herbs up to 20 cm tall, stems erect.This species can be differentiated from other species by its size, the obovate, orbicular, oval to elliptical leaves [1.5-1.9 (2.6) × 0.7-1.4(1.9) cm] that are coriaceous when dried, with an obtuse to rounded apex, and solitary, erect and terminal spikes (1.6-3.8 cm long.).Its leaves are similar to those of P. quadragularis, however this species can be distinguished by its habit and size, in addition to its phyllotaxis.
It occurs in the West Indies, Panama, Colombia, Venezuela, Guyana, Suriname, French Guiana and the Brazilian Amazon, in the States of Roraima, Amazonas and Pará (Steyermark & Callejas-Posada 2003, Guimarães et al. 2015).One of the most common species of Peperomia recorded in herbaria visited and found in lowland, montane and alluvial (várzea) forests.Hist., Bot.Ser.13(2): 83.1936.Figure 5b Epiphytic herbs up to 15 cm tall, erect and strigose stems.It is characterized by its rhomboid to rarely elliptical leaves (0.7-1.7 × 0.4-0.8cm), with an acute apex and sessile to short-petiolate (up to 0.15 mm long.).The species can be confused with P. tetraphylla, but can be differentiated by the shape of the leaves, larger and thinner (5-6 × 0.1 cm) spikes and glabrous rachis.It is also similar to Peperomia psilostachya C. DC. (which was not found in Roraima), but has a smaller (0.8-1 cm long) peduncle, while in P. psilostachya, this exceeds 3 cm long.
It occurs from Mexico to South America (Steyermark & Callejas-Posada 2003), and in Brazil is present in the Atlantic and Amazon Forests, in the States of Roraima, Amazonas, Pará and Acre (Melo et al. 2014, Guimarães et al. 2015).In the study area, it was found in lowland, montane and alluvial (várzea) forests.
It occurs in Central America, West Indies and South America to Peru and Brazil (Steyermark & Callejas-Posada 2003), where it is cited for the Atlantic and Amazon Forests, from Roraima to Mato Grosso (Guimarães et al. 2015).It is one of the most common species of Peperomia in Roraima and be found in areas of montane and alluvial (várzea) forests.
Selected material examined: BRASIL.rorAimA: [Alto Alegre], Serra dos Surucucus, 14-II-1971 (fl., fr.)  1831.Figures 5d-e Terrestrial herbs up to 8 cm tall.This species can be differentiated from other taxa mainly by being a delicate herb with small (6-12 × 3-6 mm) and sparcely pubescent leaves, as well as the pedunculate fruits.It is very similar to P. tenuipes but that species is bigger and glabrous.It can also be confused with P. ouabianae, from which it can be differentiated by the shape of its leaves and fruits.Burger (1971) reported morphological similarity between P. tenella and P. tenuipes, treating them as a single taxon, while Steyermark & Callejas-Posada (2003) considered them as: P. tenella var.tenella (Sw.) A. Dietr.and P. tenella var.tyleri (Trel.)Steyerm.Recently, Mathieu and Callejas-Posada (2006) treated them as separate species, differentiating them by height, branching and hairiness of the stems and leaves.
It occurs from Central America to Colombia, Venezuela and Brazil (Steyermark & Callejas-Posada 2003, Guimarães et al. 2015).Although Guimarães et al. (2015) cite the occurrence of the species in Brazil for the Amazon (Amazonas) and Atlantic Forest (Minas Gerais, Rio de Janeiro, São Paulo, Santa Catarina and Paraná), it is also found in areas of the Amazonian tepui of the States of Amazonas and Roraima (De Candolle 1917, Prance & Johnson 1992).In Roraima, the species has only been recorded from Mount Roraima, being abundantly found along the trail up to the top (between 1,900 and 2,300 m), in shaded sites, banks of waterfalls and rapids.Epiphytic herbs up to 10-15 cm tall, stems erect.It is characterized by its small (0.8-2 × 0.4-0.9cm), elliptical, rarely ovate to orbicular leaves with an obtuse apex, solitary and terminal spikes and cylindrical and long-pedunculate fruits.

Peperomia tetraphylla
Pantropical (Steyermark & Callejas-Posada 2003).In Brazil, it is represented in the Caatinga, Cerrado, Atlantic and Amazon Forests, in the latter it is known only from Mount Roraima (Trelease & Yuncker 1950, Yuncker 1974, Steyermark & Callejas-Posada 2003).According to Guimarães & Giordano (2004) and Monteiro & Guimarães (2008), the species occurs in montane areas of Ceará (Serra do Baturité) and high-montane forests of Rio de Janeiro (Parque Nacional do Itatiaia), respectively.The habitat of the study area is consistent with indications of Trelease & Yuncker (1950) and Steyermark & Callejas-Posada (2003), for Colombia and Venezuela, where the species can be found in areas of tepui and mountain ranges.16(1): 420.1869.Figure 5h Epiphytic herbs up to 50 cm tall, stems erect and pilose.It is characterized mainly by its orbicular to ovate or rarely elliptical leaves [(0.9) 1.2-2.4× (0.6) 1.2-2.8cm] and axillary spikes, grouped in twos to threes (rarely solitary).From the shape of its leaves and campilodromous venation, it can be confused with P. pellucida, but P. trinervula has spikes grouped in twos or threes, rarely solitary, and its stems when fresh are usually reddish in color.
It occurs in Honduras, Venezuela, Colombia, Ecuador and Brazil, where it is known exclusively from Mount Roraima (Yuncker 1974, Callejas-Posada 1999, Steyermark & Callejas-Posada 2003).It is found from 2,000 to 2,700 m, which is similar to the citations for other countries, where it occurs in the areas of mountains, tepui and mountain ranges.
, where it was found from approximately 2,100 m to 2,400 m, in lightly shaded forest areas or open areas more exposed to sunlight.