Three new species of Euphorbia subgenus Chamaesyce (Euphorbiaceae) endemic to Brazil

We describe and illustrate three new species of Euphorbia subgenus Chamaesyce from Brazil: E. blepharadena O.L.M.Silva & Cordeiro sp. nov., E. longipedunculata O.L.M.Silva & Riina sp. nov. and E. sobolifera O.L.M.Silva & P.J.Braun sp. nov. Based on morphological characteristics, E. blepharadena sp. nov. and E. longipedunculata sp. nov. are placed in the subcosmopolitan section Anisophyllum, whereas E. sobolifera sp. nov. is placed in the more geographically restricted section Crossadenia. The three new species are compared with their most similar species in each section, and accompanied by comments on habitat and distribution, illustrations, photographs, and proposed conservation status.


Introduction
Euphorbia L. includes more than 2000 species, which makes it the most diverse genus of Euphorbiaceae Juss., and one of the largest within the angiosperms (Govaerts et al. 2000;Horn et al. 2012;Webster 2014). Despite its great variation in morphology, ranging from small annual plants to large and longlived trees, the genus is characterized by a synapomorphy, unique among angiosperms, the cyathium (Horn et al. 2012). This pseudanthial inflorescence consists of a cup-like involucre with glands along its rim (sometimes with appendages of several types) enclosing a single, central pistillate flower surrounded by four or five staminate cymules with reduced axes. Both the pistillate and staminate flowers are highly reduced to a single pistil and a single stamen, respectively (Radcliffe-Smith 2001;Prenner & Rudall 2007;Horn et al. 2012;Webster 2014), and in some species with unisexual cyathia, pistillate or staminate flowers may be reduced to a pistillode or staminodes (Rizzini 1989;Silva et al. 2020).
Phylogenetic studies have confirmed the monophyly of Euphorbia and recognized four subgenera: E. subg. Athymalus Neck. ex Rchb., restricted to the Old World ); E. subg. Esula Pers., mostly centered in temperate regions of the northern hemisphere ); E. subg. Euphorbia, the most morphologically diverse, found mainly in the tropics and subtropics (Dorsey et al. 2013); and E. subg. Chamaesyce Raf., distributed primarily in the New World but also represented in the Old World (Yang et al. 2012).
Brazil is the most Euphorbia species-rich country in South America (Steinmann 2013). Currently, 64 native species of Euphorbia are recorded for Brazil, half of them endemic to the country (Flora do Brasil 2020, in construction). Since the last complete treatment of the genus for Brazil (the monograph in Flora Brasiliensis by Müller Argoviensis 1874), additional new species and new occurrences have been published, even in the past few years (Carrillo-Reyes & Steinmann 2011;Carneiro-Torres et al. 2012;Silva & Cordeiro 2015;Hurbath et al. 2018;Küllkamp et al. 2018;Silva et al. 2020).
Euphorbia subg. Chamaesyce is the most species-rich lineage of Euphorbia in Brazil, with two thirds of the species belonging to this subgenus. Within the subgenus, E. sect. Anisophyllum Roep. and E. sect. Crossadenia Boiss. are the most diverse sections, with 27 and 11 species, respectively (Flora do Brasil 2020, in construction;Silva et al. 2020). Based on extensive herbarium studies, we present and describe three new Brazilian species of Euphorbia subg. Chamaesyce, and, based on morphological evidence, we place two of them in E. sect. Anisophyllum and the third one in E. sect. Crossadenia.

Material and methods
We examined the collections of Euphorbia deposited in SP, SPF, HUEFS, MBM and RB; acronyms of herbaria follow Index Herbariorum (Thiers, continuously updated). Protologues and type specimens of related species were also analyzed through JSTOR Global Plants website (https://plants.jstor.org/). Morphological descriptions were based on observations using a 10−60 × magnification stereo microscope. We followed Beentje (2010) for general terminology, and for cyathial features we applied the specific terms from the Euphorbia Planetary Biodiversity Inventory group (www.euphorbiaceae.org) and relevant systematic treatments for Euphorbia (Horn et al. 2012;Yang et al. 2012). The distribution map was generated in QGIS ver. 3.14 (QGIS Development Team 2020), and the conservation status was proposed based on the International Union for the Conservation of Nature guidelines (IUCN 2019), adopting area of occupancy with a cell width of 2 km in GeoCAT (available from geocat.kew.org/).

Etymology
The epithet is a reference to the cyathial gland appendages, which look like eyelashes on these glands (Fig. 1G).

Distribution, ecology, and phenology
Euphorbia blepharadena sp. nov. occurs in clay soils in flat rocky outcrops (ʻlageadoʼ) in northeast Minas Gerais, within the Cerrado domain (Fig. 2). The only specimen found so far was collected in October with both flowers and fruits.

Provisional conservation status
Euphorbia blepharadena sp. nov. is only known from a single locality (Fig. 2), with AOO < 10 km² and EOO < 100 km². Its habitat is subjected to continuing decline in area, extent and quality. In the light of this, our evaluation suggests it to be classified as Critically Endangered (CR; B2ab[iii]).

Etymology
The epithet is a reference to the long peduncle of the cyathium (Fig. 3A), which is remarkable among all species of Euphorbia in Brazil.

Provisional conservation status
Euphorbia longipedunculata sp. nov. is only known from a single location (Fig. 2), it has AOO < 10 km² and EOO < 100 km². As this location is close to roadsides, it is subject to continuing decline in area, extent and quality due to the always growing anthropic pressure in Central Brazil.

Etymology
The epithet refers to the soboliferous growth form of the species: when a stem becomes decumbent and reaches the soil, it starts branching and eventually roots. This allows E. sobolifera sp. nov. to form dense colonies in the rocky outcrops where it grows (Fig. 4B).

Distribution, ecology and phenology
Euphorbia sobolifera sp. nov. grows in open vegetation on sandstone outcrops (Fig. 4A) in the Serra do Tombador, near the Jacobina Municipality, in the northern portion of the Chapada Diamantina complex in Bahia State, within the Caatinga domain (Fig. 2). The species was collected during the dry season (August) with immature fruits, but individuals cultivated in the São Paulo Botanical Garden have been producing cyathia throughout the year, although we could not make them produce viable fruits.

Provisional conservation status
Euphorbia sobolifera sp. nov. is only known from a single locality (Fig. 2), with AOO < 10 km² and EOO < 100 km², and its habitat is subjected to continuing decline in area, extent and quality. We suggest that it should be classified as Critically Endangered (CR; B2ab[iii]).

Discussion
Both Euphorbia blepharadena sp. nov. and E. longipedunculata sp. nov. are here placed in E. sect. Anisophyllum based on morphological characters, such as the presence of interpetiolar stipules and opposite leaves with the base asymmetrical (Yang et al. 2012). Euphorbia sobolifera sp. nov., in turn, Amongst the species of Euphorbia sect. Anisophyllum found in Brazil, E. blepharadena sp. nov. is most similar to E. foliolosa. due to its long and entire styles (Fig. 1H) and the presence of a colleter on the apex of leaf margin teeth ( Fig. 1D; Silva et al. 2014). Euphorbia bahiensis (Klotzsch & Garcke) Boiss. and E. hyssopifolia L. also share with E. blepharadena sp. nov. the herbaceous and erect habit with cyathia arranged in dichasia, but lack the features shared with E. foliolosa mentioned above (Silva et al. 2014). A more detailed comparison among E. bahiensis, E. blepharadena sp. nov., E. foliolosa and E. hyssopifolia is presented in Table 1.
The cyathial glands bearing digitate appendages (Fig. 1G)  Euphorbia longipedunculata sp. nov., the other new species placed in E. sect. Anisophyllum, was hidden in numerous herbaria collections under the common E. potentilloides, which is widely distributed across the Cerrado domain (Simmons & Hayden 1997). This was most probably due to the superficial resemblance of these species, especially considering the plasticity in leaf shape of E. potentilloides as described by Simons & Hayden (1997). Despite the high variability in leaf shape (Simons & Hayden 1997: fig. 17), E. potentilloides is not known to possess orbicular leaves as in E. longipedunculata sp. nov. (Fig. 3A).
Another species that is also similar to Euphorbia potentilloides is E. burchellii Müll.Arg (Müller Argoviensis 1874). However, E. burchellii is only known from the type and rarely would be confused with E. longipedunculata sp. nov., due to its lanceolate to linear leaves (vs rounded in E. longipedunculata sp. nov.). A comprehensive comparison among these three species is given in Table 2.
Within Euphorbia sect. Crossadenia, the third newly described species, E. sobolifera sp. nov., is most similar to E. appariciana due to its 6-costate stems with short internodes (Fig. 4C-E) and unisexual cyathia ( Fig. 4F-M) but differs from the latter by being dioecious (vs monoecious in E. appariciana) and presenting more conspicuous and opposite leaves (Fig. 4E), while in E. appariciana, the leaves are completely absent or very rudimentary (Rizzini 1989). Additionally, E. sobolifera sp. nov. has longer and thinner stems that reach up to 2 m long, becoming decumbent (Fig. 4B), whereas in E. appariciana, stems are thicker, always erect and they usually reach up to 20 cm tall. Slender decumbent branches are also present in E. teres M.Machado & Hofacker, but the latter has terete stems (vs 6-costate stems in E. sobolifera sp. nov.; Fig. 4E). Finally, Euphorbia flaviana Carn.-Torres & Cordeiro also has terete stems, but these are always erect, reaching more than 1 m high, and its cyathial glands are similar to those of E. sobolifera sp. nov., but they lack an appendage (vs short crenulate appendage in E. sobolifera sp. nov.). A morphological comparison of the new species with the others mentioned above is given in Table 3.
The dioecy of Euphorbia sobolifera sp. nov. was confirmed through the observation in cultivation of three distinct individuals. These were collected by B.G. Brito in the type locality and sent to São Paulo for cultivation at the São Paulo Botanical Garden (two individuals of different sexes) and also at the Botany Department at the University of São Paulo (one male individual). Individuals of different sexes were growing together in the São Paulo Botanical Garden and we have been observing them for around one year while one consistently produced staminate cyathia and the other pistillate ones. However, a single fruit was observed in an individual at São Paulo Botanical Garden (Fig. 4K), that unfortunately did not reach maturity. Therefore, fruits and seeds are missing in the description and type specimen of E. sobolifera sp. nov., because we were unable to cross the individuals to produce more viable fruits. Branches from both male and female individuals collected by B.G. Brito were gathered to compose a single herbarium sheet to better represent the species in the holotype in accordance with article 8.2 of the International Code of Nomenclature for Algae, Fungi and Plants (Turland et al. 2018 seeds could not be observed in this species, representatives of Euphorbia sect. Crossadenia have highly conserved seed features (seed coat with low and rounded tubercles and the presence of a caruncle-like feature but without an elaiosome) that may be synapomorphic to the group (Yang et al. 2012;Silva et al. 2020).
In conclusion, the three new species presented in this work represent important additions to the Euphorbiaceae in the Flora of Brazil 2020 project, increasing the number of species of Euphorbia in Brazil to 67. These new species also show interesting uncommon features among the Brazilian species: the dioecy and soboliferous growth form of E. sobolifera sp. nov., the long pedunculate cyathia of E. longipedunculata sp. nov., and the digitate cyathial glands of E. blepharadena sp. nov., which is rare in E. sect. Anisophyllum. Although these species are only known from their types, descriptions of taxa from single collections are important for conservation and enhancement of sampling efforts in underexplored areas of the Neotropics (Wood et al. 2017;Antar et al. 2018;Riina et al. 2018;Silva et al. 2020).