Here we describe a new species of Passiflora subg. Passiflora (Passifloraceae sensu stricto) found in the Brazilian Atlantic rainforest in areas of campos rupestres of the João Pinto formation in Minas Gerais and on granitic inselbergs of Espírito Santo. The new species, named Passiflora ita, is described, illustrated, compared to similar species and its conservation status is preliminarily assessed as Endangered (EN) following IUCN Red List categories and criteria, reinforcing the importance of the areas where it occurs (which are not national or state-level parks) as priorities for conservation.
Citation: Mezzonato-Pires A. C., Ribeiro R. da S. & Gonella P. M. 2021: Maracujá on the rocks: a new Passiflora species (Passifloraceae sensu stricto) from the rupicolous ecosystems of the Brazilian Atlantic rainforest. – Willdenowia 51: 371–381. https://doi.org/10.3372/wi.51.51305
Version of record first published online on 14 December 2021 ahead of inclusion in December 2021 issue.
The Atlantic rainforest is a complex mosaic of vegetation types that extends along the entire E coast of Brazil, also occurring in smaller areas of Argentina and Paraguay (Joly 1999; IBGE 2019), and is recognized as a biodiversity hotspot due to its high endemism rate combined with severe habitat destruction level (Myers & al. 2000). Despite being well known for its exuberant ombrophilous and seasonal forests, this phytogeographical domain contains several other vegetation types as a result of the climatic, edaphic and altitudinal diversity of the Brazilian coast. Among these vegetation types, the rupicolous ecosystems stand out in areas where rocks of different geologies outcrop and are inhabited by communities of species adapted to the conditions of water stress, such as intense sunlight and winds, shallow soils and high thermal amplitude (Porembski & al. 1998; Martinelli 2007). These ecosystems can be divided into campos rupestres (over quartzite and iron ore; Vasconcelos 2011; Silveira & al. 2016), campos de altitude (the “Brazilian Paramos”; mainly on granite and above 1500 m; Safford 1999, Vasconcelos 2011) and lowland inselbergs (“sugar-loaves”, on granite/gneiss at lower elevations; Porembski & al. 1998; Paula & al. 2020).
Passiflora L. (Passifloraceae sensu stricto, popularly maracujás in Portuguese or passionflower/passionfruit in English) is a genus of mainly climbing plants or lianas with over 560 species (Krosnick & al. 2013), of which 157 occur in Brazil (Bernacci & al. 2020). Although the Atlantic rainforest is the main centre of species diversity in the country (84 species), the majority of these species are found in ombrophilous forests (55 species), while only 10 species are reported from the aforementioned rupicolous ecosystems.
Passiflora is considered the largest genus of climbing flowering plants of the neotropical region (Acevedo-Rodríguez & al. 2015+) and can be easily recognized by the presence of tendrils, petiole usually with the presence of extrafloral nectaries, flower with androgynophore, a well-developed corona and a tricarpellate and unilocular ovary. The genus has a complex history of infrageneric classification, starting in the 19th century with Candolle (1822), who subdivided the genus into seven sections. Since then, some modifications were published, with emphasis on the important work of Killip (1938), who subdivided Passiflora into 22 subgenera. By the end of the 20th century, Escobar (1989) modified part of Killip's (1938) classification and described a new subgenus, P. subg. Porphyropathanthus L. Escobar. This classification remained until the proposal of Feuillet & MacDougal (2003), who drastically reduced the number of subgenera to four, namely: P. subg. Astrophea (DC) Mast., P. subg. Deidamioides (Harms) Killip, P. subg. Decaloba (DC.) Rchb. and P. subg. Passiflora. Currently, two other subgenera are also recognized: P. subg. Tetrapathea (DC.) P. S. Green (Krosnick & al. 2009) and P. subg. Tryphostemmatoides (Harms) Killip (Restrepo & al. 2019). Only the four subgenera recognized by Feuillet & MacDougal (2003) are found in Brazil.
Passiflora subg. Passiflora is the largest among the subgenera, characterized by: species with herbaceous habit; bracts large and usually whorled; flowers generally large (>3 cm in diameter) and coloured (petals, sepals and filaments of the corona); corona with filaments varying in the number of series, usually three series or more, except for some species which can have one or two series; corona filaments frequently with different sizes and banded with distinct colours; nectar ring and limen can be present; and fruit frequently >3 cm long (Cervi 1997). Currently, the subgenus is divided into six supersections, 20 sections and 11 series (Feuillet & Macdougal 2003). The largest supersection is P. supersect. Stipulata MacDougal & J. M. Feuillet described as having foliaceous stipules with clearly asymmetric base and bracts also foliaceous. The richest section is P. sect. Granadillastrum (Triana & Planch.) Feuillet & J. M. MacDougal, with 66 species (Ulmer & MacDougal 2004), comprising species with conspicuous stipules, mainly subreniform or oblong-ovate, bracts free, leaves usually trilobed or entire and flowers with a conspicuous corona (Ulmer & MacDougal 2004).
During fieldwork for the floristic inventory of the campos rupestres areas of E Minas Gerais, a species of Passiflora was found that did not fit any named species. Further herbarium investigations uncovered other collections of such species from granitic inselbergs from Espírito Santo state. In this work, we describe and illustrate this new species, map its distribution, discuss the morphological relationships with the putative closest species and preliminarily assess its conservation status following the IUCN (International Union for Conservation of Nature) Red List categories and criteria (IUCN 2012).
Material and methods
The field expeditions were carried from June 2020 and are ongoing. The collected material was deposited in the herbaria CESJ and MBML (herbarium codes according to Thiers 2021+). Other herbaria were consulted via the online databases of Reflora (2021) and SpeciesLink (2021), as well as digitized specimens at the virtual herbaria of F, MEXU, MO, NY and US. One specimen with similarities with the new species was located at RB but was not seen in loco, therefore it is not included in the paratypes list. The terminology for floral and vegetative characters follows Cervi (1997) and Radford & al. (1974). Data for the preparation of Table 1 were extracted from Cervi (1997).
The distribution map was prepared with the Geographic Information System (GIS) software QGIS 3.4 (QGIS Development Team 2021). The layers of biomes, geopolitical areas, phytogeography and protected areas used in this study were extracted from Instituto Brasileiro de Geografia e Estatística (IBGE 2019, 2020), Banco de Dados Geomorfométricos do Brasil – TOPODATA ( http://www.dsr.inpe.br/topodata/), Instituto Estadual de Florestas – IEF ( http://www.ief.mg.gov.br/) and Fraga & al. (2019). For the conservation status assessment, a Darwin Core (DwC) dataset was assembled with the georeferenced occurrence deposited in collections. The methods of the IUCN Red List categories and criteria version 3.1 (IUCN 2012) were employed and the values of Extent of Occurrence (EOO) and Area of Occupancy (AOO) were calculated using the conservation assessment tool GEOCAT ( http://geocat.kew.org/) using the standard IUCN grid of 2 × 2 km (Bachman & al. 2011).
Holotype: Brazil, Minas Gerais, Conselheiro Pena, Serra do Padre Ângelo, Pico do Padre Ângelo, platô do topo do pico, 19°19′05.04″S, 41°34′42.26″W, 1480 m, 21 Aug 2020, P. M. Gonella & al. 1565 (CESJ; isotype: MBML).
Diagnosis — Passiflora ita differs from the other species of P. supersect. Granadillastrum by having stipules foliaceous, asymmetric ovate, apex mucronate; petiole with 2–4 sessile, elliptic to circular glands; lamina entire; bracts ovate, 10.3–21.5 × 7–9 mm; sepals oblong-lanceolate, cucullate, carinate, apex with arista 1.7–1.8 mm long; corona filaments in 3 well-defined series and 1 undefined series; third series of corona filaments erect-inclined toward androgynophore, filiform, united at base.
Description — Herbaceous vine with tendrils, entirely glabrous; stems reddish green at apex, turning brown to yellowish brown with age, cylindric, 0.8–2 mm in diam., striate. Stipules basifixed, foliaceous, caducous, yellowish green with reddish nerves, asymmetric ovate, 11.4–23.9 × 7.4–14.5 mm, glabrous, base asymmetric rounded, margin entire or slightly serrate glandular, apex acute, mucronate, mucro 0.3–0.6 mm long. Petiole reddish, 5.2–13.7 × 0.4–0.8 mm, glabrous; glands 2–4, paired or alternate, located in upper portion or also in lower portion of petiole, 2.1–5.6 mm from apex of petiole, sessile, vinaceous, elliptic to circular, 0.5–0.9 × 0.5–0.8 mm. Lamina peltate, green with reddish nerves and margin, entire, ovate to ovate-lanceolate, 22.4–86 × 17.5–50 mm, chartaceous, both surfaces glabrous, base cordate, rounded to truncate, margin entire, apex emarginate to obtuse. Inflorescence 1-flowered. Peduncle green to reddish, 17–32 mm long. Bracts whorled, green to pinkish, ovate to narrowly ovate, 10.3–21.5 × 7–9 mm, glabrous. Pedicel green to reddish, 4.4–6.4 mm long. Flowers 30.1–54.5 mm in diam.; hypanthium campanulate, 2.5–3.8 × 5.8–8.1 mm, glabrous; sepals abaxially green, brownish green, purple to pinkish, adaxially purple, oblong-lanceolate, cucullate, carinate, 14–25.3 × 6.9–7.9 mm, glabrous, apex acute to obtuse, with arista 1.7–1.8 mm long; petals purple on both surfaces, oblong-lanceolate, 18.6–21.9 × 8.1–8.6 mm, glabrous, apex obtuse; corona with 3 well-defined series of filaments and 1 undefined series of sparse filaments; first series of filaments radial, banded with bluish purple and white along entire length, filiform, 12.5–14 × 0.3–0.8 mm; second series of filaments radial, banded with bluish purple and white along entire length, filiform, 3.4–9.2 × 0.3–0.5 mm; third series of filaments erect-inclined toward androgynophore, dark purple, banded with white toward apex, filiform, 3.1–5.8 × 0.4–0.6 mm, bases united for 0.8–1.1 mm; undefined series located between second and third well-defined series, with scattered filaments not forming a proper series, dark purple, filiform, 1.9–2.4 × 0.1–0.2 mm; operculum adnate to united base of third series of filaments, 1.2–2.1 mm long, membranous, apical portion free for 0.2–0.7 mm, apex plicate; nectar ring present; limen cupuliform, 1.4–1.6 mm long; androgynophore green with vinaceous spots, 8.6–9.2 mm long; stamen filaments with vinaceous spots, 5–5.6 × 0.6–1 mm, glabrous; anthers 5.3–7 × 2.2–2.4 mm; ovary green, oblong, 2.9–4.5 × 1.6–2 mm, glabrous; style with purple spots, 5.7–6.1 × 0.2–0.5 mm. Fruit green, oblong to ellipsoid, 22–31 × 11–16 mm. Seed ovate or obovate to ellipsoid, 4.5–4.9 × 2.5–3 mm, testa reticulate-foveolate.
Phenology — Collected with flowers in January, February, March, May, June, August, September and November, and with fruits in February, March and June, therefore suggesting a continuous reproductive period year-round.
Distribution and habitat — Passiflora ita occurs in the Atlantic rainforest domain in the states of Minas Gerais and Espírito Santo, SE Brazil (Fig. 4). In Minas Gerais, the species was found in areas of quartzitic campos rupestres of the João Pinto formation, in the municipalities of Alvarenga and Conselheiro Pena in the E region of the state. These areas include the Serra do Padre Ângelo, where the species was recorded in the sectors of Pico do Padre Ângelo (Fig. 4C), Serra do Pinhão and the Serra da Palha Branca; it was also recorded in a quartzitic outcrop near the district of Vista Alegre (Alvarenga) and at the Pico da Aliança. In these areas, the species occurs in open areas under direct sunlight, among and on rock outcrops with herbaceous-shrubby vegetation at elevations of 920–1550 m. The species was also recorded from granitic inselbergs in the state of Espírito Santo, in the municipalities of Santa Leopoldina (Pedra Preta), São Roque do Canaã (Alto Misterioso; Fig. 4D) and Serra (APA Mestre Álvaro; Fig. 4E), where it also occurs as a rupicolous element exposed to direct sunlight, at elevations of 600–1078 m. A specimen collected in the municipality of Santa Teresa, Espírito Santo [Perdiz & al. 825 (RB 563073 – image!)], may be an additional occurrence of P. ita. The specimen lies within the reported range of P. ita and shares similarities in the shape of petiole glands, stipules and bracts. The specimen, however, lacks a mature flower, making it impossible to ascertain its identity. Future field observations at this location should provide a better understanding of this specimen.
Preliminary conservation status — Endangered: EN B1ab(iii)+2ab(iii). Passiflora ita has a naturally fragmented distribution (Fig. 4), occurring in isolated populations on hilltops that are subject to various threat situations. The species has an estimated EOO of 3362 km2 and an estimated AOO of 44 km2 (Fig. 4B). The Atlantic rainforest in the states of Minas Gerais and Espírito Santo has been severely altered, with most of its original area converted into pastures and other agricultural activities (Fig. 4C–E), resulting in small and isolated fragments of natural vegetation remaining. In the areas of campos rupestres where P. ita was found, it is threatened by the invasion of exotic grasses such as Melinis minutiflora P. Beauv. (“molasses-grass”) and species of Urochloa P. Beauv. (“brachiaria”), which were introduced in the surrounding pasturelands. The fern Pteridium aquilinum (L.) Kuhn (Dennstaedtiaceae) also poses a threat, invading the natural areas of the region (Gonella & al. 2015). The proximity of these areas of campos rupestres to pastures and human settlements makes them vulnerable to anthropogenic fires, given that the use of fire for pasture renovation and clearance of deforested areas is a common practice in the region. The populations of P. ita and other endangered species at Serra do Padre Ângelo were affected by such an anthropogenic fire in late 2020 (Andrino & Gonella 2021; Antar & al. 2021b; Kollmann & Gonella 2021), which can potentiate the invasion by the aforementioned alien species. In some of the areas, the presence of cattle was also observed directly on the campos rupestres. In the inselberg habitats, P. ita is similarly vulnerable to biological invasions, fire, grazing and mining (Porembski & al. 2016). In all studied areas, P. ita was observed forming small populations with low density and frequency of individuals. None of the known populations is found inside national and state-level parks, and the EOO polygon does not include any such type of protected area. Other areas of similar habitats can be found in the region and have the potential for the occurrence of the species, hence floristic inventories in protected areas such as the Sete Salões State Park (campos rupestres) and the Natural Monument of Pontões Capixabas (inselbergs) could result in the discovery of new populations. The species is currently recorded only for the Environmental Protection Area Mestre Álvaro (category of sustainable use). Given this scenario, we recommend that P. ita should be assessed as Endangered (EN) based on the aforementioned criteria of the IUCN (2012).
Etymology — The epithet chosen for the species is a noun in apposition, originating in the noun itá of the Tupi-Guarani language, meaning “rock” (Carvalho 1987). The epithet alludes to the rupicolous habit of the species, growing among and over rocks.
Additional specimens examined — Brazil: Espírito Santo: Santa Leopoldina, Luxemburgo, Pedra Preta, 15 Mar 2005, L. Kollmann & al. 7422 (MBML); São Roque do Canaã, Alto Misterioso, pedra 7, 19°48′07.6″S, 40°46′07.9″W, 1078 m, 27 Aug 2006, C. Esgario & al. 90 (MBML); Serra, Mestre Álvaro, 20°09′51″S, 40°18′24″W, 600 m, 1 Mar 2011, L. Kollmann & R. Cribari 12211 (MBML). — Minas Gerais: Alvarenga, Pico da Aliança, no topo do pico, 19°23′43.8″S, 41°40′08.8″W, 1440 m, 9 May 2021, P. M. Gonella & al. 2930 (MBML); Conselheiro Pena, Chapada do João Pinto, 19°20′17″S, 41°33′26″W, 18 Apr 2018, L. Kollmann & R. Cipriano 13508 (MBML); Conselheiro Pena, Serra do Padre Ângelo, Pico do Padre Ângelo, platô do topo do pico, 1500 m, Jun 2020, R. S. Ribeiro & al. 649 (MBML); ibid., 19°19′12.78″S, 41°34′42.02″W, 1515 m, 30 Nov 2020, P. M. Gonella & D. P. Cordeiro 1823 (MBML); ibid., próximo ao cruzeiro, 19°19′13.89″S, 41°34′44.18″W, 1550 m, 15 Mar 2021, P. M. Gonella & D. P. Cordeiro 2325 (MBML); ibid., primeiro platô da subida do pico, vale da mata nebular na vertente leste, 19°18′47.14″S, 41°34′36.53″W, 1265 m, 13 Sep 2020, P. M. Gonella & al. 1697 (CESJ, MBML); Serra da Palha Branca, afloramento ao lado do mirante da Bela Adormecida, 19°20′15.5″S, 41°33′26.4″W, 1060 m, 30 Jan 2021, P. M. Gonella & al. 1903 (MBML); Serra do Pinhão, área de afloramentos acima da Cachoeira do Diabo, na margem direita do córrego do Pinhão, 19°16′24.24″S, 41°34′41.49″W, 975 m, 31 Jan 2021, P. M. Gonella & al. 1985 (MBML); ibid., subida para o Pico do Sossego, 19°13′43.27″S, 41°34′22.57″W, 1070 m, 1 May 2021, P. M. Gonella & al. 2415 (MBML); ibid., base do Pico do Sossego, 19°14′16.9″S, 41°34′48.7″W, 1260 m, 2 May 2021, P. M. Gonella & al. 2527 (MBML); Afloramento quartzítico próximo a Vista Alegre (distrito de Alvarenga), 19°23′49.6″S, 41°33′26.4″W, 920 m, 1 Feb 2021, P. M. Gonella & al. 2061 (MBML); ibid., 18 Mar 2021, P. M. Gonella 2395 (MBML).
Based on the presence of conspicuous and ovate stipules, free bracts, entire leaves, and flowers with conspicuous corona, Passiflora ita is best placed in P. [subg. Passiflora supersect. Stipulata] sect. Granadillastrum. The new species shows morphological affinity with P. miersii Mast. of P. sect. Kermesinae (Cervi) Feuillet & J. M. MacDougal and P. castellanosii Sacco of P. sect. Granadillastrum (Table 1).
The similarity observed between the new species and Passiflora miersii has led to specimens of P. ita being considered under the misapplied name P. miersii by Borges & al. (2020) in the floristic treatment of the family for Espírito Santo. Other floristic studies dealing with the states where P. ita occurs did not mention specimens of the species (Vitta & Pirani 2015; Imig & al. 2018; Moraes & al. 2018).
Passiflora ita can be easily distinguished from P. castellanosii and P. miersii by vegetative characters. Although the three species are glabrous, P. ita possesses 2–4 glands on the petiole that are sessile, elliptic to circular and not stipitate as in the other two species. Furthermore, the bracts of P. ita (10.3–21.5 × 7–9 mm) are intermediate in size between P. castellanosii, with larger bracts (25–40 × 15–25 mm) and P. miersii, with smaller ones (6–8 × c. 2 mm). The number of filament series of the corona also varies between these species, P. ita having three well-defined series and one undefined series (vs three well-defined series in P. castellanosii and four well-defined series in P. miersii).
The filament series here referred to as “undefined” in Passiflora ita is a set of filiform filaments that do not form a series per se, because the scarce filaments are scattered between the second and third well-defined series (Fig. 1J). These characters are not found in the other two species.
Passiflora ita is the eleventh species of the genus found in the rupicolous ecosystems of the Atlantic rainforest. Before P. ita, the latest species described was P. rupestris Bernacci & al., from the campos rupestres of Serra Negra, part of Serra da Mantiqueira, in SE Minas Gerais (Bernacci & al. 2014).
Similar to that reported for species of Asteraceae by Antar & al. (2021b), Passiflora ita occurs both on areas of quartzitic campos rupestres and granitic inselbergs, therefore showing tolerance to distinct edaphic conditions. Passiflora ita adds to the growing list of species recently described from the campos rupestres and associated vegetation of the João Pinto formation (e.g. Gonella & al. 2015; Andrino & Gonella 2021; Antar & al. 2021a, 2021b; Kollmann & Gonella 2021), demonstrating the relevance of this area as a refuge of biodiversity and a priority for conservation. The same holds for the inselbergs where the species was found, which harbour unique biodiversity and have revealed many new, threatened species (e.g. Fraga & Feres 2007; Esgario & al. 2009; Monge & al. 2018).
ACMP wrote the first draft of the manuscript and led the investigation. ACMP and RSR prepared the figures and map. PMG and RSR performed field observations and collections. PMG performed the conservation status assessment. ACMP, RSR and PMG revised and edited the manuscript.
Distribution (according to Bernacci & al. 2020) and morphological traits in Passiflora ita and closely related taxa (according to Cervi 1997). Brazilian states: BA = Bahia; CE = Ceará; DF = Distrito Federal; ES = Espírito Santo; MG = Minas Gerais; MS = Mato Grosso do Sul; MT = Mato Grosso; PA = Pará; RJ = Rio de Janeiro; SE = Sergipe; SP = São Paulo. *size of horn not given in description of P. miersii.
The authors are grateful to Ednilson Caetano Ribeiro, Lucian Medeiros and Júlio César Ribeiro for company and guidance in the field work; Luiz França for logistic support in the field expeditions; Danilo Cordeiro, Gabriele Silva, Thais Condez, Eliana Ramos, Pedro Bartholomay and Alan Araújo for company in fieldwork; Caroline Andrino for suggestions to the improvement of the manuscript; Weverson Cardoso for sending photos of the species from the inselbergs of Espírito Santo; Cláudio Nicoletti de Fraga and Junior Nass for photographs used in this manuscript; Joelcio Freitas for the line drawing; Beethoven Belém for editing some images; and two anonymous reviewers for their comments on an earlier version of this paper. License for fieldwork was granted by the Authorization and Information System in Biodiversity (SISBIO), from the Chico Mendes Institute for Biodiversity Conservation (ICMBio). RSR thanks a fellowship grant by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Projeto:403440/2020-3; Processo: 301395/2021-7). This work was undertaken with the support of The Mohamed bin Zayed Species Conservation Fund, project no.192522325. PMG also thanks IDEA WILD for research equipment.