Two new species of Marsdenia (Apocynaceae) from limestone outcrops in Brazil

Abstract: Limestone outcrops often harbour floras rich in threatened and narrowly endemic species. Still, these formations, usually associated with karst landscapes, remain floristically poorly known, and so are often neglected in conservation programmes. In Brazil, three species of Marsdenia (Apocynaceae) endemic to limestone outcrops are known: M. breviramosa, M. virgultorum and M. zehntneri. In this work, we describe and illustrate two new species of Marsdenia restricted to karst landscapes: M. calcaria from the state of Minas Gerais and M. phallica from the state of Goiás. We also include illustrations of M. zehntneri, the species morphologically most similar to the two new species, and in situ images of the species of Marsdenia from limestone formations in Brazil (except for M. virgultorum, which is known only from the type). A geographic distribution map and an identification key for the five species known from limestone formations are also provided. Citation: Espírito Santo F. S., Bitencourt C., Ribeiro P. L. & Rapini A. 2018: Two new species of Marsdenia (Apocynaceae) from limestone outcrops in Brazil. — Willdenowia 48: 109–116. doi: https://doi.org/10.3372/wi.48.48107 Version of record first published online on 5 April 2018 ahead of inclusion in April 2018 issue.


Introduction
Calcareous outcrops are formations of sedimentary rocks composed predominantly of calcium carbonate produced by marine organisms. After uplift, these carbonate formations are then carved by rainwater and rivers, forming karst landscapes, marked by deeply rugged terrain, often with steep columns and cliffs, deep crevices and fissures, usually associated with underground drains and caves (e.g. Vermeulen & Whitten 1999;Clements & al. 2006;De Waele & al. 2009). In these outcropping islands, the rock is either exposed or covered by shallow, poor, alkaline soils, and is situated in an environment subjected to high temperatures, intense solar incidence and strong water restriction. Plants in these landscapes tend to be specialized and tolerant of extreme conditions; on the other hand, they are uncompetitive and quite vulnerable to disturbances (Médail & Verlaque 1997). In addition, their populations are usually small and isolated; therefore, they are susceptible to local extinctions caused by stochastic events and have a lower recolonization capacity (Fischer & Stöcklin 1997).
Calcareous formations harbour a high diversity of plants, especially in terms of rare and endemic species, as well as vulnerable ones (Cowling & al. 1994;Xu 1995;Willis & al. 1996a, b;Bardot-Vaucoulon 1997;Médail & Verlaque 1997;Vermeulen & Whitten 1999;Tuyet 2001;Zhu & al. 2003;Clements & al. 2006;Hart 2007;Zhang 110 Espírito Santo & al.: Two new species of Marsdenia from Brazil & al. 2017). This unique diversity is highly threatened by the cement and lime industry, the transformation of the vegetation cover, removal of wood in forested areas, tourism and climate change (Vermeulen & Whitten 1999;Clements & al. 2006;Day 2010a, b;Coelho & al. 2012;Melo & al. 2013). Human impacts on some karst landscapes have been severe and lasting (e.g. Day 2010a, b), but karst lands that are harder to access tend to be the habitat of the last remnants of natural vegetation in a region, even when close to cities; on the other hand, their flora remains poorly known and the lack of information causes its neglect in conservation programs (Vermeulen & Whitten 1999;Coelho & al. 2012).
Globally, carbonate karst is estimated to occur over approximately 10 -15 % of the land surface (Ford & Williams 2007). However, it can be commoner in particular regions; for instance, karst occurs on more than half of the Caribbean land area, and is mostly concentrated (90 %) in the Greater Antilles (Day 2010a, b). In contrast, carbonate areas cover probably less than 2 % of the South American land surface, and most of them are concentrated in Central Brazil, with a few areas scattered along the Andes (Auler 2004). In Brazil, the karst area corresponds to 5 -7 % of the country, totalling between 425 000 and 600 000 km 2 , most of which is from the Upper Proterozoic and Lower Cambrian, belonging to the Bambuí and Una groups, in the states of Minas Gerais, Bahia and Goiás, Central Brazil (Auler & Farrant 1996, in which see fig. 1 for the distribution of karst areas in Brazil).
Recently, a new species of Allamanda L. (A. calcicola Souza-Silva & Rapini, Apocynaceae), a genus widely used as an ornamental due to its large and abundant flowers, has been recognized, occurring exclusively in karst landscapes in the São Francisco Basin (Souza-Silva & Rapini 2009). In Serra do Ramalho, SW Bahia, along with A. calcicola, another new species of Apocynaceae was found, Marsdenia breviramosa Rapini & Fontella (Rapini & Fontella-Pereira 2011). Among the 40 species of Marsdenia in Brazil, only two others occur exclusively in limestone outcrops: M. virgultorum (E. Fourn.) Malme, described in the 19 th century (Fournier 1885) and known only from the type material, collected in Lagoa Santa, Minas Gerais, and M. zehntneri Fontella, which, although occurring in the states of Minas Gerais, Bahia and Goiás, was only described in the 1960s (Fontella-Pereira 1965).
During the preparation of the taxonomic treatment of Marsdenia (Apocynaceae: Asclepiadoideae: Marsdeni eae) from Brazil, two other new species, endemic to limestone outcrops and previously confused with M. zehnt neri, were recognized. They are described below as M. calca ria, from N Minas Gerais, and M. phallica, from Goiás. The five Marsdenia shrub species endemic to karst landscapes in Brazil can be readily separated based on the key below. However, the morphological similarity between them suggests a phylogenetic proximity, and this complex of species in Marsdenia could be an excellent group for biogeographic investigations in limestone outcrops.

Phenology -Collected with flowers in November and with fruits in May.
Distribution and ecology -Marsdenia calcaria is known exclusively from a limestone outcrop, growing directly on rocks, in Engenheiro Dolabela, state of Minas Gerais, Brazil (Fig. 3), in remnants of deciduous forest, where individuals of Myracrodruon urundeuva Allemão (Anarcardiaceae) and Encholirium sp. (Bromeliaceae) are common.
Conservation status -The species is known only from the type locality, situated about 100 m from a minor road, 800 m from the BR-131 highway and 1.2 km from the village. The surroundings were changed by agricultural and livestock activities, causing the population of Marsdenia calcaria to become even more isolated. Two other similar calcareous outcrops look suitable to this species, one 270 m and other 1.1 km to the north; together, they form a strip smaller than 0.5 km 2 . Found in a single locality, with a small area of occurrence and occupation, under strong anthropogenic pressure, this species should be considered Critically Endangered, CR B1ab(iii)+2ab(iii), according to IUCN (2016) criteria.

Remarks
Phenology -Collected with flowers from October to December and with fruits in March, April, July and August. Distribution and ecology -Found in deciduous seasonal forests, on limestone outcrops, exclusively in the state of Goiás (Fig. 3).
Conservation Status -Among the areas of occurrence of Marsdenia phallica, only the environmental conditions of the type locality are known. It is situated on a roadside, in an area whose vegetative matrix has been replaced by pasture areas. However, estimates of the extent of occurrence (3780 km²) and area of occupancy (32 km²) indicate that M. phallica should be considered Endangered, EN B1ab(i,ii,iii)+2ab(i,ii,iii), according to IUCN (2016) criteria.
Etymology -The epithet of the species refers to the peculiar shape of the corona lobe, which resembles a phallus.
Remarks -Marsdenia phallica can be recognized by the shrubby, erect habit, lanceolate, narrowly elliptic or linear leaves, flowers with a shortly campanulate corolla, adaxially with a central vinaceous tinge at the basal portion of the lobes, pilose on the throat, and by the corona lobes usually formed by a laterally bulging lower portion and a narrowly lanceolate upper portion, acute and recurved at the apex.