Novelties in Brazilian Waltheria L. (Byttnerioideae, Malvaceae): two new species and one re-establishment

452 Acta Botanica Brasilica 34(3): 449-459. July-September 2020 Figure 1. Geographical distribution of Waltheria biribiriensis, W. brachypetala, W. ferruginea and W. terminans in eastern Brazil, with details of (A) phytogeographic domains and (B-C) bioregion delimitations. CDp: Chapada Diamantina Province; SERp: Southern Espinhaço Province, with its districts (GMd: Grão-Mogol District, DPd: Diamantina Plateau District and IQd: Iron Quadrangle District). Table 1. Main diagnostic features of the “Waltheria ferruginea alliance” sensu Saunders (1995, unpublished), comparing Waltheria biribiriensis, W. brachypetala, W. ferruginea and W. terminans. Character W. biribiriensis W. brachypetala W. ferruginea W. terminans Stipule length (mm) c. 6.0 7.0–11.0 3.0–3.2 7.0–9.0 Leaf blade length (cm) 3.5–13.0 4.2–10.2 3.4–10.4 1.6–2.6


Introduction
Waltheria is a pantropical genus including c. 50-60 species (Bayer & Kubitzki 2005), with 23 of them native to Brazil (Silva- Coutinho et al. 2019). Although the genus is widespread, species of Waltheria are usually narrowly restricted to particular regions of the Neotropics, northern Mexico and North America (Saunders 1993). Most species are endemic to the open, seasonally dry habitats in South America, namely the Brazilian Cerrado, Caatinga and Chaco (Saunders 1995, unpublished).
Waltheria is a shrubby-herbaceous genus belonging to Byttnerioideae -one of the nine clades in Malvaceae sensu Alverson et al. (1999), supported by further studies (e.g. Whitlock et al. 2011;Richardson et al. 2015). Byttnerioideae is characterized by having clawed and often caducous petals, small flowers, shorter than 2-3 cm in length, without epicalyx and usually with a reduced or absent androgynophore. Palynological traits can be diagnostic for the subfamily as well, and most species exhibit elongated pollen grains with prominent operculate apertures (Cristóbal 1968;Bayer & Kubitzki 2005). Waltheria is placed in Hermannieae, a tribe distinguished by having flat petals and absence of androgynophore (Saunders 1995;unpublished). Waltheria is also within subtribe Melochinae, where trends such as the gradual reduction of the number of ovules per locule are observed (Saunders 1995, unpublished;Bayer & Kubitzki 2005).
Melochinae species usually have heterostylic flowers, where two floral morphotypes, "longistylous" and "brevistylous", exhibit different stamen/style length ratios (Kohler 1976;Saunders 1993). Waltheria presents the floral polymorphism typical of the subtribe as well as the uttermost case of carpel reduction, with its species bearing only one carpel with one locule and two ovules per locule, typically producing only one seed per capsular fruit (Saunders 1995, unpublished;Bayer & Kubitzki 2005).
Several infrageneric classifications have been previously applied to Waltheria (e.g. Schumann 1886; Rose 1899; Saunders 1995, unpublished). Saunders (1995, unpublished) provided one of the most important contributions to the systematics of the genus, addressing evolutionary aspects of heterostyly as well as infraspecific taxonomical circumscriptions (except for the W. indica complex). Saunders described ten new species (1995, unpublished), with only three of them effectively published (Saunders 2005;Saunders & Pozner 2007).
We have identified unpublished names of taxa endemic to specific regions of campo rupestre vegetation that require revision. According to Saunders (1995, unpublished), the areas of campo rupestre in the eastern South American mountaintops are the major center of species richness of Waltheria, with many species or potential clades, such as the Waltheria ferruginea alliance sensu Saunders (1995, unpublished), restricted to this high-elevation habitat. These species are found in different areas of campo rupestre determined as the newly recognized districts of the Southern Espinhaço province (Colli-Silva et al. 2019).
Given this background, we hereby present taxonomical and nomenclatural novelties in a set of species that belong in the informal Waltheria ferruginea alliance sensu Saunders (1995, unpublished). We provide detailed morphological information, updated distribution data and highlight morphological features that distinguish the different species in the alliance. Furthermore, we review the circumscription of the most widespread species of the alliance, Waltheria brachypetala, and its related taxon, W. ferruginea, providing detailed descriptions and a brief nomenclatural history, as both species were traditionally treated as conspecific, and data on biogeography and ecology.

Taxonomic treatment
Waltheria ferruginea A. St-Hil. was described based on the collection Saint-Hilaire s.n., from Minas Gerais. He presented a diagnosis with a complete description of the species and a detailed illustration. Thirty-three years later, Waltheria brachypetala Turcz. was published based on the collection Blanchet 2744 from the state of Bahia (Turczaninow 1858). In the Flora Brasiliensis, Schumann (1886) proposed to synonymize the latter name under W. ferruginea, as he believed they were conspecific due to the lack of characters supporting their distinction.
Distribution and Habitat-Waltheria brachypetala is endemic to Brazil, where it is widely distributed in the Northeastern region (Alagoas, Bahia Ceará, Paraíba, Pernambuco, Piauí, Rio Grande do Norte, and possibly Sergipe, but without confirmed records), as well as in the state of Minas Gerais, in Southeastern Brazil. It occurs in open, dry habitats of the Caatinga, Cerrado and Atlantic Forest domains, in elevations between 30-718 m (Fig. 1).
We provide the first occurrence record in the state of Paraíba, as well as the first record in the Atlantic Forest domain.
Phenology-Waltheria brachypetala can be found with flowers and fruits throughout the year.
Conservation status-Due to its wide distribution range, Waltheria brachypetala is classified as Least Concern (LC) or Near Threatened (NT) according to our preliminary conservation assessment. This species occurs in protected areas in the states of Bahia (Raso da Catarina Ecological Station, Boqueirão da Onça National Park, Canudos Biological Station and Lagoa de Itaparica Environmental Protection Area), Ceará (Aiuaba Ecological Station, Serra das Almas Private Reserve of Natural Heritage and Ubajara National Park), and Pernambuco (Catimbau National Park), and in Grande Sertão Veredas National Park in the states of Bahia and Minas Gerais. Waltheria brachypetala also occurs on roadsides.
Distribution and habitat-Waltheria ferruginea is endemic to the state of Minas Gerais. It can be found in elevations between 700-948 m in the Cerrado, associated to campo rupestre vegetation, specifically in the Southern Espinhaço Range province (specifically in the Grão-Mogol and Diamantina Plateau districts), where several other endemic plant species are reported (Colli-Silva et al. 2019) (Fig. 1).
Phenology-Flowers can be found in February, March, August and November and fruits in March.
Conservation Status-According to our conservation assessment, Waltheria ferruginea is potentially classified as Endangered (EN) under the IUCN criterium B. This species is not found within protected areas and its Area of Occurrence is less than 500 km 2 .
Comments- Saunders (1995, unpublished) cites the herbarium P as the possible collection where the Waltheria ferruginea holotype is deposited; however, she did not verify or locate such material. We found two specimens of W. ferruginea labeled as Saint-Hilaire s.n. at P (barcodes P02273703 and P02273702), which warrants a lectotypification. We therefore chose the specimen P02273702 (barcode number) as the lectotype, as it possibly is the sample used for the illustration originally published by Saint-Hilaire. Morphological comments about distinctive characters between Waltheria ferruginea and W. brachypetala are discussed above and in Table 1.
It resembles Waltheria ferruginea by its stalked and multiradiate trichomes on branches and leaves and axillary inflorescences, but differs by its whitish to slightly yellowish trichomes (vs. ferrugineous), bracteoles usually 2-3-lobed to rarely entire apically (vs. always entire apically), and by the capsules chartaceous at apex and membranaceous below (vs. capsules chartaceous throughout).
Distribution and habitat-Waltheria biribiriensis is endemic to the state of Minas Gerais, growing on campo rupestre vegetation in the Cerrado, in elevations between 800-1200 m, in the Southern Espinhaço province (Diamantina Plateau district), a bioregion that concentrates a significant amount of endemic plant species (Colli-Silva et al. 2019) (Fig. 1).
Phenology-Flowering specimens are reported from December to May, with fruits in May.
Conservation status-According to the conservation assessment under IUCN criterium B, Waltheria biribiriensis is potentially Vulnerable (VU). Waltheria biribiriensis has not yet been recorded within protected areas and its Area of Occurrence is less than 500 km 2 .
Waltheria ferruginea and W. biribiriensis are both endemic to the campo rupestre vegetation in Minas Gerais, but the latter has a more restricted distribution (Fig.  1). Some populations of the two species are found in sympatry; however, they can be easily separated by the previously mentioned morphological characters (Tab. 1). Additionally, Waltheria biribiriensis is found in elevations up to 1200 m, while Waltheria ferruginea is restricted to elevations around 900 m.
Waltheria terminans resembles W. brachypetala by its shrubby lifeform and stalked multiradiate trichomes on the branches, but differs by having spirally arranged leaves (vs. distichally arranged), leaf blade with 7-8 pairs of secondary veins (vs. 14-17 pairs of secondary veins), and axillary inflorescences only in the terminal portion of the branches (vs. axillary along all the branch).
Distribution and habitat-Known only from the state of Minas Gerais, occurring in some municipalities and localities of campo rupestre vegetation in the Southern Espinhaço province (Diamantina Plateau district), in elevations between 1100-1300 m (Fig. 1).
Etymology-The specific epithet refers to the location of the inflorescences, which, in addition to being axillary, are always arranged in the terminal portions.
Phenology-Waltheria terminans is found with flowers between November and January to May and fruits in November.
Conservation status-According to our preliminary conservation assessment, Waltheria terminans, similarly to W. biribiriensis, is potentially Vulnerable (VU). Only one population of Waltheria terminans has been registered within a protected area, in Serra do Cabral State Park. Its Area of Occurrence is less than 500 km 2 .
Comments-Waltheria terminans was previously described by Saunders (1995, unpublished) as a new taxon but not effectively published. It can be distinguished from its relative species, W. brachypetala, by the spiral leaf arrangement (vs. distichous in W. brachypetala), petiole 0.2−0.3 cm long (vs. 0.6−1.1 cm long), leaf blade 1.6−2.6 cm long (vs. 4.3−9.5 cm long), inflorescences only in the terminal portions (vs. along the branches), oblanceolate to widely obovate bracteoles (vs. elliptic to widely elliptic) and petals rounded at the apex (vs. emarginate). Further morphological characters are summarized in Table 1.
Some populations of W. terminans are found in sympatry with W. biribiriensis and W. ferruginea, where they share the same lifeform; however, W. terminans can be easily distinguished by its leaves 1.6-2.6 cm long (vs. 3.4-13.0 cm long) and by other characters summarized in Table 1. Waltheria terminans reaches the highest elevations when compared to other species above, up to 1,300 m.