Diversification of African Tree Legumes in Miombo–Mopane Woodlands

plants Article Diversification of African Tree Legumes in Miombo–Mopane Woodlands Ivete Maquia 1,2,†, Silvia Catarino 1,3,†, Ana R. Pena 4, Denise R.A. Brito 2, Natasha. S. Ribeiro 5, Maria M. Romeiras 1,4 and Ana I. Ribeiro-Barros 1,6,* 1Linking Landscape, Environment, Agriculture and Food (LEAF), Instituto Superior de Agronomia (ISA), Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisbon, Portugal; [email protected] (I.M.); [email protected] (S.C.); [email protected] (M.M.R.) 2Biotechnology Center, Eduardo Mondlane University, Av. de Moçambique Km 1.5, Maputo 1109, Mozambique; [email protected] 3Forest Research Center (CEF), Instituto Superior de Agronomia (ISA), Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal 4Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisbon, Portugal; [email protected] 5Faculty of Agronomy and Forest Engineering, Eduardo Mondlane University, Campus1, P.O. Box 257, Maputo 1102, Mozambique; [email protected] 6Unidade de Geobiociências, Geoengenharias e Geotecnologias (GeoBioTec), Faculdade de Ciências e Tecnologia, Universidade NOVA de Lisboa, 2829-516 Monte de Caparica, Portugal *Correspondence: aribeir[email protected] †These authors contributed equally to this work. Received: 27 May 2019; Accepted: 18 June 2019; Published: 20 June 2019   Abstract: The southern African Miombo and Mopane ecoregions constitute a unique repository of plant diversity whose diversification and evolutionary history is still understudied. In this work, we assessed the diversity, distribution, and conservation status of Miombo and Mopane tree legumes within the Zambezian phytoregion. Data were retrieved from several plant and gene databases and phylogenetic analyses were performed based on genetic barcodes. Seventy-eight species (74 from Miombo and 23 from Mopane, 19 common to both ecoregions) have been scored. Species diversity was high within both ecoregions, but information about the actual conservation status is scarce and available only for ca. 15% of the species. Results of phylogenetic analyses were consistent with current legume classification but did not allow us to draw any conclusion regarding the evolutionary history of Miombo and Mopane tree legumes. Future studies are proposed to dissect the diversity and structure of key species in order to consolidate the network of conservation areas. Keywords: diversity; Miombo; Mopane; tree legumes; Zambezian phytoregion 1. Introduction Tropical dry forests and woodlands constitute a large portion of the world’s vegetation, covering one-sixth of the earth’s surface and more than half of the African continent [ 1 , 2 ]. Among them, the Miombo–Mopane woodlands are the most predominant type of vegetation in Southern Africa, and together with Amazonia, Congo, New Guinea and the North American deserts, are considered wilderness areas of global conservation significance [ 3 ]. The woodlands play a crucial role in formal and informal economies, supporting the livelihoods of millions of rural and urban people, by providing important resources such as timber, food, medicines, biofertilizers, housing and energy [4–8] . The Miombo and Mopane woodlands also play an important role in the ecosystem dynamics, particularly with respect to biodiversity, water, carbon and energy balance [9–13]. Plants 2019,8, 182; doi:10.3390/plants8060182 www.mdpi.com/journal/plants Plants 2019,8, 182 2 of 19 The plant diversity of these ecosystems comprises a wealthy repository of biodiversity, with a high proportion of native species, which makes it biologically unique [ 14 , 15 ]. According to Olson et al. [ 16 ], five sub-regions have been delineated through the Miombo woodlands (i.e., Angolan Miombo woodlands, Central Zambezian Miombo woodlands, Zambezian Baikiaea woodlands, Eastern Miombo woodlands and Southern Miombo woodlands) that cover about 3,000,000 km 2 across the Zambezian region of Angola, Democratic Republic of Congo, Malawi, Mozambique, Tanzania, Zambia and Zimbabwe [ 17 , 18 ]. The Mopane woodlands represent the second most significant type of vegetation in the Zambezian phytoregion, covering approximately 600,000 km 2 . This region includes two sub-areas (i.e., Zambezian and Mopane woodlands, and Angolan Mopane woodlands), and is distributed over northern Namibia, southern Angola, Zimbabwe, Botswana, Zambia, Malawi, southern Mozambique and northern South Africa [17,19]. The Miombo and Mopane woodlands are dominated by species belonging to the Leguminosae [ 2 ], which is considered the second most economically important plant family [ 20 – 23 ]. This family includes over 19,500 species spanning about 770 genera and six subfamilies, namely Caesalpinioideae, Cercidoideae, Detarioideae, Dialioideae, Duparquetioideae and Papilionoideae, many of which establish root-nodule symbiosis with N 2 fixing rhizobia bacteria [ 23 ]. The Miombo woodlands are dominated by trees of the genera Brachystegia,Julbernardia and Isoberlinia, while the Mopane woodlands are dominated by Colosphosperum mopane (Benth.) Leonard [ 9 , 17 , 24 ]. Most of these trees are under severe ecological pressure, due to logging and charcoal production [ 25 , 26 ], as well as fires related to animal, human and climate factors [ 6 , 10 , 11 , 13 ], which have contributed to the massive degradation of these woodlands and raised the need for their conservation [4,24,27,28]. African forests are among the most understudied regions in the world with respect to phylogenetic diversity [ 29 ]. Characterization of a region’s phylogenetic diversity, which is based on the evolutionary relationships between species from a given geographical area, can be a powerful tool to analyze the phylogenetic structure of natural communities and can assist the study of processes governing the assembly of species in ecological communities [ 30 , 31 ]. The identification of areas with more or less phylogenetic diversity based on species richness is another important element for conservation studies [ 32 ]. Although the African woodlands remain of enormous evolutionary interest, assessing species diversification within Miombo and Mopane plant communities across West and East African woodlands is still understudied. Since the dominant plant lineages in Miombo and Mopane are tree legumes, this provides an excellent case study to understand the diversity and the evolutionary history of these two predominant types of vegetation in Southern Africa. In this context, the objectives of this study were: (i) to characterize the diversity and distribution of Miombo and Mopane tree legumes within the Zambezian phytoregion (Figure 1); (ii) to provide a unique view of their phylogenetic diversity and how these lineages have evolved across West and East African woodlands; and (iii) to provide new data to assist the implementation of conservation strategies and the sustainable management of the Mopane and Miombo woodlands. Plants 2019,8, 182 3 of 19 Plants 2019, 8, x FOR PEER REVIEW 3 of 18 Figure 1. Geographical distribution of the Miombo–Mopane woodlands in the Zambezian phytoregion. 2. Results 2.1. Tree Legumes Diversity and Conservation Status Our study categorized 78 Leguminosae trees, of which 74 were representative of the Miombo woodlands and 23 of the Mopane woodlands (19 species common to both habitats) (Table 1). Overall, the largest number of species was found in Zambia, with 71 out of the 78 species (91%), while the Democratic Republic of Congo (DRC) had the lowest number (51 species or 65%) (Table 1). Five of the six recognized subfamilies were found in the Miombo woodlands: Caesalpinioideae, the most frequent (27 species), followed by Papilionoideae (22 species), Detarioideae (21 species), and Cercidoideae and Dialioideae with only three and one species, respectively. Among the 34 genera, Brachystegia and Acacia were the most diverse with 12 and 11 species, respectively. The number of species per country ranged from 50 in the DRC to 67 in Zambia. The Mopane woodlands harbored four subfamilies of legume trees, 14 species belonging to the Caesalpinioideae subfamily, followed by Papilionoideae with six species. Only two species from Detarioideae and one from Cercidoideae were retrieved. The number of genera was lower in Mopane than in Miombo (15 versus 34). The highest number of species was recorded in Zimbabwe (23) and the lowest in the DRC (11). Table 1. Leguminosae tree species from Miombo and Mopane ecosystems: main habitat, distribution in the Zambezian area, conservation status (International Union for Conservation of Nature - IUCN) and habit. Taxon Subfamily Habitat Distribution 1 Conser vation Status 2 Habit A O DR C Z M Z W T Z M W M Z Acacia arenaria Schinz Caesalpinioi deae Miombo and Mopane X X X NE Shrub or small tree 2–9 m Acacia erubescens Welw. ex Oliv. Caesalpinioi deae Miombo and Mopane X X X X X X X NE Shrub or tree 2–10 m Acacia galpinii Burtt Davy Caesalpinioi deae Miombo X X X X X X NE Large tree 8–36 m Figure 1. Geographical distribution of the Miombo–Mopane woodlands in the Zambezian phytoregion. 2. Results 2.1. Tree Legumes Diversity and Conservation Status Our study categorized 78 Leguminosae trees, of which 74 were representative of the Miombo woodlands and 23 of the Mopane woodlands (19 species common to both habitats) (Table 1). Overall, the largest number of species was found in Zambia, with 71 out of the 78 species (91%), while the Democratic Republic of Congo (DRC) had the lowest number (51 species or 65%) (Table 1). Five of the six recognized subfamilies were found in the Miombo woodlands: Caesalpinioideae, the most frequent (27 species), followed by Papilionoideae (22 species), Detarioideae (21 species), and Cercidoideae and Dialioideae with only three and one species, respectively. Among the 34 genera, Brachystegia and Acacia were the most diverse with 12 and 11 species, respectively. The number of species per country ranged from 50 in the DRC to 67 in Zambia. The Mopane woodlands harbored four subfamilies of legume trees, 14 species belonging to the Caesalpinioideae subfamily, followed by Papilionoideae with six species. Only two species from Detarioideae and one from Cercidoideae were retrieved. The number of genera was lower in Mopane than in Miombo (15 versus 34). The highest number of species was recorded in Zimbabwe (23) and the lowest in the DRC (11). Plants 2019,8, 182 4 of 19 Table 1. Leguminosae tree species from Miombo and Mopane ecosystems: main habitat, distribution in the Zambezian area, conservation status (International Union for Conservation of Nature - IUCN) and habit. Taxon Subfamily Habitat Distribution 1Conservation Status 2Habit AO DRC ZM ZW TZ MW MZ Acacia arenaria Schinz Caesalpinioideae Miombo and Mopane X X X NE Shrub or small tree 2–9 m Acacia erubescens Welw. ex Oliv. Caesalpinioideae Miombo and Mopane X X X X X X X NE Shrub or tree 2–10 m Acacia galpinii Burtt Davy Caesalpinioideae Miombo X X X X X X NE Large tree 8–36 m Acacia gerrardii Benth. Caesalpinioideae Miombo and Mopane X X X X X X NE Shrub or tree 5–15 m Acacia hebeclada DC. Caesalpinioideae Mopane X X X NE Shrub or small tree to 3 m Acacia kirkii Oliv. Caesalpinioideae Mopane X X X X X X X NE Tree 2.5–18 m Acacia mellifera (Vahl) Benth. Caesalpinioideae Miombo and Mopane X X X X X NE Tree 4–9 Acacia nigrescens Oliv. Caesalpinioideae Miombo and Mopane X X X X X X NE Tree 4–30 m Acacia nilotica (L.) Willd. ex Delile Caesalpinioideae Miombo and Mopane X X X X X X LC Tree 3–15 m Acacia polyacantha Caesalpinioideae Miombo X X X X X X X NE Large tree 3.5–20 m Acacia robusta Burch. Caesalpinioideae Miombo X X X X NE Tree 5-30 m Acacia sieberiana DC. Caesalpinioideae Miombo X X X X X X X NE Tree 3–25 m Acacia welwitschii Oliv. Caesalpinioideae Miombo X X X NE Large tree 3–20 m Afzelia quanzensis Welw. Detarioideae Miombo X X X X X X X NE Shrub or tree 1.5–35 m Albizia adianthifolia (Schum.) W.Wight Caesalpinioideae Miombo X X X X X X X NE Tree 2.5–40 m Albizia anthelmintica Brongn. Caesalpinioideae Miombo X X X X X X NE Shrub or tree 2–12 m Albizia antunesiana Harms Caesalpinioideae Miombo X X X X X X X NE Tree 6–18 m Albizia glaberrima (Schum. & Thonn.) Benth. Caesalpinioideae Miombo X X X X X X X NE Shrub or tree 9–25 m Albizia harveyi E.Fourn. Caesalpinioideae Miombo X X X X X X X NE Tree 1.5–20 m Albizia versicolor Oliv. Caesalpinioideae Miombo X X X X X X X NE Tree 3–20 m Amblygonocarpus andongensis (Oliv.) Exell & Torre Caesalpinioideae Miombo X X X X X X X NE Tree 6–25 m Baikiaea plurijuga Harms Detarioideae Miombo and Mopane X X X LR/NT Tree 6–25 m Baphia bequaertii De Wild. Papilionoideae Miombo X X X NE Shrub or tree 3–10 m Plants 2019,8, 182 5 of 19 Table 1. Cont. Taxon Subfamily Habitat Distribution 1Conservation Status 2Habit AO DRC ZM ZW TZ MW MZ Baphia massaiensis Taub. Papilionoideae Miombo X X X X X X X LC Shrub or tree to 8–10 m Bauhinia petersiana Bolle Cercidoideae Miombo X X X X X X X NE Shrub or tree 3–10 m Bauhinia thonningii Schum. Cercidoideae Miombo and Mopane X X X X X X NE Shrub or tree to 2–20 m Bauhinia tomentosa L. Cercidoideae Miombo X X X X X X X NE Shrub or tree 1–8 m Bobgunnia madagascariensis (Desv.) J.H.Kirkbr. & Wiersema Papilionoideae Miombo X X X X X X X NE Shrub or tree 2–15 m Brachystegia allenii Hutch. & Burtt Davy Detarioideae Miombo X X X X X X NE Tree 3–20 m Brachystegia bakeriana Burtt Davy & Hutch. Detarioideae Miombo X X X VU B1+2c Shrub or tree to 10 m Brachystegia boehmii Taub Detarioideae Miombo X X X X X X X NE Tree 2.5–25 m Brachystegia floribunda Benth. Detarioideae Miombo X X X X X X NE Tree 4–15 m Brachystegia gossweileri Burtt Davy & Hutch. Detarioideae Miombo X X X NE Tree 6–24 m Brachystegia longifolia Benth. Detarioideae Miombo X X X X X X NE Tree 2–30 m Brachystegia puberula Burtt Davy & Hutch. Detarioideae Miombo X X X LC Tree 6–12 m Brachystegia spiciformis Benth Detarioideae Miombo X X X X X X X NE Tree 5–40 m Brachystegia tamarindoides Benth. Detarioideae Miombo X X X X X NE Tree 4–30 m Brachystegia taxifolia Harms Detarioideae Miombo X X X X NE Shrub or tree 2–16 m Brachystegia utilis Hutch. & Burtt Davy Detarioideae Miombo X X X X X X X NE Tree 6–20 m Brachystegia wangermeeana De Wild. Detarioideae Miombo X X X X X NE Tree 1.5–20 m Burkea africana Hook. Caesalpinioideae Miombo X X X X X X X NE Tree 4–20 m Cassia abbreviata Oliv. Caesalpinioideae Miombo and Mopane X X X X X X NE Shrub or tree 3–15 m Colophospermum mopane (Benth.) Leonard Detarioideae Mopane X X X X X NE Tree 4–18 m tall Cordyla africana Lour. Papilionoideae Miombo X X X X X NE Tree 9–40 m Plants 2019,8, 182 6 of 19 Table 1. Cont. Taxon Subfamily Habitat Distribution 1Conservation Status 2Habit AO DRC ZM ZW TZ MW MZ Craibia zimmermannii (Harms) Dunn Papilionoideae Miombo X X NE Tree 4–5 m Dalbergia arbutifolia Baker Papilionoideae Miombo X X X X X X NE Shrub or tree 3–18 m Dalbergia boehmii Taub. Papilionoideae Miombo X X X X X X X NE Shrub or tree 4.5–21 m Dalbergia melanoxylon Guill. & Perr. Papilionoideae Miombo and Mopane X X X X X X X LR/NT Spiny shrub or tree 1–30 m Dalbergia nitidula Baker Papilionoideae Miombo X X X X X X X NE Shrub or tree 2–12 m Dialium englerianum Henriq. Dialioideae Miombo X X X X NE Tree 6–23 m Dichrostachys cinerea (L.) Wight & Arn. Caesalpinioideae Miombo and Mopane X X X X X X X LC Shrub or tree 1–12 m Elephantorrhiza goetzei (Harms) Harms Caesalpinioideae Miombo X X X X X X X NE Shrub or tree 1–7 m Entada abyssinica Steud. ex A. Rich. Caesalpinioideae Miombo and Mopane X X X X X X X NE Tree 2.7–15 m Erythrophleum africanum (Benth.) Harms Caesalpinioideae Miombo and Mopane X X X X X X X NE Tree 4–18 m Faidherbia albida (Delile) A.Chev. Caesalpinioideae Miombo and Mopane X X X X X X X NE Tree 6–30 m Guibourtia coleosperma (Benth.) J. Léonard Detarioideae Miombo X X X X NE Tree 12–30 m Isoberlinia angolensis (Benth.) Hoyle & Brenan Detarioideae Miombo X X X X X NE Shrub or tree 1–20 m Isoberlinia scheffleri (Harms) Greenway Detarioideae Miombo X X VU B1+2b Tree 30–46 m Isoberlinia tomentosa (Harms) Craib & Stapf Detarioideae Miombo X X X X X NE Tree 3–18 m Julbernardia globiflora (Benth.) Troupin Detarioideae Miombo X X X X X X X NE Tree 5–15 m Julbernardia paniculata (Benth.) Troupin Detarioideae Miombo X X X X X X X NE Tree 2–20 m Millettia stuhlmannii Taub. Papilionoideae Miombo X X X NE Tree 6–25 m Millettia usaramensis Taub. Papilionoideae Miombo X X X X NE Shrub or tree 2–10 m Plants 2019,8, 182 7 of 19 Table 1. Cont. Taxon Subfamily Habitat Distribution 1Conservation Status 2Habit AO DRC ZM ZW TZ MW MZ Mundulea sericea (Willd.) A. Chev. Papilionoideae Miombo X X X X X X NE Large shrub or tree 1–8 m Ormocarpum trichocarpum (Taub.) Engl. Papilionoideae Miombo and Mopane X X X X NE Shrub or small tree 1–6 m Peltophorum africanum Sond. Caesalpinioideae Miombo and Mopane X X X X X X NE Tree 3–12 m Pericopsis angolensis (Baker) Meeuwen Papilionoideae Miombo X X X X X X X NE Tree 3–20 m Philenoptera bussei (Harms) Shrire Papilionoideae Miombo X X X X X NE Tree 3–15 m Philenoptera nelsii (Schinz) Schrire Papilionoideae Mopane X X X NE Shrub or tree 4–12 m Philenoptera violacea (Klotze) Shrire Papilionoideae Miombo X X X X X X X NE Tree 4.5–27 m Pterocarpus angolensis DC. Papilionoideae Miombo X X X X X X X LR/NT Tree 5–30 m Pterocarpus brenanii Barbosa & Torre Papilionoideae Miombo X X X X X X X LC Tree 4–12 m Pterocarpus lucens Guill. & Perr. Papilionoideae Miombo and Mopane X X X X X LC Tree 7.5–18 m Pterocarpus rotundifolius (Sond.) Druce Papilionoideae Miombo and Mopane X X X X X X X NE Tree 3–25 m Senna petersiana (Bolle) Lock Caesalpinioideae Miombo X X X X X X NE Shrub or small tree 2–6 m *Tamarindus indica L. Detarioideae Miombo X X X X X X X LC Tree to 25 m Xanthocercis zambesiaca (Baker) Dumaz-le-Grand Papilionoideae Miombo X X X X NE Tree 7–30 m Xeroderris stuhlmannii (Taub.) Mendonça & E.P. Sousa Papilionoideae Miombo and Mopane X X X X X NE Tree up to 20 m Total numbers - Number of species (Miombo) - - 58 50 67 62 64 60 62 - - Number of species (Mopane) - - 19 11 21 23 17 18 17 - - Number of species (Miombo and/or Mopane) - - 62 51 71 66 65 62 64 - - * The origin of Tamarindus indica is uncertain and some sources (Africa Plant Database) suggest that it is native only in Madagascar. 1 Distribution: AO—Angola; DRC—Democratic Republic of Congo; ZM—Zambia; ZW—Zimbabwe; TZ—United Republic of Tanzania; MW—Malawi; MZ—Mozambique. 2 Conservation status according to IUCN Red List: LC—least concern; NT—near threatened; VU—vulnerable; NE—not evaluated. Plants 2019,8, 182 8 of 19 Information on the conservation status of the Miombo and Mopane trees is still scarce as most of the species (66 species or 85%) have not yet been assessed globally, according to the categories and criteria of the International Union for Conservation of Nature (IUCN) Red List (Table 1). Therefore, only 12 species could be evaluated, of which seven were classified with least concern (Acacia nilotica (L.) Willd. ex Delile; Baphia massaiensis Taub.; Brachystegia puberula Burtt Davy & Hutch.; Dichrostachys cinerea (L.) Wight & Arn.; Pterocarpus brenanii Barbosa & Torre; Pterocarpus lucens Guill. & Perr.; Tamarindus indica L.), three as near threatened (Dalbergia melanoxylon Guill. & Perr.; Pterocarpus angolensis DC.; Baikiaea plurijuga Harms), and two as vulnerable species (Isoberlinia scheffleri (Harms) Greenway; Brachystegia bakeriana Burtt Davy & Hutch) (Figure 2). Plants 2019, 8, x FOR PEER REVIEW 7 of 18 Xanthocercis zambesiaca (Baker) Dumaz-leGrand Papilionoide ae Miombo X X X X NE Tree 7– 30 m Xeroderris stuhlmannii (Taub.) Mendonça & E.P. Sousa Papilionoide ae Miombo and Mopane X X X X X NE Tree up to 20 m Total numbers - Number of species (Miombo) - - 58 50 67 62 64 60 62 - - Number of species (Mopane) - - 19 11 21 23 17 18 17 - - Number of species (Miombo and/or Mopane) - - 62 51 71 66 65 62 64 - - * The origin of Tamarindus indica is uncertain and some sources (Africa Plant Database) suggest that it is native only in Madagascar. 1 Distribution: AO—Angola; DRC—Democratic Republic of Congo; ZM—Zambia; ZW—Zimbabwe; TZ—United Republic of Tanzania; MW—Malawi; MZ— Mozambique. 2 Conservation status according to IUCN Red List: LC—least concern; NT—near threatened; VU—vulnerable; NE—not evaluated. Information on the conservation status of the Miombo and Mopane trees is still scarce as most of the species (66 species or 85%) have not yet been assessed globally, according to the categories and criteria of the International Union for Conservation of Nature (IUCN) Red List (Table 1). Therefore, only 12 species could be evaluated, of which seven were classified with least concern (Acacia nilotica (L.) Willd. ex Delile; Baphia massaiensis Taub.; Brachystegia puberula Burtt Davy & Hutch.; Dichrostachys cinerea (L.) Wight & Arn.; Pterocarpus brenanii Barbosa & Torre; Pterocarpus lucens Guill. & Perr.; Tamarindus indica L.), three as near threatened (Dalbergia melanoxylon Guill. & Perr.; Pterocarpus angolensis DC.; Baikiaea plurijuga Harms), and two as vulnerable species (Isoberlinia scheffleri (Harms) Greenway; Brachystegia bakeriana Burtt Davy & Hutch) (Figure 2). Figure 2. Leguminosae species from Miombo and Mopane woodlands and their conservation status according to the IUCN Red List. (A) Baikiaea plurijuga occurs in Miombo and Mopane woodlands and is classified as near threatened; (B) Brachystegia bakeriana occurs in Miombo and is classified as vulnerable; (C) Dichrostachys cinerea occurs in both ecoregions and is classified as least concern; (D) Pterocarpus angolensis occurs in Miombo woodlands and is classified as near threatened. Figure 2. Leguminosae species from Miombo and Mopane woodlands and their conservation status according to the IUCN Red List. ( A )Baikiaea plurijuga occurs in Miombo and Mopane woodlands and is classified as near threatened; ( B )Brachystegia bakeriana occurs in Miombo and is classified as vulnerable; ( C )Dichrostachys cinerea occurs in both ecoregions and is classified as least concern; ( D )Pterocarpus angolensis occurs in Miombo woodlands and is classified as near threatened. 2.2. Molecular Phylogenetic Analysis As DNA sequences were not available for all the selected taxa, the analyzed set was reduced to a total of 67 species from the original set of 78 (Table 2). A total of eight datasets were created: two for each single locus (internal transcribed spacer (ITS), matK and rbcL), and two combined (ITS +matK + rbcL). The ITS matrix had the lower number of taxa and haplotype diversity (n =38, Hd =0.9986), while rbcL had the highest of the three (n =53, Hd =1.0000), followed by matK (n =69, Hd =0.9987). The combined set of ITS+matK+rbcL had a total of 70 sequences, with a single shared haplotype ( Hd =0.9996 ). A summary of the processed molecular data of this study is available in Table S1 of the Supplementary Materials. Plants 2019,8, 182 9 of 19 Table 2. Leguminosae tree species from Miombo and Mopane ecosystems used in the phylogenetic analyses. GenBank accession numbers for the corresponding internal transcribed spacer (ITS) and cpDNA (rbcL and matK) sequences. Taxon Subfamily rbcL matK ITS Acacia arenaria Schinz Caesalpinioideae JX572181 JX517408 - Acacia erubescens Welw. ex Oliv. Caesalpinioideae JF265248 JF270605 JQ265878 Acacia galpinii Burtt Davy Caesalpinioideae JX572194 JX518092 JQ265866 Acacia gerrardii Benth. Caesalpinioideae JF265250 JF270607 JQ265879 Acacia hebeclada DC. Caesalpinioideae JX572199 JX517672 JQ265920 Acacia kirkii Oliv. Caesalpinioideae JX572204 JX517387 JQ265829 Acacia mellifera (Vahl) Benth. Caesalpinioideae JX572211 JX517310 - Acacia nigrescens Oliv. Caesalpinioideae EU213440 EU214210 KY688811 Acacia nilotica (L.) Willd. ex Delile Caesalpinioideae JF265255 JF270612 JX139101 Acacia polyacantha Caesalpinioideae - - JQ265902 Acacia robusta Burch. Caesalpinioideae JX572222 JX517547 - Acacia sieberiana DC. Caesalpinioideae JF265259 JX517353 JQ265854 Acacia welwitschii Oliv. Caesalpinioideae JX572234 JX518159 - Afzelia quanzensis Welw. Detarioideae JX572247 JX518045 KY306488 Albizia adianthifolia (Schum.) W.Wight Caesalpinioideae JQ025020 JQ024935 - Albizia anthelmintica Brongn. Caesalpinioideae JX572254 JX517977 - Albizia antunesiana Harms Caesalpinioideae - - - Albizia glaberrima (Schum. & Thonn.) Benth. Caesalpinioideae JX572256 JX518104 - Albizia harveyi E.Fourn. Caesalpinioideae JX572257 JX518176 - Albizia versicolor Oliv. Caesalpinioideae JX572260 AF274210 - Amblygonocarpus andongensis (Oliv.) Exell & Torre Caesalpinioideae JX572301 AF521812 - Baikiaea plurijuga Harms Detarioideae JX572322 JX517704 KY306501 Baphia bequaertii De Wild. Papilionoideae - - - Baphia massaiensis Taub. Papilionoideae JF265298 JF270652 - Bauhinia petersiana Bolle Cercidoideae JX572327 JX517937 - Bauhinia thonningii Schum. Cercidoideae KU568124 KT461985 - Bauhinia tomentosa L. Cercidoideae JX572328 JX517621 KX057838 Bobgunnia madagascariensis (Desv.) J.H.Kirkbr. & Wiersema Papilionoideae JX572335 AY386940 EF560800 Brachystegia allenii Hutch. & Burtt Davy Detarioideae KU568100 KX146320 - Brachystegia bakeriana Burtt Davy & Hutch. Detarioideae - - - Brachystegia boehmii Taub Detarioideae JX572347 EU361886 KY306513 Brachystegia floribunda Benth. Detarioideae KU568148 KX146363 KY306515 Brachystegia gossweileri Burtt Davy & Hutch. Detarioideae - - - Brachystegia longifolia Benth. Detarioideae KU568078 KX146300 AF513687 Brachystegia puberula Burtt Davy & Hutch. Detarioideae - - - Brachystegia spiciformis Benth Detarioideae - EU361888 KY306518 Brachystegia tamarindoides Benth. Detarioideae - - - Brachystegia taxifolia Harms Detarioideae - - - Brachystegia utilis Hutch. & Burtt Davy Detarioideae - - - Brachystegia wangermeeana De Wild. Detarioideae - - - Burkea africana Hook. Caesalpinioideae JQ025025 JQ024940 KX057840 Cassia abbreviata Oliv. Caesalpinioideae JX572384 JF270682 - Colophospermum mopane (Benth.) Leonard Detarioideae JF265343 JF270696 AY955788 Cordyla africana Lour. Papilionoideae JF265371 KP177913 - Craibia zimmermannii (Harms) Dunn Papilionoideae JX572478 JX518072 - Dalbergia arbutifolia Baker Papilionoideae JX572499 JX517956 AB828608 Plants 2019,8, 182 16 of 19 23. LPWG. A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 2017,66, 44–77. [CrossRef] 24. Jew, E.K.; Dougill, A.J.; Sallu, S.M.; O’Connell, J.; Benton, T.G. Miombo woodland under threat: Consequences for tree diversity and carbon storage. For. Ecol. Manag. 2016,361, 144–153. [CrossRef] 25. Graham, P.H.; Vance, C.P. Legumes: Importance and constraints to greater use. Plant Physiol. 2003 ,131, 872–877. [CrossRef] [PubMed] 26. Catarino, S.; Duarte, M.C.; Costa, E.; Carrero, P.G.; Romeiras, M.M. Conservation and sustainable use of the medicinal Leguminosae plants from Angola. PeerJ 2019,7, e6736. [CrossRef] [PubMed] 27. Chirwa, P.W.; Syampungani, S.; Geldenhuys, C.J. Managing southern African woodlands for biomass production: The potential challenges and opportunities. In Bioenergy from Wood; Seifert, T., Ed.; Springer: Dordrecht, The Netherlands, 2014; pp. 67–87. 28. Romeiras, M.M.; Figueira, R.; Duarte, M.C.; Beja, P.; Darbyshire, I. Documenting biogeographical patterns of African timber species using herbarium records: A conservation perspective based on native trees from Angola. PLoS ONE 2014,9, e103403. [CrossRef] [PubMed] 29. Zhou, Y.; Chen, S.; Hu, G.; Mwachala, G.; Yan, X.; Wang, Q. Species richness and phylogenetic diversity of seed plants across vegetation zones of Mount Kenya, East Africa. Ecol. Evol. 2018 ,8, 8930–8939. [CrossRef] [PubMed] 30. Hardy, O.J.; Senterre, B. Characterizing the phylogenetic structure of communities by an additive partitioning of phylogenetic diversity. J. Ecol. 2007,95, 493–506. [CrossRef] 31. Winter, M.; Devictor, V.; Schweiger, O. Phylogenetic diversity and nature conservation: Where are we? Trends Ecol. Evol. 2013,28, 199–204. [CrossRef] [PubMed] 32. Forest, F.; Grenyer, R.; Rouget, M.; Davies, T.J.; Cowling, R.M.; Faith, D.P.; Balmford, A.; Manning, J.C.; Proche¸s, S.; van der Bank, M.; et al. Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 2007,445, 757–760. [CrossRef] [PubMed] 33. Timberlake, J.; Chidumayo, E.; Sawadogo, L. Distribution and Characteristics of African Dry Forests and Woodlands. In The Dry Forests and Woodlands of Africa: Managing for Products and Services; Chidumayo, E.N., Gumbo, D., Eds.; Earthscan: London, UK, 2010; pp. 11–41. 34. Meerts, P. An annotated checklist to the trees and shrubs of the Upper Katanga (DR Congo). Phytotaxa 2016 , 258, 201–250. [CrossRef] 35. Scholes, R.J.; Archer, S.R. Tree-grass interactions in savannas. Annu. Rev. Ecol. Syst. 1997 ,28, 517–544. [CrossRef] 36. Ratnam, J.; Bond, W.J.; Fensham, R.J.; Hoffmann, W.A.; Archibald, S.; Lehmann, C.E.R.; Anderson, M.T.; Higgins, S.I.; Sankaran, M. When is a ‘forest’ a savanna, and why does it matter? Glob. Ecol. Biogeogr. 2011 , 20, 653–660. [CrossRef] 37. Daru, B.H.; Van der Bank, M.; Davies, T.J. Unravelling the evolutionary origins of biogeographic assemblages. Divers. Distrib. 2018,24, 313–324. [CrossRef] 38. White, F. The Vegetation of Africa; Unesco: Paris, France, 1983. 39. Gauthier, P.; Debussche, M.; Thompson, J.D. Regional priority setting for rare species based on a method combining three criteria. Biol. Conserv. 2010,143, 1501–1509. [CrossRef] 40. IUCN. Guidelines for Using the IUCN Red List Categories and Criteria, Version 13. Standards and Petitions Subcommittee. Available online: http://www.iucnredlist.org/documents/RedListGuidelines.pdf (accessed on 14 February 2019). 41. Romeiras, M.M.; Catarino, S.; Gomes, I.; Fernandes, C.; Costa, J.C.; Caujap é -Castells, J.; Duarte, M.C. IUCN Red List assessment of the Cape Verde endemic flora: Towards a global strategy for plant conservation in Macaronesia. Bot. J. Linn. Soc. 2016,180, 413–425. [CrossRef] 42. Isaac, N.J.; Redding, D.W.; Meredith, H.M.; Safi, K. Phylogenetically-Informed Priorities for Amphibian Conservation. PLoS ONE 2012,7, e43912. [CrossRef] 43. IUCN. The IUCN Red List of Threatened Species. Version 2017-3. Available online: http://www.iucnredlist.org (accessed on 3 June 2018). 44. Ribeiro-Barros, A.I.; Catarino, S.; Moura, I.; Ramalho, J.C.; Romeiras, M.M.; Ghodhbane-Gtari, F. Actinorhizal trees and shrubs from Africa: Distribution, conservation and uses. Antonie Leeuwenhoek 2019 ,112, 31–46. [CrossRef] [PubMed] 45. The Bonn Challenge. Available online: http://www.bonnchallenge.org (accessed on 19 June 2019). Plants 2019,8, 182 17 of 19 46. Chiteculo, V.; Surovy, P. Dynamic Patterns of Trees Species in Miombo Forest and Management Perspectives for Sustainable Production—Case Study in Huambo Province, Angola. Forests 2018,9, 321. [CrossRef] 47. Chiteculo, V.; Abdollahnejad, A.; Panagiotidis, D.; Surov ý , P.; Sharma, R. Defining Deforestation Patterns Using Satellite Images from 2000 and 2017: Assessment of Forest Management in Miombo Forests—A Case Study of Huambo Province in Angola. Sustainability 2019,11, 98. [CrossRef] 48. Mugasha, W.A.; Eid, T.; Bollandsås, O.M.; Mbwambo, L. Modelling diameter growth, mortality and recruitment of trees in miombo woodlands of Tanzania. South. For. A J. For. Sci. 2017,9, 51–64. [CrossRef] 49. Chidumayo, E.N. Management implications of tree growth patterns in miombo woodlands of Zambia. For. Ecol. Manag. 2019,436, 105–116. [CrossRef] 50. Vane-Wright, R.I.; Humphries, C.J.; Williams, P.H. What to protect?—Systematics and the agony of choice. Biol. Conserv. 1991,55, 235–254. [CrossRef] 51. Pollock, L.J.; Rosauer, D.F.; Thornhill, A.H.; Kujala, H.; Crisp, M.D.; Miller, J.T.; McCarthy, M.A. Phylogenetic diversity meets conservation policy: Small areas are key to preserving eucalypt lineages. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2015,370, 20140007. [CrossRef] 52. Mazel, F.; Pennell, M.W.; Cadotte, M.W.; Diaz, S.; Dalla Riva, G.V.; Grenyer, R.; Leprieur, F.; Mooers, A.O.; Mouillot, D.; Tucker, C.M.; et al. Prioritizing phylogenetic diversity captures functional diversity unreliably. Nat. Commun. 2018,9, 2888:1–2888:9. [CrossRef] 53. Kress, W.J.; Erickson, D.L.; Swenson, N.G.; Thompson, J.; Uriarte, M.; Zimmerman, J.K. Advances in the use of DNA barcodes to build a community phylogeny for tropical trees in a Puerto Rican forest dynamics plot. PLoS ONE 2010,5, e15409. [CrossRef] 54. Kang, Y.; Deng, Z.; Zang, R.; Long, W. DNA barcoding analysis and phylogenetic relationships of tree species in tropical cloud forests. Sci. Rep. 2017,7, 12564. [CrossRef] 55. Liu, J.; Liu, J.; Shan, Y.X.; Ge, X.J.; Burgess, K.S. The use of DNA barcodes to estimate phylogenetic diversity in forest communities of southern China. Ecol. Evol. 2019,9, 5372–5379. [CrossRef] [PubMed] 56. Krajewski, C. Phylogeny and Diversity. Science 1991,254, 918. [CrossRef] 57. Losos, J.B. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol. Lett. 2008,11, 995–1003. [CrossRef] [PubMed] 58. Srivastava, D.S.; Cadotte, M.W.; MacDonald, A.A.M.; Marushia, R.G.; Mirotchnick, N. Phylogenetic diversity and the functioning of ecosystems. Ecol. Lett. 2012,15, 637–648. [CrossRef] 59. Mouquet, N.; Devictor, V.; Meynard, C.N.; Munoz, F.; Bersier, L.F.; Chave, J.; Couteron, P.; Dalecky, A.; Fontaine, C.; Gravel, D.; et al. Ecophylogenetics: Advances and perspectives. Biol. Rev. 2012 ,87, 769–785. [CrossRef] 60. Linder, H.P.; De Klerk, H.M.; Born, J.; Burgess, N.D.; Fjeldså, J.; Rahbek, C. The partitioning of Africa: Statistically defined biogeographical regions in sub-Saharan Africa. J. Biogeogr. 2012 ,39, 1189–1205. [CrossRef] 61. World Wildlife Fund. Available online: https://www.worldwildlife.org/publications/terrestrial-ecoregionsof-the-world (accessed on 19 June 2019). 62. Figueiredo, E.; Smith, G. Plants of Angola/Plantas de Angola; South African National Biodiversity Institute (SANBI Publishing): Pretoria, South Africa, 2008. 63. African Plant Database. Available online: http://www.ville-ge.ch/musinfo/bd/cjb/africa/index.php (accessed on 19 June 2019). 64. Plants of the World Online. Available online: http://powo.science.kew.org (accessed on 19 June 2019). 65. Flora of Mozambique. Available online: http://www.mozambiqueflora.com (accessed on 19 June 2019). 66. Flora of Zambia. Available online: http://www.zambiaflora.com (accessed on 19 June 2019). 67. Flora of Malawi. Available online: http://www.malawiflora.com (accessed on 19 June 2019). 68. Flora of Zimbabwe. Available online: http://www.zimbabweflora.co.zw (accessed on 19 June 2019). 69. The Plant List. Available online: http://www.theplantlist.org (accessed on 19 June 2019). 70. Brenan, J.P.M. Flora Zambesiaca: Mozambique, Malawi, Zambia, Zimbabwe, Botswana. Volume Three: Part One; Crown Agents for Oversea Governments and Administration: London, UK, 1970. 71. Pope, G.V. Flora Zambesiaca: Mozambique, Malawi, Zambia, Zimbabwe, Botswana; Volume Three: Part Six; Royal Botanic Gardens: Kew, UK, 2000. 72. Pope, G.V.; PolHill, R.M. Flora Zambesiaca: Mozambique, Malawi, Zambia, Zimbabwe, Botswana; Volume Nine: Part Five; Royal Botanic Gardens: Kew, UK, 2001. Plants 2019,8, 182 18 of 19 73. Sanfilippo, M. Trinta Á rvores e Arbustos do Miombo Angolano. Guia de Campo para a Identificaç ã o; COSPE: Firenze, Italy, 2013. 74. Urso, V. Vinte Á rvores e Arbustos do Mopane Angolano. Guia de Campo para a Identificaç ã o; COSPE: Firenze, Italy, 2013. 75. Global Biodiversity Information Facility (GBIF). Available online: http://www.gbif.org (accessed on 19 June 2019). 76. CBOL Plant Working Group; Hollingsworth, P.M.; Forrest, L.L.; Spouge, J.L.; Hajibabaei, M.; Ratnasingham, S.; Fazekas, A.J. A DNA barcode for land plants. Proc. Natl. Acad. Sci. USA 2009 ,106, 12794–12797. [CrossRef] 77. De Vere, N.; Rich, T.C.; Trinder, S.A.; Long, C. DNA barcoding for plants. In Plant Genotyping Methods in Molecular Biology (Methods and Protocols); Batley, J., Ed.; Humana Press: New York, NY, USA, 2015; pp. 101–118. 78. Tripathi, A.M.; Tyagi, A.; Kumar, A.; Singh, A.; Singh, S.; Chaudhary, L.B.; Roy, S. The internal transcribed spacer (ITS) region and trnhH-psbA are suitable candidate loci for DNA barcoding of tropical tree species of India. PLoS ONE 2013,8, e57934. [CrossRef] 79. Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; Buxton, S.; Cooper, A.; Markowitz, S.; Duran, C. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012,28, 647–1649. [CrossRef] [PubMed] 80. Li, W.; Cowley, A.; Uludag, M.; Gur, T.; McWilliam, H.; Squizzato, S.; Park, Y.M.; Buso, N.; Lopez, R. The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Res. 2015 ,43, W580–W584. [CrossRef] [PubMed] 81. Katoh, K.; Rozewicki, J.; Yamada, K.D. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 2017, bbx108. [CrossRef] [PubMed] 82. Rozas, J.; Ferrer-Mata, A.; S á nchez-DelBarrio, J.C.; Guirao-Rico, S.; Librado, P.; Ramos-Onsins, S.E.; S á nchez-Gracia, A. DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. Mol. Biol. Evol. 2017,34, 3299–3302. [CrossRef] [PubMed] 83. Capella-Guti é rrez, S.; Silla-Mart í nez, J.M.; Gabald ó n, T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009,25, 1972–1973. [CrossRef] [PubMed] 84. S á nchez, R.; Serra, F.; T á rraga, J.; Medina, I.; Carbonell, J.; Pulido, L.; Mar í a, A.; Capella-Gut í errez, S.; Huerta-Cepas, J.; Gabald ó n, T.; et al. Phylemon 2.0: A suite of web-tools for molecular evolution, phylogenetics, phylogenomics and hypotheses testing. Nucleic Acids Res. 2011 ,39, W470–W474. [CrossRef] [PubMed] 85. Pina-Martins, F.; Paulo, O.S. Concatenator: Sequence data matrices handling made easy. Mol. Ecol. Resour. 2008,8, 1254–1255. [CrossRef] 86. Lanfear, R.; Calcott, B.; Ho, S.Y.; Guindon, S. PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 2012,29, 1695–1701. [CrossRef] 87. Lanfear, R.; Frandsen, P.B.; Wright, A.M.; Senfeld, T.; Calcott, B. PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses. Mol. Biol. Evol. 2017,34, 772–773. [CrossRef] 88. Guindon, S.; Dufayard, J.F.; Lefort, V.; Anisimova, M.; Hordijk, W.; Gascuel, O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010 ,59, 307–321. [CrossRef] 89. Soltis, D.E.; Soltis, P.S.; Chase, M.W.; Mort, M.E.; Albach, D.C.; Zanis, M.; Savolainen, V.; Hahn, W.H.; Hoot, S.B.; Fay, M.F.; et al. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot. J. Linn. Soc. 2000,133, 381–461. [CrossRef] 90. Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014,30, 1312–1313. [CrossRef] [PubMed] 91. Silvestro, D.; Michalak, I. RaxmlGUI: A graphical front-end for RAxML. Org. Divers. Evol. 2012 ,12, 335–337. [CrossRef] 92. Huelsenbeck, J.P.; Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001 ,17, 754–755. [CrossRef] [PubMed] 93. Rambaut, A.; Drummond, A.J. Tracer v1.6. Available online: http://tree.bio.ed.ac.uk/software/tracer/(accessed on 1 March 2019). Plants 2019,8, 182 19 of 19 94. Miller, M.A.; Pfeiffer, W.; Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the 2010 Gateway Computing Environments Workshop (GCE), New Orleans, LA, USA, 14 November 2010; pp. 1–8. 95. Rambaut, A. FigTree, a Graphical Viewer of Phylogenetic Trees. Institute of Evolutionary Biology University of Edinburgh. Available online: http://tree.bio.ed.ac.uk/software/figtree/(accessed on 1 March 2019). © 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).