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Acta Botanica Brasilica

Print version ISSN 0102-3306On-line version ISSN 1677-941X

Acta Bot. Bras., ahead of print  Epub Nov 11, 2019

http://dx.doi.org/10.1590/0102-33062019abb0241 

Article

Increasing the known floristic diversity of Brazilian inselbergs: two new species of Mandevilla (Apocynaceae) from Espírito Santo

Juan Francisco Morales1  2  3  * 
http://orcid.org/0000-0002-8906-8567

Ludovic J.C. Kollmann4 
http://orcid.org/0000-0002-2283-6402

1 Missouri Botanical Garden, 63110, St. Louis, MO, USA

2 University of Bayreuth, 95447, Bayreuth, Germany

3 Universidad Estatal a Distancia, 474-2050, San José, Costa Rica

4 Instituto Nacional da Mata Atlântica, 29650-000, Santa Teresa, ES, Brazil


ABSTRACT

Two new species of Mandevilla endemic to inselbergs of the state of Espírito Santo, Brazil, are described. Mandevilla alata resembles M. callista but differs by having winged stems, shorter petioles, shorter pedicels, and a white corolla with a red throat. Mandevilla ibitubana resembles M. grazielae but differs by having short-petiolate leaves, a white corolla, and shorter anthers. Illustrations, a distribution map, conservation assessments and a key to species of Mandevilla growing on inselbergs in Espirito Santo are included.

Keywords: apocynoids; Ibituba; Mesechiteae; Santa Teresa; Pancas

Introduction

Inselbergs are Precambrian granitic and gneissic rock outcrops present on all continents, but more diverse in south eastern Brazil, Madagascar, and south western Australia (Burke 2003; Porembski 2007; Rabarimanarivo et al. 2019). They have a rich and endemic flora from ecological isolation and extreme microclimatic and geomorphological conditions (Safford 1999). In Brazil, most inselbergs are found in Espírito Santo, northern Rio de Janeiro, north eastern Minas Gerais, and southern Bahia (Ab’Saber 1967; Paula et al. 2016; Campos-Rocha et al. 2018). A few inselberg formations are also known from north eastern Brazil (Sales-Rodrigues et al. 2014; Maia et al. 2015).

The flora of Espírito Santo, Brazil, is poorly known. Major collecting efforts have been made recently, but many regions are still unexplored. Recent studies of inselbergs and forest from the area have led to the description of several narrowly endemic species (Kollmann 2008; Leme et al. 2008; 2010; Leme & Kollmann 2009; Versieux & Wanderley 2010; Silva et al. 2014; Goldenberg & Kollmann 2015; Meyer et al. 2016; Campos-Rocha et al. 2018; Meyer et al. 2018; Chautems et al. 2019).

Apocynaceae are highly diverse in Brazil, with around 760 species reported (Koch et al. 2015). In the last fifteen years, as a result of floristic, taxonomic or phylogenetic studies, several endemic species and genera have been described (e.g., Konno et al. 2006; Sales et al. 2006; Rapini & Farinaccio 2010; Rapini & Pereira 2011; Farinaccio 2013; Espirito Santo et al. 2018a ; b; Scudeler et al. 2018; Pereira et al. 2019). Mandevilla (apocynoids, Mesechiteae) comprises ca. 180 neotropical species (Morales 2018). It is characterized by its leaf blade with colleters on the adaxial surface of the midvein, racemose inflorescence, and style head with five longitudinal ribs (Simões et al. 2004; 2006). In Brazil, ca. 72 species are known, of which twelve are endemic to inselbergs (Tab. 1).

Table 1  Mandevilla species endemic to Inselbergs in Brazil. AL: Alagoas; BA: Bahia; ES: Espirito Santo; MG: Minas Gerais; PB: Paraiba; RJ: Rio de Janeiro; SP: São Paulo. 

Species State(s)
Mandevilla alata J.F.Morales & L. Kollmann * ES
Mandevilla crassinoda (Gardner) Woodson RJ
Mandevilla dardanoi M.F. Sales, Kin.-Gouv. & A.O. Simões AL, PB, PE
Mandevilla duartei Markgr. MG
Mandevilla fistulosa M.F. Sales, Kin.-Gouv. & A.O. Simões BA, ES, MG
Mandevilla grazielae M.F. Sales, Kin.-Gouv. & A.O. Simões ES, MG
Mandevilla harleyi M.F. Sales, Kin.-Gouv. & A.O. Simões MG
Mandevilla ibitubana J.F.Morales & L. Kollmann * ES
Mandevilla lucida Woodson ES, RJ
Mandevilla luetzelburgii (Ross & Markgraf) Woodson BA, ES, MG
Mandevilla splendens (Hooker) Woodson MG, RJ,
Mandevilla venulosa (Müller Argoviensis) Woodson RJ, SP

* Described here

During fieldwork led by the former Museu Augusto Ruschi and the Jardim Botanico do Rio de Janeiro two new species of Mandevilla restricted to inselbergs from Espírito Santo were found. The first has been collected on several inselbergs in Santa Teresa and Pancas, whereas the second is known from inselbergs near Ibituba, Baixo Guandu.

Materials and methods

This paper is part of the monograph of Mandevilla Lindl. and specimens from the following herbaria were consulted: A, AAU, ALCB, AS, ASE, ASU, B, BAB, BEREA, BHCB, BIGU, BM, BOLV, BR, C, CAS, CAUP, CAY, CDMB, CEN, CEPEC, CGE, CHAPA, CHOCO, CICY, CIIDIR, CIMI, CM, COAH, COL, CR, CVRD, CUVC, CUZ, DPU, DS, DUKE, E, EAP, ECON, ENCB, ESA, ESAL, F, FCME, FCQ, FDG, FI, FI-W, FMB, FUEL, G, G-BOIS, G-DC, GB, GFJP, GH, HAL, HB, HBG, HERZU, HOXA, HRB, HRCB, HSB, HUA, HUCO, HUQ, HURB, IAN, IBGE, ICESI, INPA, IPA, JAUM, JE, JEPS, JPB, K, L, LAGU, LD, LE, LIL, LLANOS, LP, LPB, LZ, M, MA, MBM, MBML, MEDEL, MEXU, MG, MICH, MIRR, MHES, MO, MOL, NY, O, P, P-BA, P-HB, P-JU, P-LA, PEL, PMA, PORT, PR, PSO, Q, QAME, QAP, QCA, QCNE, QPLS, R, RB, RON, S, SI, SP, SPF, SPFR, STRI, SURCO, TEFH, TRIN, TULV, U, UB, UBT, UC, UCAM, UCOB, UDBC, UIS, UPS, UPTC, US, USF, USJ, USM, USZ, UVAL, W, WU, WAG, WIS, VALLE, VEN, VIC, XAL, Z, and ZT, acronyms according to Thiers (2018). Descriptions were made based on herbarium specimens, preserved flowers (alcohol 70 %), and fresh material. Data on distribution, habitat, and phenology were obtained from herbarium vouchers and field notes. Parts of the corolla tube are described following Morales & Fuentes (2004). The terminology for the morphological description follows Radford et al. (1974) and Stearn (2004). The conservation status was assessed by calculating the extent of occurrence (EOO) and the area of occupancy (AOO) with GeoCAT (Bachman et al. 2011) and applying the IUCN Red List Categories and Criteria, version 3.1 (IUCN 2017). The AOO was calculated based on a user defined grid cell of 2 km.

Results and discussion

Taxonomic treatment

Mandevilla alata J. F. Morales & L. Kollmann, sp. nov. Type:-BRAZIL. Espírito Santo: Santa Teresa, Alto Perdido, 19°49’37"S, 40°44’23"W, 1/X/2010, L. Kollmann, R. Kollmann, 12061 (Holotype, MBML! [barcode MBML40557]; isotypes, MBML! [barcode MBML00004199, barcode MBML00004200], RB!).

Figs. 1, 2, 3.

Figure 1  Mandevilla alata. A. Branchlet with inflorescence. B. Detail of the leaf blade and petiole, showing the arrangement of the colleters. C. Detail of the adaxial surface of the leaf blade, showing the colleters along the midvein. D. Calyx, pedicel, and floral bract. E. Adaxial view of three sepals, showing the colleters at the base. F. Corolla tube partially open, showing the anthers. G. Anther, dorsal view. H. Style-head. I. Nectary and ovary. J. Follicles. K. Seed. (A-I from Kollmann & Kollmann 12061, MBML, J-K from Smith s.n., CR). 

Figure 2  Mandevilla alata A. Inflorescence and leave. B. Stem with longitudinal wings. C. Inflorescence with two flowers and buds.. D. Branch with follicles. 

Figure 3  Distribution map of Mandevilla alata and M. ibitubana. 

Mandevilla alata J. F. Morales & L. Kollmann resembles M. callista Woodson, but differs by its winged stems (vs. subterete), petiole 18-30(-36) mm long (vs. 55-135 mm), pedicels 6-16(-20) mm long (vs. 23-52(-65) mm), corolla throat red (vs. white), and anthers 6.5-7.2 mm long (vs. 8-9 mm).

Woody vine; stems with well developed longitudinal wings, sparsely and inconspicuously puberulent, soon glabrescent; interpetiolar colleters up to 1.5 mm in young stems, fully developed in old stems, up to 1 cm long. Leaves opposite; petiole 18-30(-36) mm long; blade 4.5-13.5(-15) × 3.2-6.5(-8) cm, ovate to ovate-elliptic, apex acuminate to caudate, base cordate, membranaceous, sparsely puberulent when young adaxially, soon glabrescent, abaxially glabrous, except for the sparse indument near the base of petiole, slightly bullate, without domatia, not revolute, colleters numerous, along the midvein, clustered at the base of the midvein, and along the petiole costa, secondary and tertiary veins conspicuously impressed on both surfaces. Inflorescence axillary, sparsely and minutely puberulent, glabrescent, many-flowered (+20), peduncle 43-98 mm long, pedicels 6-16(-20) mm long; bracts 4-5.5 × 0.9-1.2 mm, linear-ovate to linear-elliptic, scarious; sepals 2.2-4.1 × 1.1-1.7 mm, ovate, unequal, caducous during the anthesis, minute, the apex acuminate, not reflexed, minutely puberulent, the colleter solitary, opposite to the sepal, subentire to irregularly laciniate; corolla infundibuliform; tube greenish white proximally, reddish-white distally, lobes white, internal part of the tube red, minutely puberulent, lower part of tube gibbous, the lower part 15-20 × 3-5.1 mm, the upper part 13-16 mm long, campanulate, 13-17 mm in diam. at the orifice, the apex of the floral bud obtuse to rounded; lobes 18-22 × 9-11 mm, obliquely obovate; stamens inserted at the base of the upper part of the corolla tube, anthers 6.5-7.2 mm long, glabrous dorsally, the base auriculate, the auricles rounded, style-head 3.2-3.5 mm long; ovary 1.8-2.1 mm long, minutely puberulent; nectary annular, slightly 5-lobed, 1/2-2/3 as long as the ovary. Follicles 19-23.5 × 0.4-0.9 mm, free, only united at the apex, sparsely and minutely puberulent, inconspicuously moniliform; seeds 10-12 mm long, minutely puberulent, coma 8-26 mm long, tan.

Distribution and habitat: Endemic to Espírito Santo state, Brazil, growing on inselbergs at 200-750 m.

Phenology: Flowering in February, April, October, and December. Fruiting in January and October.

Etymology: the name refers to the winged stems, an unusual character in Mandevilla.

Conservation status: Endangered (EN). Mandevilla alata has an EOO of 670,803 km2 and AOO of 24 km2. As with many species of neotropical Apocynaceae, the actual population size is unknown. However, most of the populations of this species are located in areas without any kind of federal protection. The habitat where M. alata grows has been altered in recent years due to fire, which was confirmed during field work in 2010, 2014, and 2018. At least two populations were extinguished by fire in Pancas near Pedra Agulha. Based on its habitat restricted to Inselbergs, the low AOO and the fragmented and continuing decline of its habitat this species is classified as Endangered (EN) following the IUCN criteria B2a biii.

Observations: Few species in Mandevilla have winged stems (e.g., M. anceps Woodson, M. angustata (Steyerm.) J.F. Morales, M. lancifolia Woodson, M. nerioides Woodson) all of which grow on inselbergs in the Amazonian basin or quartzitic formations (Tepuis) of the Guayana shield in Colombia, Venezuela, Peru, and Brazil. Mandevilla alata is easily distinguished from these species by its petiolate leaves, with petioles usually more than 1.8 cm long (vs. 0.1-8 mm), inflorescences with peduncles 43-98 mm long (vs. 0-35 mm), and follicles 19-23.5 cm long (vs. 7-17 cm). Morphologically, Mandevilla alata resembles M. callista Woodson (1933: 700), but differs by its winged stems, shorter petioles, shorter pedicels, red corolla throat and smaller anthers. Mandevilla alata is restricted to Espírito Santo, whereas M. callista is known from Colombia to Bolivia, growing in wet forest from 300 m up to 1800 m of the Andes.

The discovery of a new Mandevilla of the “exothostemon” group from Espírito Santo was unexpected. This group of ca. 77 species was recognized as a subgenus by Woodson (1933) and as a section by Pichon (1948). However, these circumscriptions are not monophyletic (Simões et al. 2006). Most of the species have calyx lobes with a single colleter (sometimes deeply lacerated) and gibbous corolla tube. They are common in lowlands or middle elevations from Venezuela to Bolivia. In Brazil, they are most abundant in lowlands of the Amazonian basin. In Espírito Santo, only M. hirsuta (Rich.) K. Schum. and M. scabra (Hoffmanns. ex Rome. & Schult.) K. Schum., neither of which belongs to this group, have been reported. However, molecular studies are necessary to determinate the closest affinities of M. alata.

The region of Santa Teresa has been designated as one of the pilot areas of the Biosphere Reserve of Atlantic Forest in Espírito Santo, with many areas with high priority for biodiversity conservation (Mendes & Padovan 2000; Monge et al. 2018; 2019). Inselbergs are particularly abundant, but many remain unexplored because they are accessible only by air (Sarthou et al. 2009) (Fig. 4). In Mandevilla alone, at least four additional undescribed species have been collected recently on inselbergs in Santa Teresa and surrounding areas. Other Apocynaceae described from Espírito Santo and adjacent states include M. fistulosa M.F. Sales, Kin.-Gouv. & A.O. Simões, M. grazielae M.F. Sales, Kin.-Gouv. & A.O. Simões, and Rauvolfia capixabae I. Koch & Kin.-Gouv.

Figure 4  Inselbergs in Espírito Santo, Brazil (photos: J.F. Morales). A. Ibituba. B. Pancas. 

Paratypes: BRAZIL. Espírito Santo: São Roque de Canaã, Pedra do Pionte (São Bento), 28/II/2004, Fontana et al. 754 (CR, MBLM), 16/X/2004, Fontana et al. 949 (MBML); Santa Teresa, Vale do Canaã, 3/XII/1998, Kollmann et al. 1196 (MBML, UEC), 21/XI/2008, Kollmann et al. 11334 (CR, MBML); Santa Teresa, Alto Perdido, fazenda Montanhosa, terrenos dos Bridge, 14/IV/2007, Kollmann, et al. 9624 (CR, MBML), 14/IV/2007, Kollmann et al. 9623 (MBML); Santa Teresa, Vale do Canaã, 21/XI/2008, Kollmann et al. 11332 (CR, MBML); Lajinha, Pancas, 7/X/2007, Smith s.n. (CR).

Mandevilla ibitubana J.F. Morales & L. Kollmann, sp. nov. Type:-BRAZIL. Espirito Santo: Baixo Guandu, Ibituba, 19°41’32,26"S, 40°44’23"W, 13/IV/2013, L. Kollmann, A.P.Fontana, A.C.Lima, R.Gribel & M.Lemes 12660 (Holotype MBML (barcode MBML00045741)!, isotypes CEPEC!, CR!, RB!)

Figs. 2, 3, 5, 6.

Figure 5  Mandevilla ibitubana A. Branchlet with inflorescence. B. Detail of the stem pubescence. C. Calices, pedicels, floral bracts, and floral bud. D. Open corolla tube, showing the position of anthers. E. Adaxial view of two sepals, showing the colleters at the base. F. Details of the colleters. G. Anther, dorsal view. H. Style-head. I. Nectaries and ovary. J. Follicles. K. Seed. (A-I from Kollmann et al. 12660, MBML, J-K from Morais & Morales s.n., JAR). 

Figure 6  Mandevilla grazielae and M. ibitubana. A, D. Caducous sepals. B, E. Corolla bud. C, F. Corolla. (A-C, M. grazielae, D-F M. ibitubana; (photos: J.F. Morales) 

Mandevilla ibitubana J.F. Morales & L. Kollmann resembles M. grazielae M.F. Sales, Kin.-Gouv. & A.O. Simões but differs by subsessile leaves, with petioles 3-5 mm long (vs. 6-11 mm), corolla white (vs. purple), and anthers 3.9-4.2 mm long (vs. 6-7 mm).

Shrub 1-1.5 m; stems without wings, moderately to densely puberulent, glabrescent with age; interpetiolar colleters up to 0.5 mm in young stems, caducous or not evident in old stems. Leaves opposite; petiole 3-5 mm long; blade 3.4-6.7 × 1-3.1 cm, ovate to ovate-elliptic, apex acuminate, base slightly cordate, membranaceous, densely puberulent on both surfaces, not bullate, without domatia, not revolute, colleters numerous, clustered at the base of the midvein adaxially, secondary and tertiary veins conspicuously impressed abaxially, slightly impressed adaxially. Inflorescence axillary or terminal, minutely puberulent, 3-6-flowered, peduncle 6-17mm long, pedicels 4-9 mm long; bracts 1.2-1.3 × 0.5-0.8 mm, narrowly ovate, scarious; sepals 2.1-3.2 × 0.9-1 mm, narrowly ovate to narrowly ovate-elliptic, equal, caducous during the anthesis, minute, the apex acute, slightly reflexed, minutely and inconspicuously puberulent, colleters alternate with the sepals, 1-2, entire; corolla hypocrateriform; white, internal part of the tube cream, glabrous, corolla tube straight, 16-17 mm long, 1.4-2.3 mm in diam. at the orifice, the apex of the floral bud acute; lobes 14-16 × 10-12 mm, obliquely obovate; stamens about the middle of the tube length, anthers 3.9-4.2 mm long, glabrous dorsally, the base auriculate, the auricles rounded, style-head 1.7-1.8 mm long; ovary 2.8-3 mm long, glabrous; nectaries five, as long as the ovary. Follicles 3-4.5 × 1.5-3.2 mm, free, only united at the apex, minutely puberulent, inconspicuously moniliform; seeds 6-7 mm long, glabrous or glabrescent, coma 8-26 mm long, tan.

Distribution and habitat: Endemic to Espírito Santo, Brazil, growing on Inselbergs, at 200-400 m. Flowering and fruiting April, June, and July.

Etymology: the name refers to the type locality.

Conservation status: Critically endangered (CR), based on criteria B1ab + B2ab iii,iv. Only two populations are known (AOO = 8 km2), and they are restricted to Inselbergs and are represented by only a few individuals. No additional populations were found in other inselbergs in the Ibituba region, during recent field work in 2015 and 2018. Future surveys will probably reveal additional populations in other areas, but based on the current evidence, this species is assessed as CR on the IUCN Red List.

Observations: Mandevilla ibitubana resembles M. grazielae, sharing similar erect habit, short-petiolate leaves, reduced and few-flowered inflorescences, caducous sepals, and small follicles. The sepals of both species are caducous, falling off during anthesis or even when flowers are in buds (Fig. 6). This feature is unusual in Mandevilla and reported only in M. alata, M. grazielae, and M. ibitubana. In Mandevilla, sepals are persistent, falling off or sometimes persistent during fruiting or even can be persistent on fruits. Mandevilla ibitubana is separated by its petioles 3-5 mm long (vs. 6-11 mm), hypocrateriform corolla (vs. infundibuliform), corolla lobes white (vs. purple), and anthers 3.9-4.2 mm long (vs. 6-7 mm).

Baixo Guandu is located just in the border between Minas Gerais and Espírito Santo states. Ibituba is a small town located ca. 20 km S of Baixo Guandu and surrounded by many inselberg formations (Fig. 4). Few collections have been made in this area, mostly in the last decade, but it is basically unexplored. Further fieldwork can reveal more novelties.

Paratypes: BRAZIL. Espírito Santo: Ibituba, 6 km E, road to Itaguaçú, 9/VII/2018, Morais & Morales s.n. (JAR).

Key to species of Mandevilla growing on inselbergs in Espirito Santo, Brazil

1. Woody vines …………………………………………………………………………… 2

2. Stems conspicuously winged; leaf blades not bullate; sepals caducous during the antesis; corolla white, the mouth red, the lower part of the tube gibbous; follicles conspicuously moniliform ………………………………………………… M. alata

2'. Stems not winged; leaf blades bullate; sepals not caduceus, persistent; corolla pink, the lower part of the tube not gibbous; follicles more or less continuous, not moniliform …………………………………………………………………….... M. luetzelburgii

1'. Erect shrubs……………………………………………………………………………… 3

3. Corolla yellow, the mouth 16-20 mm in diam.; leaf blade obovate to obovate-elliptic… M. fistulosa

3'. Corolla purple, pink to white, the mouth 2-15 mm in diam.; leaf blade elliptic to ovate-elliptic ………………………………………………………………………… 4

4. Sepals persistent; inflorescence longer than the subtending leaves ……………………………………………………………………… M. lucida

4'. Sepals caducous during the antesis; inflorescence shorter than the subtending leaves … 5

5. Petioles 6-11 mm long; corolla infundibuliform; anthers 6-7 mm long ….… M. grazielae

5'. Petioles 3-5 mm long; corolla hypocrateriform; anthers 3.9-4.2 mm long … M ibitubana

Acknowledgements

Financial support was provided by the DAAD, the Museu de Biologia Mello Leitão, and the Missouri Botanical Garden. The first author thanks Andre Pavioti Fontana for support during fieldwork in Espirito Santo. Ludovic Kollmann thanks the “Instituto Nacional da Mata Atlântica”, from the “Ministério da Ciência, Tecnologia e Inovaçao (MCTIC) “Programa de Capacitação Institucional (PCI)” (CNPq - 312488/2016-5). The following herbaria allowed the study of their collections: CEPEC, CR, MBML, RB. Barry Hammel (MO) reviewed the English.

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Received: July 08, 2019; Accepted: September 18, 2019

* Corresponding author: drjfranciscomorales@gmail.com

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