Miconia gigantea , a long-forgotten endemic and endangered species of Melastomataceae in the Brazilian Atlantic Forest

Taxonomic and floristic studies in the state of Rio de Janeiro allowed the rediscovery of Miconia gigantea, an endemic species to the Atlantic Forest, until recently known only from the type specimen, collected over 100 years by A.F.M. Glaziou. We present an amended and detailed description of M. gigantea, providing characteristics of the flowers, fruits and seeds, in addition to illustrations, comments about taxonomic affinities with closely related species, the presently known distribution together with new occurrence records, and the conservation status.


INTRODUCTION
In the Brazilian flora, Melastomataceae are the sixth-richest family of angiosperms, with 1,360 species, and the fifth-richest family in terms of endemism, with 408 species that are found only in the Atlantic Forest (Forzza et al. 2010, Baumgratz et al. 2015a).
Miconia Ruiz & Pav. is the genus with the greatest number of species in Brazil, represented by 281 species, of which 76 are endemic to the Atlantic Forest (Goldenberg and Caddah 2015).The genus has a wide morphological diversity, and has not been revised since the monographs of Cogniaux (1886Cogniaux ( -1888Cogniaux ( , 1891)), with several taxa circum-scribed by inconsistent morphological characteristics (Goldenberg et al. 2013).
Miconia gigantea Cogniaux is one of the 26 species which are endemic of the Atlantic Forest in the state of Rio de Janeiro.Although there are several floristic and taxonomic studies on the family Melastomataceae in this state, no record of this species is mentioned (Baumgratz 1980, 1982, 1984, 1996, 1997a, b, Baumgratz et al. 2006, Silva et al. 2013, Silva-Gonçalves et al. 2014).The few floristic studies conducted in the region where the type specimen was collected (municipality of Angra dos Reis) did not mention the occurrence of the species (Callado et al. 2009, C.Y.G. Manão, unpublished data).However, L.P.G.Rosa (unpublished data) conducted a floristic and phytosociological study of the Montane Atlantic LILIAN P.G.DA ROSA, JOSÉ F.A. BAUMGRATZ and SEBASTIÃO J. DA SILVA NETO Forest in the Ilha Grande State Park, from the same municipality, and listed M. gigantea as a doubtful species, because the material found was sterile.Cogniaux (1891) described M. gigantea as doubtful (species incertae sedis), and based on a single, sterile collection (Glaziou 17548).Recent surveys and floristic studies have recognized this species as endemic to the Atlantic Forest and to the flora of the state of Rio de Janeiro (Stehmann et al. 2009, Forzza et al. 2010, Goldenberg et al. 2013, The Plant List 2013, Baumgratz et al. 2015b, Goldenberg and Caddah 2015).
Fieldwork has led to the rediscovery of Miconia gigantea in the municipality where the type was collected, and in nearby poorly known or previously unvisited areas.Several individuals of M. gigantea were found in areas with the same type of physiognomy and altitudes, with vegetative characteristics consistent with those described in the original paper (Cogniaux 1891), and matching the type specimens.Furthermore, specimens collected with flowers and fruits have now made it possible to confirm the distinctiveness of this species.We present an amended and detailed description of M. gigantea, providing morphological characteristics of the flowers, fruits and seeds, in addition to illustrations, comments on taxonomic affinities with closely related species, the presently known distribution, with new occurrence records, and the conservation status.
Samples were collected on expeditions to the Conservation Units of the state of Rio de Janeiro.
Five samples of each individual in reproductive and/ or vegetative state was collected according to the usual procedures of taxonomic studies proposed by Guedes-Bruni et al. (2002).Reproductive structures were fixed in 70% ethanol for morphological studies and illustration.Habitat, ecological aspects of the populations, details of vegetative and reproductive characteristics and phenological data were record in the field, in addition to photographs.Vouchers were deposited at HRJ and RB (acronyms according to Thiers 2013).
The description was prepared through detailed analysis of vegetative and reproductive structures of the specimens collected and samples of herbarium BR, F, HRJ, K, P, R, RB and RBR, including types.For the species description we used concepts and terminology proposed by Radford et al. (1974) and Baumgratz (1985).Abbreviations of author names follow Brummitt and Powell (1992).
Specimens examined: BRAZIL.Etymology: The epithet "gigantea" refers to the large size of the trees, described on the labels of type individuals (BR and P) by A.F.M. Glaziou as "très grand arbre".
Phenology: The specimens were collected with flowers in August and September, and with fruits in August, September and December.
Distribution and Habitat: Miconia gigantea was found predominantly in remnants of Dense Montane Ombrophilous Forest, and more occasionally in Submontane formations, in areas of the municipalities of Angra dos Reis, Mangaratiba, Paraty and Rio Claro, in the state of Rio de Janeiro (Fig. 3).It occurs aggregated or sparsely distributed within and on the slopes of preserved humid forests, in addition to treeless areas, ranging from 400-800 m elevation (Fig. 2a, b).Most individuals collected are large, with stem circumferences up to 1.14 m.
Conservation status: Miconia gigantea is endemic to the state of Rio de Janeiro, thus far known only from montane and submontane Atlantic Forest in four contiguous municipalities in the southern part of the state, including an insular remnant (Ilha Grande).It has an EOO of 1.333,79 km² and AOO of 44 km², and is subject to four situations of threat.The fragmentation of vegetation due to grazing areas and/or expansion of urban and rural areas has led to a continuing decline of the EOO, AOO and habitat quality.Although this species occurs in four Conservation Units (Ilha Grande State Park, Cunhambebe State Park, Serra da Bocaina National Park, and Rio das Pedras Private Natural Heritage Reserve (RPPN)), there is no guarantee of the viability of subpopulations since they are represented by only a small number of individuals, except in Cunhambebe State Park, where there are more than 80 trees.Based on our current knowledge, the values of EOO and AOO, and IUCN (2014) criteria, the species is assigned a conservation status of Endangered [EN B1ab (i,ii,iii) + B2ab (i,ii,iii)].
Taxonomic relationships: The position of Miconia gigantea in Cogniaux's classification (1886-1888; 1891) for the genus is very doubtful, due to inconsistencies in the circumscriptions of the sections and series.The tentative nature of this classification is also apparent in the results of recent phylogenetic analyses that showed these taxonomic categories of Miconia as non-monophyletic (Michelangeli et al. 2004, Goldenberg et al. 2008). Recently, Goldenberg et al. (2013) noted the possibility that M. gigantea belongs to the section Glossocentrum, probably due to the morphological similarity with Miconia cabucu Hoehne.Based on the anthers that are short, oblong, and with the apex obliquely truncated and the connective sometimes with a dorsal calcar, M. gigantea can be placed in this section.It is very close to M. cabucu, and Goldenberg and Reginato ( 2007) pointed out that the two may be a single taxon.However, M. cabucu can be distinguished, mainly, by the generally smaller leaves, and the anthers with an attenuated base and the connective with ventral appendage.In addition, so far there is no record of the latter for the flora of the state of Rio de Janeiro, based on the checklists of Baumgratz et al. (2015b) and Goldenberg and Caddah (2015).
Within section Glossocentrum, Miconia gigantea also shows similarities to two species that are endemic to the state of Rio de Janeiro, M. saldanhae Cogniaux and M. oblongifolia Cogniaux, in having leaves with 5 acrodromous veins distinctly suprabasal, the abaxial surface rufous, densely covered with stellate trichomes, and pentamerous flowers, with the lobes of the calyx much smaller than the tube.However, M. saldanhae is distinguished by the leaves with shorter petioles (1-2 cm long), base often attenuate, calyx clearly with 4-5 lobes, and the ovary distinctly pilose.Miconia oblongifolia differs from M. gigantea in having leaves with shorter petioles (2-3 cm long), shorter petals (ca. 2 mm long), and unappendaged stamens.Two other species of Glossocentrum section that occur in southeastern Brazil have morphological similarities to Miconia gigantea.Miconia gigantea by the size of the tree, morphology of the leaves, and nodes of the branches with interpetiolar linear protrusions, as also noted by these authors.However, M. shepherdii is distinguished mainly by the indumentum of dendritic trichomes, leaves with denticulate margin, and tetramerous flowers, with unappendaged stamens.Miconia gigantea can also be said to resemble M. formosa Cogn., by the tree habit, indumentum stellate-lepidote, and discolorous leaves, but the latter is distinguished by leaves that are smaller, narrow-elliptic to elliptic, with bases cuneate to acute, apices short to longacuminate (or abrupt cuspidate) and acrodromous veins clearly (1-3 cm long) suprabasal.
In Dense Ombrophilous Forest formations in the state of Rio de Janeiro, the main morphological features of Miconia gigantea that make it possible to identify it in the field, including in the canopy, are: the leaves generally large in length and width, which can reach to 55 × 40 cm, discolorous, with the adaxial surface green, and the abaxial surface grey-brownish to pale-brownish, and the indumentum completely covering the abaxial surface (Fig. 1a, b).In these characteristics, M. gigantea can resemble M. formosa, M. hypoleuca Triana, M. ovalifolia Cogniaux and M. shepherdii, but the vegetative and reproductive characteristics can distinguish them from each other: Miconia hypoleuca by the lanate indumentum, leaves with higher order venation forming a fine, well-defined reticulum and mature orange fruits; M. ovalifolia by the tomentose-stellate indumentum; and M formosa and M shepherdii by the characteristics previously mentioned.Moreover, M. gigantea can also be placed in Miconia series Glomeratiflorae (Cogniaux 1886(Cogniaux -1888(Cogniaux , 1891)), based on the inflorescences in panicles with no spiciform branches, and flowers arranged in glomerules, with short oblong anthers, 1-porose, and the connective appendage slightly 2-lobed.In this series it is related to M. crassipes Triana, M. organensis Gardner and M. ovata Cogniaux, by having leaves with the abaxial surface brownish, completely covered by the lepidotestellate indumentum.Miconia organensis differs in its unappendaged stamens and pilose ovary; M. ovata in its crenulated-denticulate leaf-margins and persistent calyx; and M. crassipes in having leaves with auriculate-cordate base and slightly denticulate margin, and in the shorter length of the petiole, in addition to being endemic to Peru.
M.K. Caddah (unpublished data) while carrying out taxonomic studies in Miconia sect.Discolor subsect.Discolor Caddah & R.Goldenb., proposed the synonymization of M. gigantea, M. cabucu and M. ovalifolia with M. formosa.However, based on our previous reviews and by the fact that the author analyzed only the material type and sterile of M. gigantea, we do not agree with this proposition.These species are morphologically closely related, and we believe that population genetics research associated with phylogenetic studies may improve the understanding of the relationships between them.
Notes: Advancing knowledge of the diversity of Miconia in the Brazilian Atlantic Forest is still a challenge, because the numerous species present in this domain, the lack of taxonomic revision, species poorly known or represented by few specimens or only the type specimen, and unidentified specimens in herbaria collections.Furthermore, nomenclatural problems still persist, and the classification of the genus is complex.Recent phylogenetic studies for the tribe Miconieae show Miconia as a polyphyletic genera.Miconia gigantea is a good example of this, because until very recently existing trees were unknown, as well as a fertile specimen collected in the nineties, and the taxon was described based only on a sterile specimen.

CONCLUSIONS
The rediscovery of Miconia gigantea has allowed us to present an amended description for the species, describing for the first time the flowers and fruits, and to increase the knowledge of vegetative characteristics.It also provides fertile specimens in herbaria, reveals new areas of occurrence for the species and highlights M. gigantea for the first time as an Endangered Brazilian species.The control of threats in the areas of occupancy and monitoring of the species are necessary in order to ensure the maintenance of M. gigantea in nature.Thus, the rediscovery of Brazilian species of Melastomataceae can provide valuable information about the Brazilian flora, increasing morphological and ecological knowledge of the taxonomic diversity of the family, and assist in the solution of taxonomic problems.

ACKNOWLEDGMENTS
We are grateful to the curators of the above-cited herbaria for making their collections available for study; to Luiz Antonio Ferreira dos Santos Filho for the review of the assessment of the species conservation status; to Maria Alice de Rezende for the illustrations; to Rafael Ribeiro for the map; to anonymous reviewers for the valuable suggestions ; to the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) for financial support to the first author, and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brazilian National Council for Scientific and Technological Development) for financial support to the second author.
Figure 2 -a.individuals of Miconia gigantea Cogn.(arrows) in Dense Ombrophilous Forest of the Cunhambebe State Park, Rio de Janeiro, Brazil, which are distinguished by the color of the adaxial surface of the leaves.b. remnant individuals of M. gigantea in a pasture area.c. detail of buds and flowers.d. details of young (green) and mature (purple-black) fruits.

Figure 3 -
Figure 3 -Distribution map of Miconia gigantea Cogn., endemic to Rio de Janeiro, southeastern Brazil, with the localities of the occurrence the specimens.