Flora of Espírito Santo: Celastroideae (Celastraceae)

Abstract Here we present a taxonomic treatment of the subfamily Celastroideae (Celastraceae) in the state of Espírito Santo, southeastern Brazil, as a part of the ongoing project Flora do Espírito Santo. The work is based on analyses of herbaria specimens and fieldwork since 2012. Two genera and thirteen species are reported for Espírito Santo, covering all the vegetation formations found in the state. Celastrus is represented by one species, C. liebmannii, the unique climbing species of the subfamily in Brazil. Monteverdia are shrubs and trees characterized by fruits 2-valved, pericarp coriaceous and white aril. The genus is represented by twelve species, corresponding nearly to one third of the Brazilian species. Celastrus liebmannii is formally reported by the first time to Espírito Santo. Morphological descriptions, comments, color photographs plates, and identification keys for genera and Monteverdia species are provided.


Introduction
Celastraceae comprise about 1,200 species and 100 genera found in tropical, subtropical, and temperate areas worldwide (Simmons 2004).As currently delimited, the taxon includes the species formerly recognized in Hippocrateaceae as the subfamilies Hippocrateoideae and Salacioideae (Simmons 2004;Lombardi 2014).Celastraceae sensu stricto is nearly restricted to the subfamily Celastroideae, according to provisional delimitation by Simmons (2004).
Celastroideae (sensu Simmons 2004) include about 70 genera and 750 species.The subfamily is characterized by having alternate leaves (rarely opposite, in Zinowiewia only, in Brazil), intrastaminal disc, isostemonous androecium and stamens alternating with petals.In the New World, Celastroideae comprise erect plants (subshrubs to large trees), and the climbing Celastrus.The subfamilies Hippocrateoideae and Salacioideae are mainly climbing plants with opposite leaves (rarely alternate), extrastaminal disc, and with 3 (-5) stamens.In Brazil, Celastroideae comprise nine genera (eight with only one species) and 56 species, being the genera Celastrus and Monteverdia found in the state of Espírito Santo.
The Brazilian species in Celastrus and Monteverdia were first described as Maytenus.Maytenus racemosa Reissek (1861: 30) was described in Flora brasiliensis by Reissek and later transferred to Celastrus by Loesener (1896: 459), while all the remaining Brazilian Maytenus species were transferred to Monteverdia (Biral et al. 2017), with the exception of Maytenus boaria Molina (1782: 177), which is now the only species in the genus in Brazil.
Here, we provide a current overview of the subfamily Celastroideae (Celastraceae), in the state of Espírito Santo, in the Atlantic Forest of southeastern Brazil.We also provide identification keys, morphological descriptions, images, and comments on each species.The treatment herein is a contribution to the project Flora of Espírito Santo to fill some lacunae because there are no floristic studies of the family in the state.

Study site
Espírito Santo (ES hereafter) is a state in Southeastern Brazil (Fig. 1) and is divided into two geomorphological formations.The Barreiras formation occurs in the coastal plain in the south, that begins narrow and widens towards the north.Mountains occupy more inland areas, with the highest points at to 2,980 m, in the Serra do Caparaó (IPEMA 2005).Following the Köppen classification system, the plains are Aw and Am, while the mountains are Cfa and Cfb.Climate is seasonal throughout, with an average rainfall of 1,000 to 1,600 mm, and temperature of 24 ºC in the lowlands and 12 ºC in the highlands (Alvares et al. 2013).The Atlantic Forest phytogeographic domain dominates the state, with several types of vegetation, including mangroves, restingas, seasonal semideciduous forests, high-altitude grasslands, and dense ombrophilous forest (Simonelli & Fraga 2007;Garbin et al. 2017).

Taxonomic treatment
This treatment is based on herbarium material received by the first author while at the HRCB herbarium (acronyms follow Thiers, continuously updated), mostly from MBML and VIES (loans and donations).Additionally, the herbaria CVRD, MBML, RB, SAMES and VIES were visited by both authors.Images from recent collections were examined from virtual herbaria, available through SpeciesLink network (CRIA 2022) and Reflora -Virtual Herbarium (2022).In addition to examining herbarium specimens, botanical collections in ES have been done sparingly since 2012 and most of those specimens are at HRCB with duplicates at SHPR.Areas visited by the authors included Conservation Units in the municipalities of Cariacica, Santa Teresa, Sooretama and Linhares.
Morphological descriptions followed the model of the species descriptions in Biral et al. (2015) and terminology follows Radford et al. (1974).Conservation status of the species in the state followed Fraga et al. (2019) and CNCFlora "red list" at national level (CNCFlora 2022).Around 480 herbarium specimens were analysed for the elaboration of this floristic treatment.

Results and Discussion
Thirteen species in the Celastroideae are found in ES.The genus Celastrus is limited to C. liebmannii Standley (1931: 316-317), the only species in the genus in Brazil, and recently identified by the first time in the state.Monteverdia comprise twelve species, around 26% of the total species in this genus in the country (BFG 2018).Some species presented by Dutra et al. (2015) in the checklist of ES are based on herbarium misidentification [e.g., Monteverdia horrida (Reissek 1861: 5) Biral (Biral et al. 2017: 689), M. urbaniana (Loesener 1893: 10) Biral (Biral et al. 2017: 690), M. aquifolium (Martius 1841: 91) Biral (Biral et al. 2017: 688); see Biral (2022) for an example on the misidentification for the latter] and are not presented here.Three species are threatened in the state (Fraga et al. 2019): M. fugax and M. patens are endangered (EN) and M. macrophylla is critically endangered (CR).
Celastrus liebmannii is the only climbing species in the subfamily in Brazil, and the genus is the unique in Brazil that has 3-valved fruits with an orange to crimson aril that surrounds entirely the seed.The paniculiform cyme with a long peduncle identifies the species in the Neotropics.In Brazil, it is found from Bahia to Paraná mainly in the dense ombrophilous forest, and less commonly in the seasonal semideciduous and gallery forests.Even though distributed by a large geographic area, the species is infrequent within its distribution range, being represented by a few herbarium collections.In ES, C. liebmannii is found only in Conservation Units.Considering all Brazilian records, it seems that the species occurs mainly in pristine forests.A. Rich., Hist. Phys. Cuba, Pl. Vasc. 346. 1845.Shrubs to large trees, glabrous or rarely pubescent on young twigs.Stipules triangular to large triangular.Leaves margins entire, spinose or crenate/crenulate, along its entire margin or only close to the apex, sometimes obscurely crenate.Inflorescence fasciculate, a cyme, simple or compound, or reduced to an isolated flower, peduncle reduced or rare conspicuous, usually shorter than pedicels, multi or few-flowered; bracts and bracteoles minute, triangular, present at the base of the flowers and more rarely at the inflorescence ramifications.Flowers bisexual or functionally unisexual; sepals 5, imbricate, free; petals 5, imbricate, free; disc rounded, pentagonal or lobed, fused with the ovary wall, green in vivu, thickened; anthers ovate dehiscing by a longitudinal slit; carpels 2, style evident or reduced, stigma entire or slightly 2-lobed, ovules 2 per locule.Fruits spheroid or obovoid, 2-valved, red to yellow when ripe, apex rounded or quadrangular, style persistent (tiny) or not; seeds 1-3, smooth or rugose, blackened when dry, white aril.
Monteverdia gonoclada is probably a complex of species (Biral et al. 2017), and is found in many vegetation formations in Brazil, most commonly in the restingas, dense ombrophilous and seasonal semideciduous, and also in the Cerrado and campos rupestres (rocky, high elevation fields) (Carvalho-Okano & Leitão-Filho 2004).This species is characterized by the combination of flattened twigs, elliptic, often pruinose, leaf with crenate margins, and compound cymes with an evident peduncle (usually longer than the pedicel).In ES, the species occurs in dense, riverine and seasonal forests, at 250-1,143 m of elevation, where it is not as abundant as in similar forests in Minas Gerais and São Paulo.It may be confused with M. brasiliensis because of similar leaf size and shape, but it can be differentiated by its pruinose leaf with entirely crenate margins.
Monteverdia macrophylla is a shrub from the understory of the dense ombrophilous and the seasonal semideciduous forests, from Bahia to Rio de Janeiro, at from sea level to 500 m elevation.This species is identified by its large, often spinosemargined (sometimes entire) leaf, and quadrangular red (when ripe) fruit.The number of spines on leaves margins is variable: e.g., the specimen J.R. Pirani et al. 3458 (K,2 sheets,NY,SPF) has leaves with entire margin, with four pairs of spines near at the leaf base, and with seven pairs of spines evenly distributed along the leaf length.Monteverdia macrophylla is sometimes misidentified in herbaria collections as M. aquifolium (Mart.)Biral because of its spinose leaves, but large leaf size and quadrangular, red (when ripe) fruit clearly separate the species.Quadrangular fruit allows confusion with M. horrida, from the Caatinga of Minas Gerais and Bahia.According to the label of Gomes 3202 (HRCB, VIES), the species is locally known by the vernacular name "camboatá-de-espinho".
The species was reported as critically endangered (Fraga et al. 2019) several locations suggesting a larger population size, so its inclusion in this category may need to be re-examined; putatively is not a threatened species in the state.In addition to the 12 municipalities in which it has been found, we found unvouchered specimen from Sooretama.

Assis et al. 761 (VIES).
Monteverdia obtusifolia is a shrub or treelet endemic to Brazil, from northern coastal São Paulo to Pará state (Carvalho-Okano & Leitão-Filho 2004), found commonly in the restinga and mangroves, and less often in the dense ombrophilous and in seasonal forests (brejo de altitude) in northeastern Brazil (BFG 2018).Among the commonest species of Celastraceae in ES, it is found in abundance in herbarium collections.Monteverdia obtusifolia is easily recognized by leaf and inflorescence.The leaf is variable in size and shape, always with inconspicuous secondary veins visible on both surfaces of the leaf.The leaf is often pruinose and discolor, gray to bluish on the adaxial side and reddish on the abaxial side, when dried.The inflorescence is a ramified cyme, compound (paniculiform), with an evident and long peduncle, longer than the pedicel, unusual for the genus.May be confused with M. distichophylla by the leaves but is differentiated by the ramified versus fasciculate inflorescence.
Monteverdia patens occurs discontinuously in the dense ombrophilous forest from Paraíba to Santa Catarina but can be found in the brejos de altitude and in the Caatinga of northeastern Brazil, from 50 to 1,160 m of elevation.In ES, a few specimens have been collected in the tabuleiros forests.It is characterized by the combination of pubescent twigs, entire or obscurely crenate leafmargins and multi-flowered fascicles.The species resembles M. evonymoides due to leaf size and inflorescence but the entire or obscurely crenate versus conspicuously crenate leaf, the ratio of leaf dimensions (1:2 vs. 1:3), and the life form (tree rather than shrub or small tree) separate the former from the latter.Nonetheless, the distinction between both species is not well delimitated and additional study is necessary.
Monteverdia quadrangulata is endemic to Brazil, found in the states of ES, Minas Gerais and Bahia, in the Atlantic Forest (dense ombrophilous forest, seasonal semideciduous forest and rocky outcrops), between 120-600 m of elevation.Few specimens are available in herbaria.It may be confused with M. macrophylla because the spinose leaves, but its quadrangular young twigs and many spines on the leaf margin (18-33 rather than 9-13 in the latter) clearly identify it.The species was classified as EN (endangered) in the latest version of the "Red list" provided by CNCFlora (2022).
Monteverdia schumanniana is a shrub or treelet in the dense ombrophilous forest understory.The species occurs from southern Bahia to Santa Catarina from sea level to ca. 1,000 m (decreasing commonness with altitude).Its winged or strongly flattened young twigs, large flower (5-6 mm diameter) in contracted and few-flowers cymes clearly identify it.The inflorescence in M. schumanniana is contracted with an inconspicuous peduncle that may be seen under magnification.The specimen Kollmann 3275 (MBML, RB) is labelled as a scandent shrub, but which characteristic (scandent) has not been observed or reported elsewhere.

Figure 1 -
Figure 1 -Map of study area, the Espírito Santo state, Southeast Brazil, highlighting the altitudinal range.
, but we found recent collections of Monteverdia macrophylla from
in herbaria collections.Monteverdia ardisiifolia has never been collected in ES, and has larger, elliptic-obovate, leaves that usually dry dull, with 10-14 pairs of inconspicuous, on both sides of the leaf, secondary veins.