Notes on Atriplex , Oxybasis and Dysphania ( Chenopodiaceae ) in West-Central Tropical Africa

The Chenopodiaceae is a large family within the order Caryo phyllales. It comprises ~ 1600 species and is divided into ~ 110 genera (Sukhorukov 2014, Hernández-Ledesma et al. 2015). It is mostly distributed in the arid regions of the World. The exact number of the family’s representatives in Africa is still unknown, but according to our investigations, the number of indigenous and alien species may reach at least 300, including the largest genera Caroxylon Thunb. (~ 60 spp.), Atriplex L. (40 spp.), Chenopodium L. s.str. (25 spp.), and Suaeda Forssk. (20 spp.). Only a few Chenopodiaceae species are found in West-Central Tropical Africa (Hauman 1951), in contrast to arid territories in the northern, eastern and southern parts of the continent with high taxonomic richness. The most common chenopodiaceous species distributed in West-Central Tropical Africa (Burundi, Central African Republic, Cameroon, D.R.Congo, Equatorial Guinea, Gabon, Republic of Congo, and Rwanda) is the American Dysphania ambrosioides (L.) Mosyakin & Clemants (Baker & Clarke 1909, Renier 1948, Hauman 1951, Cavaco 1963, Fernández-Casas 1994, Fernández-Casas & Morales-Valverde 1995), previously placed in the genus Chenopodium. Taxonomy of the indigenous representatives of the family in Africa is still insufficiently studied. In the past decade, taxonomic revisions were only prepared for the genera Sarcocornia A.J.Scott in Southern Africa (Steffen et al. 2009, 2010) and Atriplex in East Tropical Africa and the Mascarene Islands (Sukhorukov 2012, 2013). However, some genera, especially Atriplex and Dysphania (subfam. Chenopodio ideae), are difficult to diagnose and are often confused with other native or even alien taxa (Sukhorukov 2012). In the present article, the amendments to Chenopodiaceae in West-Central Tropical Africa concern both genera. A closer look at a single Atriplex species collected in D.R.Congo and previously identified as Atriplex hastata or ‘Atriplex sp.’ (Hauman 1951) revealed that it is a new species from Atriplex sect. Teutliopsis described in the present article. Additionally, we have discovered new, previously misidentified, specimens of Dys-


MATERIAL AND METHODS
Morphological characters were studied using the material available in the herbaria B, BM, BR, BRLU, E, G, K, LE, MHA, MW, P, and W.However, collections of Atriplex and Oxybasis from West-Central Tropical Africa were found in BR only, and the specimens of Dysphania congolana are present in BR, E, K and P. Standard herbarium techniques were used.The cross-sections of the fruits of Atriplex congolensis were made by hand and examined using a light microscope (Mikmed-1, Biolam).The images of the bract-like cover were prepared using Carl Zeiss Axiovision camera.Geographical areas follow Brummit (2001).

RESULTS AND DISCUSSION
In his revision of Chenopodiaceae in the former Belgian Congo, Hauman (1951) accepted two Atriplex taxa: 'Atriplex hastata L.' (now A. prostrata Boucher ex DC.) and 'Atriplex sp.' The former was found to be a record based on misidentification (2 below), and the latter proved to represent a new species (1 below).Chenopodium congolanum (now in Dysphania) seems to be more common than previously thought (3 below).

A new Atriplex species from West-Central Tropical Africa
A thorough revision of Atriplex specimens collected in West-Central Tropical Africa shows that they all have the same morphology, and that they distinctly differ from A. prostrata (A.hastata auct.non L.) and its relatives within Atriplex sect.Teutliopsis.This justifies the description of a new species, Atriplex congolensis.
The new species is the only representative of Atriplex sect.Teutliopsis in tropical Africa (see also Sukhorukov 2012).This section comprises at least 26 representatives (A.Sukhorukov, unpubl.res.) mainly distributed in temperate Eurasia and littoral zones of North America.According to the molecular results, it seems to be monophyletic except for A. oblongifolia Waldst.& Kit.(Kadereit et al. 2010).The most significant characters of this section are the annual life history, leaves with isolateral or bifacial anatomy, a C 3 photosynthetic pathway (Moser 1934, Winter 1981, Sukhorukov 2006), partially caducous leaf indumentum consisting of bladder hairs (Sukhorukov 2006), clusters comprising both male and female flowers (Kondorskaya 1984), herbaceous bract-like covers enclosing the fruit (Sukhorukov 2006), and an evident seed dimorphism (Iljin 1936, Sukhorukov 2006).Some members of Atriplex sect.Teutliopsis are widely distributed ruderal plants, e.g. A. patula, A. micrantha C.A.Mey., and A. prostrata (Welsh 2003, Schwarz 2003, Sukhorukov 2006, 2014).The majority of the representatives originate in the steppes and semi-deserts of Asia, with secondary distribution areas in the coastal zones of Europe and North America (Sukhorukov 2006).Several species of this section are found in Africa (A. chenopodioides, A. congolensis, A. davisii, A. nilotica, A. patula, A. prostrata, and A. verreauxii), and some of them have been misidentified for a long time (Sukhorukov 2010, present article).The majority of the African species occurs in Northern Africa, representing a Mediterranean extension of the Eurasian area of the section (Sukhorukov 2006).Exceptions are A. nilotica, an endemic of the Upper Nile valley (Sukhorukov 2010), and A. chenopodioides, restricted to Algeria, Morocco, and the southern part of Spain.Only two endemic species occur south of the Sahara: A. congolensis and A. verreauxii.The narrow endemic A. congolensis belongs to the montane element of the Katanga flora.The Afromontane character of parts of Katanga, especially on the high plateaus, is well known (Lisowski et al. 1971) though not frequently mentioned.The South African A. verreauxii obviously represents a further migration of the section southwards.In table 1 we present the differences in morphology and distribution pattern between all African species of Atriplex sect.Teutliopsis, along with taxonomic remarks.
Morphologically, A. congolensis is similar to A. nilotica from Egypt, but it differs in having leaf blades with slightly hastate (not clearly lobate or serrate-dentate) lobes, a less dense and interrupted inflorescence and a lower number (up to 6) of female flowers in each cluster.Annual, branched from the base, with the ascendant branches up to 70(-100) cm.Leaves semi-appressed to the stem, with petioles to 2 cm long, blades to 35 × 25 mm, green or grayish, thick, oblong, ovoid or almost rhombic, entire or serrulate or slightly hastate, upper leaves oblong and entire.Inflorescence leafy at base, branched, with slightly interrupted flower clusters consisting of both male and female (5-10) flowers; bract-like cover triangular or rhombictriangular, 2.5-7 mm, with two lobes; its segments connate to ¼, usually with large (to 2 mm long) 2-6 dorsal appendages (fig.2).Fruit one-seeded, seed either brown or black; pericarp of fruits with brown seed 15-30 µm thick, colourless, 1-3-layered, the outer layer of smooth cells intermixed with scattered spongy cells; pericarp of fruits with black seed 10-18 µm thick, 1(-2)-layered, composed of spongy cells; brown seeds 1.5-1.8× 1.8-2.0× 0.6-0.7 mm, flattened, seed-coat testa 10-12 µm thick, smooth in outline (at crosssections), outer cell walls of its cells without depositions of tannin-like substances (vertical stalactites); black or reddishblack seeds 1.3-1.5 × 1.3 × 0.4-0.5 mm, flattened or slightly convex, seed-coat testa 20-25 µm thick, smooth or wavy in outline, outer cell walls of its cells with vertical stalactites.The identification of the representatives of this section requires a combination of the morphological characters.The most important features for identification are noted in the column with the heading Taxonomic remarks.date], Van Den Branden 211 (BR, barcodes BR000004850080 & BR000004850097), cited as "Atriplex sp." in Hauman (1951).

Atriplex congolensis
Ecology and elevation -Saline soils at altitudes 1000-1500 m.Distribution -The species is currently known from southeastern D.R.Congo (Katanga province) only, in the locations situated close to each other and mapped as one dot (fig.3).New records are possible from ecologically similar areas in Zambia.
Conservation status -Atriplex congolensis is given a preliminary Red List status of Vulnerable [VU].The species is endemic to Katanga and known from four specimens representing three subpopulations.The extent of occurrence (EOO) of Atriplex congolensis cannot be estimated because all specimens were collected more than forty years ago (chenopods are often missed by the collectors) and do not represent records of presence.Its area of occupancy (AOO) is estimated to be between 4 to 12 km 2 (which falls within the limits for Critically Endangered or Endangered status under the criterion B2).The three subpopulations represent one to three locations (sensu IUCN 2014), which is the upper limit for Critically Endangered or Endangered status under the subcriterion 'a' of criterion B2.The species is known from saline soils at 1000-1500 m elevation with no current threat known, but its AOO is very restricted.Moreover, the known localities are situated in a region with high mining activity and increasing population pressure on the vegetation.Faucon et al. ( 2010) indicated that most endemic plants found in Katanga could be considered as threatened.We thus anticipate that this unpredictable degradation in the quality of its habitat could drive Atriplex congolensis to CR or EX in a very short time.For that reason, we assigned to Atriplex congolensis a preliminary status of VU D2.The specimen cited as 'A.hastata' by Hauman (1951) was studied in BR.This identification was previously considered ambiguous (Brenan 1954), and the specimen is actually Oxybasis chenopodioides (L.) S.Fuentes, Uotila & Borsch (≡ Chenopodium chenopodioides (L.) Aellen).This species is native and widely distributed in the northern deserts and steppes of temperate Asia.It is naturalized in Burundi (Reekmans 1980), Kenya and South Africa (Sukhorukov 2014), where it was probably introduced by migratory birds (Sukhorukov 2014).
A molecular phylogeny of Dysphania remains unavailable at present.However, here we postulate that D. congolana is not closely related to any American member of the genus due to a different set of the carpological characters shared between almost all American Dysphania species and contrasting with Old World species (Sukhorukov & Zhang 2013, Sukhorukov 2014).For instance, the presence of glandular hairs on the pericarp of Brazilian D. minuata (Aellen) Mosyakin & Clemants, previously considered as a close relative of D. congolana, may be the most valuable feature contradicting the placement of both taxa into Chenopodium section Margaritaria Brenan (Simón 1996).However, it should be pointed out that, compared to other African species of Dysphania, D. congolana appears to be a remarkable taxon with respect to its morphology (Brenan 1956, Friis & Gilbert 2000) and fruit structure (Sukhorukov 2014).

Figure 3 -
Figure 3 -Distribution of Atriplex congolensis (dot), a new record of Oxybasis chenopodioides in D.R.Congo (triangle) and all known records of Dysphania congolana (black asterisks based on the examined specimens; grey asterisk -an additional record from Ethiopia cited in Friis & Gilbert 2000).