Genet Resour Crop Evol (2020) 67:875–894

https://doi.org/10.1007/s10722-020-00886-8 (0123456789().,-volV)( 0123456789().,-volV)

RESEARCH ARTICLE

Diversity of grasses () in southern , with emphasis on the conservation of pasture genetic resources

M. Trytsman . F. L. Mu¨ller . A. E. van Wyk

Received: 12 June 2019 / Accepted: 16 January 2020 / Published online: 6 February 2020 Ó Springer Nature B.V. 2020

Abstract A renewed interest in the present state of and 685 species, inferring that only 20% of the world’s genebanks conserving pasture genetic resources grass genera and 6% of world’s grass species are found worldwide motivated this study to quantify the wealth in the study area with the most speciose of grass (Poaceae) diversity indigenous to southern subfamily. is the only tribe with large

Africa, here defined as South Africa, Lesotho and numbers of both C3 and C4 species and with several Eswatini (previously Swaziland). Botanical occur- species of high grazing value, therefore, was suggested rence records were extracted from BODATSA and as a priority lineage in the collection and conservation PHYTOBAS datasets to generate a list of grass species efforts of the South African National Forage Gene- indigenous to the study area. The phylogenetic bank. This genebank conserves at present 73 genera classification, growth form, photosynthetic pathway, and 162 indigenous grass species, i.e. 48% and 24% of grazing status, endemism and conservational status the total number of taxa respectively, denoting the attributes were added to the 43,889 species level current vulnerable status of grass genetic resources in records, sourced from published literature. Results southern Africa. A need to therefore collect and from the current study indicate that the subcontinent is conserve grass genetic resources is emphasised, with represented by eight subfamilies, 25 tribes, 151 genera greater focus on the conservation of seed of well- known pasture genera classified as endangered or possibly extinct (mainly Panicum L. and Secale L.). Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10722-020-00886-8) con- Keywords Endemism Á Eswatini Á Gramineae Á tains supplementary material, which is available to authorized Lesotho Á South Africa users.

M. Trytsman (&) Á F. L. Mu¨ller Agricultural Research Council-Animal Production Institute, Lynn East, PB X05, Pretoria 0039, South Africa Introduction e-mail: [email protected]

A. E. van Wyk Poaceae (Gramineae), the members of which are Department of and Soil Sciences, University of commonly referred to as grasses and bamboos, is Pretoria, Pretoria 0002, South Africa considered as probably the most valuable plant family to humankind (Bouchenak-Khelladi et al. 2010). The A. E. van Wyk National Herbarium, South African National Biodiversity family includes the economically important cereals, Institute, Pretoria 0001, South Africa 123 876 Genet Resour Crop Evol (2020) 67:875–894 sugar crops, reeds, bamboos, forages and lawn grasses The decline in the pasture breeding capacity in (Hodkinson 2018). The success of this family can be South Africa (Truter et al. 2015) has resulted in many attributed to, amongst others, its adaptability to most of these species not being characterised and evaluated ecosystems, including arctic regions and at high for their pasture potential. Therefore, due to the lack of elevations uninhabitable by flowering (Tzvelev information regarding their pasture potential these 1989), ecological dominance in many ecosystems, and species have not yet been included in breeding and high species richness (Linder et al. 2018). evaluation programs. These plant genetic resources The important role of the Poaceae in sustainable are, however, still important sources of genetic livestock production is well known, with several material that could, under future bioclimatic condi- genera housing important pasture species (Truter et al. tions become valuable resources for breeding of future 2015; Capstaff and Miller 2018). The exploration of pasture species adapted to specific agro-ecological the potential of southern African grasses for pastures conditions. As a result, these plant genetic resources began as early as the 1900s, with the past 50 years are maintained in perpetuity at the SA-NFG as a means described as a period where the function and value of to maintain the plant genetic diversity that could southern African grasses were studied by several potentially be beneficial under future bioclimatic pasture researchers (Truter et al. 2015). An important conditions. Maintaining and conserving these plant initiative towards the conservation of grass genetic genetic resources however, puts significant financial resources in southern Africa was a collection excur- pressure on the SA-NFG. Recently, Pengelly and sion specially arranged for this purpose, to the Kruger Maass (2019) and Maass and Pengelly (2019) called National Park in South Africa, during the early 1990s. for the prioritization of germplasm as well as to This ensured that selected ecotypes of important improve the efficiency in conserving current collec- pasture species such as pubescens Nees, tions of plant genetic resources housed at genebanks Cenchrus ciliaris L., gayana Kunth, Cynodon across the globe. This, in turn, is believed to reduce the dactylon (L.) Pers., Digitaria eriantha Steud., Era- financial burdens on genebanks, by shifting efforts to grostis curvula (Schrad.) Nees and Panicum maximum only priority species, and locally adapted varieties and Jacq. were conserved in the South African National ecotypes within important pasture species with known Forage Genebank (SA-NFG) (Kruger et al. 1993). agronomic potential (Pengelly and Maass 2019; Maass However, similar to trends in the international and Pengelly 2019). This will allow for the conserva- genebank community, especially those housing trop- tion of a larger genetic diversity within species with ical and sub-tropical plant genetic resources (Maass known agronomic potential, which, in turn, will and Pengelly 2019; Pengelly and Maass 2019), the benefit future breeding programs of these species. conservation of these plant genetic resources have An example of this can be found in domesticated been under threat for the last 20 years. Generally, the African grass species such as Sorghum bicolor (L.) funding to manage and maintain forage genebanks Moench and Pennisetum glaucum (L.) R.Br. that are around the globe is on the decrease, resulting in many currently maintained and conserved for at least two- important plant genetic resources potentially being thirds of their diversity of their wild relatives (Buckler lost (Maass and Pengelly 2019). In the case of the SA- et al. 2001). NFG, the plant genetic resources maintained at the Van Wyk (1995) emphasized that the recognition facility was mainly threatened by the lack of funding and interpretation of genetic variation in organisms is which resulted in unreliable storage and testing at the heart of and called on plant facilities, coupled with a decline in trained personnel taxonomists in Africa for the urgent naming of capable of maintaining and evaluating the valuable infraspecific units. A striking example that highlighted collection of plant genetic resources housed at the the importance of this appeal was the revision of facility. Also, the SA-NFG houses a large number and Agrostis eriantha Hack. var. planifolia Goossens & diversity of plant genetic resources, many of which Papendorf being reduced to synonymy under A. eri- currently are perceived to have minimal to no antha Hack. (Victor et al. 2012). A method to agronomic potential due to the lack of information prioritize taxonomic revision of South African plant regarding their pasture potential. These species were genera was developed by Victor et al. (2015) to reduce collected with future breeding in mind. the taxonomy-conservation disorder where indicators 123 Genet Resour Crop Evol (2020) 67:875–894 877 such as revision dates, insufficient data (including diversity of indigenous grasses at tribe and species taxonomic uncertainty) and endemism were proposed level. Linking attributes such as photosynthetic path- as indicators. Furthermore, a literature review done in way, growth form and grazing status with phyloge- the early 1990s showed that only a few key or netic classification could assist in distinguishing taxa important indigenous grass species had complete with pasture potential. To ensure a similar outcome as autecological studies with the exception of Themeda for the pasture potential appraisal of legumes (Legu- triandra Forssk., Eragrostis curvula and Digitaria minosae/Fabaceae) indigenous to South Africa, eriantha (Shackleton 1991). A need for a coordinated, Lesotho and Eswatini (previously Swaziland) (Tryts- systematic approach in basic ecological research of man et al. 2016, 2019), this paper takes stock of the grass species in different biomes was therefore wealth of indigenous grass genetic resources with suggested. added references to grass species currently used in The most recent taxonomic review of genera in pasture systems. This, in turn, will help with efforts to southern African grasses was within the temperate prioritise conservation of important grass genetic Helictotrichon Besser s.l. (Mashau et al. 2010) resources at the SA-NFG, in line with the call by where two new species were identified. Germishuizen Maass and Pengelly (2019) and Pengelly and Maass and Meyer (2003) recorded major name revisions (2019). within the genera Aristida L. [= Stipagrostis Nees], Danthonia DC [= Merxmuellera Conert; = Kar- roochloa Conert & Tu¨rpe; = Chaetobromus Methods Nees; = Centropodia Rchb.; = Dregeochloa Conert], Phragmites Adans. [= Tribolium Desv.] and Rhynch- The Botanical Database of Southern Africa (BOD- elytrum Nees [= Melinis P.Beauv.] whilst Pentaschis- ATSA) maintained by the South African National tis (Nees) Spach and Setaria P.Beauv. were revised at Biodiversity Institute’s (SANBI) and stored in the species level. However, Fish et al. (2015) indicated BRAHMS platform (Le Roux et al. 2017) was that the genera Agrostis L., Anthoxanthum L., Cym- accessed on 2017/03/24 to extract the occurrence bopogon Spreng., Cynodon Rich., Echinochloa records for Poaceae. The taxon and quarter degree grid P.Beauv. and Puccinellia Parl. are also in need of cell (QDGC) records were extracted and refined, i.e. revision. Remarkably, a new species of Enneapogon alien and naturalized species, species with no QDGC Desv. ex P.Beauv. was recently identified by Mashau reference, species present outside the study area, and Coetzee (2019) i.e. Enneapogon limpopoensis namely South Africa, Lesotho and Eswatini, hence- Mashau, being possibly endemic to South Africa and forth referred to as southern Africa [SA], invalid . botanical names, synonyms, as well as incomplete The classification system followed in earlier con- taxa were removed from the dataset. Genus and tributions on the identification of southern African species names were verified using Fish et al. (2015)to grasses (Gibbs Russell 1986; Ellis 1988; Gibbs Russell ensure that only species indigenous to SA were et al. 1990) differ greatly from the present-day system included and naturalized or species recorded from (Fish et al. 2015). Gibbs Russell et al. (1990) countries bordering the study area, were excluded. The recognised five subfamilies and 21 tribes whereas database does not reflect all herbarium records from Fish et al. (2015) recognized eight subfamilies and 24 southern Africa, but mainly those housed in the tribes. Hence, one of the aims of the present study is to National Herbarium (PRE) in Pretoria and some of provide fresh insights into southern African’s valuable its satellite herbaria, notably the KwaZulu-Natal grass genetic resources within a modern classification Herbarium (NH) in Durban and the Compton Herbar- framework. For the present study, the most recent ium (NBG) in Cape Town. Despite its inherent worldwide phylogenetic classification of Soreng et al. limitations, the meaningful results generated justify (2017) will be used for taxa found in the study area. the use of this database, the only one of its kind for the The identification manuals of southern African grasses study area (Trytsman et al. 2016). (Gibbs Russell et al. 1990; Fish et al. 2015) listed all In addition, the botanical survey records contained indigenous grasses and also described the photosyn- in the PHYTOBAS database were accessed and thetic pathway and growth form, highlighting the Poaceae records with GPS locations were extracted. 123 878 Genet Resour Crop Evol (2020) 67:875–894

Table 1 Botanical records of the Poaceae indigenous to South Africa, Lesotho and Eswatini contained in the Botanical Database of southern Africa (BODATSA; maintained by SANBI) and PHYTOBAS (South African National Vegetation Data Archive) datasets Database Date #QDGCs/GPS #Taxa #Records

BODATSA: Total (QDGCs) 2017/03/24 1803 740 40,865 BODATSA: Species level (QDGCs) 2017/04/05 1803 685 40,139 PHYTOBAS: Species level (GPS) 2018/09/18 3114 373 29,589 BODATSA & PHYTOBAS: Total (QDGCs) 2018/10/26 1811 765 47,652 BODATSA & PHYTOBAS: Species level (QDGCs) 2018/10/26 1803 678 43,889 QDGCs quarter degree grid cells, GPS records with global positioning system localities

PHYTOBAS is a National Vegetation Data Archive Table 2 The post-editing contribution of BODATSA and (2003–2009), designed and administered by the late PHYTOBAS datasets Dr Bobby Westfall. This database is currently inactive #QDGC % of Total and the proposal by Specht et al. (2018) that ecological BODATSA 1564 86.7 data should be curated, proposing online open access of historical data, is supported. Since PHYTOBAS PHYTOBAS 13 0.7 seldom contain infraspecific taxa, only species level BODATSA & PHYTOBAS merged 226 12.5 records were used for further analyses. Introduced Total 1803 100.0 grass species and incomplete taxon records were also removed. A summary of the extent of the two datasets following the editing and merging processes is shown in Table 1. With the exception of references made to pathway and growth form, were added to each record. grass pasture species conserved in the SA-NFG, no For the purpose of this study, growth forms indicated other information was sourced from this genebank as ‘‘climber’’, ‘‘decumbent’’ and ‘‘scrambler’’ were database. grouped under the term ‘‘trailing’’. The information The merging of the two datasets resulted in many for the various attributes was sourced from, amongst duplicated records within a QDGC. After duplicates others, Gibbs Russell et al. (1990), Germishuizen and were removed, the contributing number of QDGCs for Meyer (2003), Van Oudtshoorn (2012), Fish et al. the two datasets were determined and are shown in (2015) and SANBI (2017). The phylogenetic classi- Table 2. BODATSA contributed to 86.7% of the total fication of Soreng et al. (2017) was followed to dataset and PHYTOBAS 0.7%. Grass species listed by compile the evolutionary relationships of subfamilies Fish et al. (2015), but not recorded in either and tribes. The bioregions vegetation map of Ruther- BODATSA or PHYTOBAS, are documented and thus ford et al. (2006) was used as a base layer for the only species not represented in this study. There generating maps with ArcView GIS 3.2, ESRI Inc. were eight indigenous grass species not recorded in 2002. This vegetation map shows 35 bioregions where either BODATSA or PHYTOBAS and these are listed a bioregion is defined as a composite special terrestrial in Table 3. unit based on similar biotic (vegetation and floristic) The collection and/or survey intensity (expressed as and physical features (landscapes and rock types) and the number of grass species per QDGC collected as processes at the regional scale (Rutherford et al. 2006). herbarium specimens), henceforth referred to as The biomes map of southern Africa (Rutherford et al. collection intensity, was calculated and mapped. This 2006) and the Ko¨ppen-Geiger climate classification is also used as a reference map to ascertain the map of southern Africa (Beck et al. 2018) are Online presence or absence of grass species within QDGCs of Resources 1 and 2 respectively, to be used as reference the study area when e.g. distribution maps are maps. compared. The ‘Red List of South African Plants’ (SANBI The taxonomy (subfamily and tribe) and descrip- 2017), was consulted for data on the conservational tive attributes, specifically endemism, photosynthetic status of indigenous grass species. A list of grasses

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Table 3 List of Poaceae species indigenous to South Africa, Lesotho and Eswatini not recorded in the Botanical Database of southern Africa (BODATSA; maintained by SANBI) and PHYTOBAS (South African National Vegetation Data Archive) datasets Species Recorded in aCatabrosa drakensbergense (Hedberg & I.Hedberg) Soreng & Fish Lesotho aEllisochloa papposa (Nees) P.M.Peterson & N.P.Barker Eastern Cape Helictotrichon rogerellisii Mashau, Fish & A.E.van Wyk Western Cape Helictotrichon roggeveldense Mashau, Fish & A.E.van Wyk Northern Cape Melinis scabrida (K.Schum.) Hack. Limpopo Pentameris praecox (H.P.Linder) Galley & H.P.Linder KwaZulu-Natal Poa leptoclada Hochst. ex A.Rich. KwaZulu-Natal, Lesotho Tribolium pleuropogon (Stapf) Verboom & H.P.Linder Southern Cape aStatus: Vulnerable with categories ‘Rare’ (not exposed to any direct or Results and discussion potential threat), ‘Near Threatened’ (likely to become at risk of extinction), ‘Vulnerable’ (high risk of Collection intensity extinction), ‘Endangered’ (very high risk of extinc- tion) and ‘Critically Endangered’ (extremely high risk The collection intensity for indigenous grass species is of extinction) will be presented. The conservation shown in Fig. 1. Collection intensity records, as status, however, applies only to species within South presented here, are not linked to species diversity as Africa’s borders and is thus not a global assessment. the latter is determined by vegetation surveys of plant

Fig. 1 Collection intensities of Poaceae indigenous to South SANBI) and PHYTOBAS (South African National Vegetation Africa, Lesotho and Eswatini as recorded in the Botanical Data Archive) datasets mapped on the bioregions of Rutherford Database of southern Africa (BODATSA; maintained by et al. (2006)

123 880 Genet Resour Crop Evol (2020) 67:875–894 communities. For this study, BODATSA included Resource 1). Pooideae contains the largest number of records documented since 1802 and PHYTOBAS world species (3968 spp.) but Panicoideae the largest records from 2003 to 2009. number of species indigenous to SA (256 spp.). It is evident that the very high collection intensities Furthermore, only 20% of the world genera (151 ([ 151 spp./QDGC) were made in the Central genera) and 6% of world species (685 spp.) are found Bushveld bioregion (Rutherford et al. (2006) as shown in SA. Even though this is a low number of species, in Fig. 2). Moreover, collection efforts were high in many have proven economic forage value worldwide, the 2528CA QDGC (red square with [ 201 spp./ e.g. Anthephora pubescens, Chloris gayana, Digitaria QDGC), indicating a possible biased collection eriantha and Eragrostis curvula, highlighting the approach close to Pretoria, Gauteng. Collection possible wealth of genetic resources contained in intensities ranging from 51 to 150 spp./QDGC are especially the tribe Paniceae. recorded in the Central Bushveld-, Lowveld-, Indian As mentioned previously, the largest number of Ocean Coastal Belt- and the Fynbos bioregions. The grass species is contained in Panicoideae resulting lower intensities (\ 100 spp./QDGC) are relatively mainly from the high number of species in Paniceae well distributed over the study area, with no record- (150 spp.). Pentameris P.Beauv. is the largest genus ings, however, in some of the central parts of the arid with 75 species followed by Eragrostis Wolf with 65 region. When the SANBI’s grass herbarium collec- species (Table 6). Pentameris is found in more tions are compared to the legume collections (Tryts- temperate regions, i.e. mainly in the Cape Floristic man et al. 2011), it is evident that the former are larger Region (Barker 1993), whereas Eragrostis is found in (± 40 139 records) than the latter (± 27 618 records) tropical and subtropical regions (Truter et al. 2015) despite the larger number of indigenous legume (also refer to Online Resource 2 for tropical, subtrop- (± 1455 intraspecific taxa of which ± 12% are trees) ical and temperate regions of SA). The importance of versus grass species (± 685 species). the Panicoideae is highlighted by the fact that both Zea mays L. and Sorghum Moench are recognized species Phylogenetic classification within the . Table 6 denotes the genera currently conserved in Worldwide the Poaceae is here treated as containing the SA-NFG. This genebank conserves at present 73 12 subfamilies, 52 tribes, 768 genera and 11,506 genera and 162 indigenous grass species, i.e. 48% and species (Soreng et al. 2017). The statistics of the 24% of the total number of taxa respectively. The low grasses as a whole is compared with the indigenous number of grass species presently conserved is a grass diversity of SA in Table 4. Grasses, indigenous particular concern if the high risk of continued loss of to SA, consist of eight subfamilies, 25 tribes, 151 genetic material as described by Pengelly and Maass genera and 685 species. The basal lineage subfamilies (2018) is taken into account. However, the renewed Anomochlooideae, Pharoideae and Puelioideae are interest from South African policy makers in restoring not represented in SA. The subfamilies of the BOP this genebank as a centre of excellence is encouraging clade (Bambusoideae, Oryzoideae and Pooideae) are and strengthen the aim to improve the collection and all present in SA, but not Micrairoideae of the conservation efforts for potentially important indige- PACMAD clade. The PACMAD clade consist of nous grass species. subfamilies Panicoideae, Aristidoideae, Chlori- doideae, Micrairoideae, Arundinoideae and Dantho- Subfamily distribution nioideae. Differences in the formal classification of Poaceae as followed by Gibbs Russell et al. (1990) and The distribution patterns, i.e. the presence or absence Fish et al. (2015), compared to that of Soreng et al. of subfamilies in QDGCs of the study area, for the (2017), is outlined in Table 5. eight subfamilies represented in SA are shown in Bambusoideae has the poorest representation of Fig. 3. Aristidoideae, Panicoideae and species in SA (Table 4). Given that Bambusoideae is covers most of the bioregions with the latter having the only grass lineage to have diversified in forests more coverage in especially the central regions of (Sungkaew et al. 2009), this is expected with forests South Africa. The presence of Panicoideae is infre- being the smallest biome in the study area (Online quent in Namaqualand, Bushmanland and Karoo 123 Genet Resour Crop Evol (2020) 67:875–894 881

123 882 Genet Resour Crop Evol (2020) 67:875–894 b Fig. 2 Bioregions of South Africa, Lesotho and Swaziland Growth form (Rutherford et al. 2006) to be used as reference map The majority of grass species in SA are described as tufted (401 spp.) followed by rhizomatous/tufted (105 regions (refer to Fig. 2) and Aristidoideae has a low spp.) and rhizomatous (59 spp.) (Fig. 4). Linder et al. presence in the central parts of the arid regions. (2018) states that the tufted growth form, stemming According to Fish et al. (2015), Panicoideae occurs in from tillering, probably evolved within Poaceae. This more mesic habitats whereas Chloridoideae occurs in growth form was found, however, to be less tolerant to drier saline habitats. heavy grazing compared to rhizomatous or stolonif- erous grasses by Reynolds (1995). The tufted growth Figure 3 further shows that Oryzoideae and Pooi- form is nonetheless an attribute of the majority of grass deae have similar distribution patterns, covering the pasture species, particularly those mentioned earlier as Cape Floristic Region, Succulent Karoo and a large key pasture species. Rhizomes (underground stems) part of the Grassland biome (Online Resource 1). are also a valuable survival trait, in not only protecting Bambusoideae occurs only in the Drakensberg Grass- the plant from trampling (Rechenthin 1956) or being land bioregion whereas Arundinoideae occurs mostly correlated with drought resistance (Zhou et al. 2014) in Central Bushveld, Lowveld and Indian Ocean but also having a regenerative ability (Zwerts et al. Coastal Belt bioregions (refer to Fig. 2). The high 2015). Da Silva et al. (2015) argues that complemen- presence of Arundinoideae in the winter rainfall zone tary growth habits of C tropical grasses, i.e. rhizoma- described by Gibbs Russell (1986) has been invali- 4 tous grasses that occupy a lower horizontal stratum dated since the addition of the Oryzoideae and and tufted grasses a higher vertical stratum, result in Danthonioideae resulted in the removal of Ehrharta coexistence and allows for greater grass diversity. Thunb. and Pentameris from Arundinoideae. Lastly, Little information on the hemicryptophyte growth Danthonioideae is found in the Cape Floristic Region, form (buds present at or near the soil surface) exists for Succulent Karroo biome (Online Resource 1) and the these indigenous species, although it is accepted that it Drakensberg Grassland bioregion.

Table 4 Statistics of tribes, genera and species of Poaceae indigenous to South Africa, Lesotho and Eswatini (SA) compared to the world Sourced from Fish et al. (2015) and Soreng et al. (2017) Subfamily Tribe World Tribe SA Genera World Genera SA Species World Species SA

Anomochlooideae 2 – 2 – 4 – Pharoideae 1 – 3 – 12 – Puelioideae 2 – 2 – 11 –

BOP clade Oryzoideae 4 2 19 4 115 28 Bambusoideae 3 2 125 2 1670 2 Pooideae 15 6 202 18 3968 58

PACMAD clade Aristidoideae 1 1 3 3 367 42 Panicoideae 13 6 247 65 3241 256 Arundinoideae 2 2 14 4 40 6 Micrairoideae 3 – 8 – 184 – Danthonioideae 1 1 19 10 292 114 Chloridoideae 5 5 124 45 1602 179 Total 52 25 768 151 11,506 685

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Table 5 Comparison of the classification of Poaceae indigenous to South Africa, Lesotho and Eswatini followed by Gibbs Russell et al. (1990) and Fish et al. (2015) compared to that of Soreng et al. (2017) aGibbs-Russell et al. (1990) bFish et al. (2015) aSoreng et al. (2017) Subfamily Tribe Subfamily Tribe Subfamily Tribe

Pooideae Triticeae Bambusoideae Bambuseae Oryzoideae Ehrharteae Brachypodieae Olyreae Oryzeae Bromeae Ehrhartoideae Ehrharteae Bambusoideae Arundinarieae Aveneae Oryzeae Bambuseae Meliceae Pooideae Brachypodieae Pooideae Meliceae Poeae Bromeae Stipeae Bambusoideae Oryzeae Meliceae Brachypodieae Olyreae Poeae Bromeae Centotheceae Stipeae Triticeae Ehrharteae Triticeae Poeae Bambuseae Aristidoideae Aristideae Aristidoideae Aristideae Arundinoideae Stipeae Arundinoideae Arundineae Panicoideae Tristachyideae Arundineae Danthonioideae Danthonieae Centotheceae Danthonieae Panicoideae Andropogoneae Paniceae Aristideae Arundinelleae Paspaleae Chloridoideae Pappophoreae Paniceae Arundinelleae Chlorideae Paspaleae Andropogoneae Panicoideae Paniceae Tristachyideae Arundinoideae Molinieae Arundinelleae Centotheceae Arundineae Andropogoneae Chloridoideae Centropodieae Danthonioideae Danthonieae Maydeae Chloridoideae Centropodieae Eragrostideae Triraphideae Triraphideae Eragrostideae Zoysieae Zoysieae Cynodonteae aTribes in phylogenetical order bTribes in alphabetical order is common in grasses (Linder et al. 2018). This trait Karoo, Grassland, Savanna and Indian Ocean Coastal can contribute to survival during unfavourable condi- Belt biomes and Oplismenus spp. in the Lowveld and tions such as seasonal drought, cold, fire or heavy Indian Ocean Coastal Belt bioregions (refer to Fig. 2 grazing when plants can regrow from the base after and Online Resource 1). A review on the concept of conditions improves (Linder et al. 2018). grazing lawns, i.e. a short-stature grassland commu- In general, most grass growth forms have a nity type, persisting and spreading under heavy relatively wide distribution throughout the study area. grazing (Hempson et al. 2014) affirms that certain The exceptions are the cushion growth form (low ecotypes of Themeda triandra Forssk. and Digitaria growing, mat forming at high altitudes) of the genus eriantha forms small cushion-like plants and dense Pentameris (eight of the 75 spp.), the trailing form of stoloniferous or rhizomatous clonal mats under fre- especially eight Panicum L. spp. and the three trailing quent grazing. This finding strengthens the call of Van Oplismenus P.Beauv. spp. Pentameris is found mainly Wyk (1995) to formally label infraspecific genetic in the Fynbos biome, Panicum spp. in the Nama-

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Table 6 Subfamilies, tribes and genera (number of species in phylogenetic classification of Soreng et al. (2017) for subfam- brackets sourced from Fish et al. (2015)) of Poaceae indige- ilies and tribes. Taxa in bold indicate the largest (most nous to South Africa, Lesotho and Eswatini following the speciose) group/s within the classification Subfamily Tribe Genera

BOP clade Oryzoideae Ehrharteae Ehrhartaab (23) Oryzeae Leersiab (2) Oryzab (2) Prosphytochloaa (1) Bambusoideae Arundinarieae Thamnocalamusa (1) Bambuseae Oxytenanthera (1) Pooideaei Meliceae Melicaa (2) Streblochaete (1) Stipeae Stipaa (2) Brachypodieae Brachypodiuma (2) Bromeae Bromusa (4) Triticeae Hordeuma (1) Secalea (1) Poeae Agrostisa (9) Anthoxanthuma (4) Calamagrostis (1) Catabrosa (1) Festucaa (8) Holcusa (1) Helictotrichona (14) Koeleria (1) Poab (3) Polypogona (1) Puccinelliaa (2) PACMAD clade Aristidoideae Aristideae Aristidaab (23) Sartidia (2) Stipagrostisab (17) Panicoideae Tristachyideae Danthoniopsisb (5) Loudetiab (5) Trichopteryx (1) Tristachyab (3) Centotheceae Megastachya (1) Paniceaecef Acrocerasb (1) Alloteropsisb (2) Anthephoraab (3) Brachiariab (16) Cenchrusb (1) Digitariaab (25) Echinochloab (9) Entolasia (1) Eriochloab (4) Leucophrys (1) Megaloprotachneb (1) Melinisab (8) Odontelytrum (1) Oplismenus (3) Panicumab(34) Paspalidiumb (2) Pennisetum (7) Pseudechinolaena (1) Sacciolepis (6) Setariaab (12) Stenotaphrumb (2) Stereochlaena (1) Tarigidiaa (1) Tricholaenaab (2) Urochloab (6) Paspaleae Paspalumb (3) Arundinelleae (1) Andropogoneaeeg Andropogonb (14) Arthraxon (1) Bothriochloab (3) Chrysopogonb (1) Cleistachneb (1) Coelorachis (1) Cymbopogonab (6) Dichanthiumb (1) Diheteropogonb (2) Elionurusb (1) Elymandra (1) Eriochrysis (2) Eulalia (2) Hackelochloa (1) Hemarthriab (1) Heteropogonb (2) Hyparrheniab (20) Hypertheliab (1) Imperatab (1) Ischaemumb (2) Miscanthusb (2) Monocymbiumb (1) Oxyrhachis (1) Phacelurus (1) Rhytachne (2) Rottboellia (1) Schizachyriumb (6) Sehima (2) Sorghastrumab (2) Sorghumb (2) Themedab (1) Trachypogonb (1) Urelytrum (1) Arundinoideae Molinieae Elytrophorus (1) Phragmites (2) Styppeiochloa (1) Arundineae Dregeochloaa (2) Danthonioideae Danthonieae Capeochloaa (3) Chaetobromusab (1) Geochloaa (3) Merxmuelleraa (4) Pentamerisa (75) Pentaschistisa (3) Pseudopentamerisa (3) Schismusab (4) Tenaxiaa (5) Triboliuma (13) Chloridoideae Centropodieae Centropodiaab (1) Ellisochloa (1) Triraphideae Triraphisa (4) Eragrostideaedh Catalepis (1) Cladoraphisa (2) Diandrochloa (2) Enneapogonab (6) Eragrostisab (65) Fingerhuthiaab (2) Pogonarthriab (1) Schmidtiab (2) Stiburus (2) Tetrachneb (1) Zoysieae Spartina (1) Sporobolusab (34)

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Table 6 continued Subfamily Tribe Genera

Cynodonteaec Acrachneb (1) Bewsiab (1) Brachychloa (2) Chlorisb (6) Coelachyrum (1) Ctenium (1) Cynodonab (6) Dactylocteniumb (4) Dinebra (1) Eleusineb (2) Enteropogonb (2) Eustachysb (1) Harpochloa (1) Leptocarydion (1) Leptochloab (5) Lepturusb (1) Lintoniab (1) Lophacmea (1) Microchloab (2) Mosdeniaa (1) Odyssea (1) Oropetiumb (1) Perotis (1) Polevansia (1) Rendlia (1) Schoenefeldiab (1) Tetrapogonb (1) Tragusab (3) Trichoneurab (2) Tripogon (1) aInclude endemic species bGenera conserved in the South African National Forage Genebank Tribes with majority of species with cPioneer, dSubclimax, eClimax, fDecreaser, gIncreaser I, hIncreaser II iTemperate grass lineage

variants within especially species of potential eco- grasses (Gibson 2009) could in effect be an important nomic significance. grass collection objective, where the focus is on pasture development for temperate regions, especially Photosynthetic pathway and grazing status for dairy farming.

The distribution of C3 and C4 grass species is shown The photosynthetic pathway distinguished in the in Fig. 5. Species with the C3 pathway are widespread subfamilies and tribes of Poaceae is shown in Table 7. in the Fynbos, Succulent Karoo biomes and the The early-branching subfamilies (Oryzoideae, Bam- Drakensberg Grassland, Sub-Escarpment Grassland busoideae and Pooideae) are shown to have a C3 bioregions (refer to Fig. 2 and Online Resource 1). photosynthetic pathway, whereas the later-branched The central arid region has low occurrences of C3 Chloridoideae has a C4 photosynthetic pathway. grass species whereas the Kalahari Duneveld biore- Interestingly, Bouchenak-Khelladi et al. (2010) found gion has none. Species with a C4 photosynthetic molecular evidence that C4 photosynthesis (of at least pathway is found in all the bioregions of SA. Vogel the subfamily Chloridoideae) may well have origi- et al. (1978) investigated the geographical distribution nated in Africa. The majority of species of Aristi- of C3 and C4 grasses in southern Africa and concluded doideae and Panicoideae are C4 whereas all species of that low temperatures during seasonal growth favour Arundinoideae and Danthonioideae are C3. Tribes the C3 grasses in the regions mentioned above. The with well-known pasture species i.e. Andropogoneae, exclusive presence of C4 in the tropical region (Online Eragrostideae and Cynodonteae contains only C4 Resource 2) as described by Vogel et al. (1978) is, species whereas Paniceae have a mixture of C3 (i.e. however, not evident in Fig. 5.C3 species such as genus Panicum) and C4 species. The importance of C4 Agrostis L., Festuca L., Helictotrichon Besser (Poeae) grasses in pasture production could lie in their ability and Pentameris (Danthonieae) were recorded in the to transfer larger proportions of plant nitrogen to roots tropical regions of the study area (Online Resource 2). in infertile environments (Long 1999), as well as The only known grass species in SA with both a C3 and larger leaf area production in fertile and disturbed C4 subspecies, Alloteropsis semialata (R.Br.) Hitchc. environments. This supports Linder et al. (2018) need special mentioning (Ellis 1974; Gibbs Russell finding that grasses has the ability to colonize, persist 1983). Alloteropsis semialata (R.Br.) Hitchc. subsp. and transform environments, properties that are the eckloniana (Nees) Gibbs Russ. has a C3 photosyn- key to success. Furthermore, evidence presented by thetic pathway and A. semialata (R.Br.) Hitchc. subsp.

Linder et al. (2018) indicated that C4 plants have a semialata (R.Br.) Hitchc. a C4, suggesting an evolu- higher carbon fixing efficiency over a range of habitats tionary reversion from C4 to C3 (Ibrahim et al. 2009). when soil resources are limited compared to C3 types. Within Panicum, a genus containing important forage However, the higher forage value in terms of crude crops, Ellis (1988) distinguished 11 Panicum spp. protein content and digestibility in C3 compared to C4 having a C3 and 23 with C4 photosynthetic pathway. 123 886 Genet Resour Crop Evol (2020) 67:875–894

Fig. 3 The distribution patterns for Poaceae subfamilies indigenous to South Africa, Lesotho and Eswatini in phylogenetic order according to Soreng et al. (2017), mapped on the bioregions of Rutherford et al. (2006)

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450

400 401

350 s e i

c 300 e p s

s 250 s a r g

f 200 o r e b

m 150 u N 105 100 59 50 18 1… 13 12 8 8 6 6 6 4 3 3 3 3 3 2 1 1 0 Tufted Trailing Cushion Geophytic Hydrophyte Rhizomatous Stoloniferous Tufted/trailing Cushion/tufted Hydrophyte/tufted Hydrophyte/trailing Rhizomatous/tufted Stoloniferous/tufted Rhizomatous/woody Hydrophyte/rhizomatous Rhizomatous/stoloniferous Hydrophyte/rhizomatous/tufted Hydrophyte/stoloniferous/tufted Rhizomatous/stoloniferous/tufted Hydrophyte/rhizomatous/stoloniferous Hydrophyte/rhizomatous/stoloniferous/tufted

Fig. 4 Growth forms of Poaceae indigenous to South Africa, Lesotho and Eswatini. Sourced mainly from Gibbs Russell et al. (1990)

Pau et al. (2012) pointed out that the evolutionary Andropogoneae are well presented in all biomes but history of Poaceae is important for understanding the narrowly presented in the drier areas namely the

C3 and C4 functional diversity of grasses, as this will Nama-Karoo and Succulent Karoo biomes (Online affect their responses to global change. Resource 1). The ecological status as defined by A comparison of the recorded successional status of Forani et al. (1978) and Van Oudtshoorn (2012) tribes (Van Oudtshoorn 2012) shows that Paniceae and indicate that the high number of Decreaser species Cynodonteae contain the largest number of species present in Paniceae further underlines this tribe’s with pioneer status, whereas Paniceae and Andro- forage value, i.e. 47% of indigenous species with pogoneae contain the largest number with climax known preferential grazing status are grouped here status (Table 7). Pioneer species are usually annuals, (Table 7). Decreasers are defined as grasses abundant growing in disturbed habitats or unfavourable condi- in good veld and will decrease when over- or tions whereas climax species are perennials, growing undergrazed, whereas Increasers will increase under only when normal, optimal growth conditions prevail any type of mismanagement. Andropogoneae and (Van Oudtshoorn 2012). Panicoideae distinctly con- Eragrostideae contain respectively the highest number tains most climax species compared to other subfam- of Increaser I and Increaser II species. ilies and thus should be the focus for further assessing grass genetic resources with pasture potential, espe- cially within the tribes Paniceae and Andropogoneae. Grass species belonging to Paniceae and

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Table 7 The number of species within Poaceae subfamilies from Gibbs Russell et al. (1990) and successional and and tribes indigenous to South Africa, Lesotho and Eswatini ecological grazing status (Van Oudtshoorn 2012) using a C3 and/or C4 photosynthetic pathway sourced mainly

Subfamily Tribe C3 C4 Pioneer Subclimax Climax Decreaser Increaser Increaser Increaser I II III

BOP clade Oryzoideae Ehrharteae 23 2 1 2 Oryzeae 5 Bambusoideae Arundinarieae 1 Bambuseae 1 Pooideae Meliceae 3 1 1 Stipeae 2 Brachypodieae 2 Bromeae 4 1 Triticeae 2 Poeae 45 1 1 2 2 2

PACMAD clade Aristidoideae Aristideae 2 40 4 3 5 2 9 3 Panicoideae 14 2 1 Tristachyideae Centotheceae 1 Paniceae 23 127 13 3 25 21 7 16 Paspaleae 3 1 Arundinelleae 1 1 1 Andropogoneae 87 5 27 7 20 5 2 Arundinoideae Molinieae 4 1 Arundineae 2 Danthonioideae Danthonieae 114 1 3 3 1 2 2 Chloridoideae Centropodieae 2 1 Triraphideae 4 1 1 Eragrostideae 84 7 11 5 2 1 25 2 Zoysieae 35 2 3 2 1 1 6 1 Cynodonteae 54 10 3 6 5 2 14 1

Endemism and conservation concern Danthonioideae (found mainly in the Cape Floristic Region and Succulent Karoo biome (see Online Figure 6 shows the collection intensity for the 257 Resource 1) contributes to nearly half of the total grass species endemic to SA. The highest number of number of endemic grass species in SA. Pentameris endemic species per QDGC is recorded in the Cape accounts for 28% of endemic species followed by Floristic Region and in the Drakensberg Alpine Centre Ehrharta (9%), Eragrostis (7%) and Tribolium (5%). (Van Wyk and Smith 2001; Rutherford et al. 2006). In Pentameris is mainly found in the Fynbos biome and terms of the presence of endemic species in the study Drakensberg Grassland bioregion, Ehrharta in the area, the Upper and Lower Karoo, Bushmanland and Fynbos and Succulent Karoo biome, Eragrostis in Lowveld are the main bioregions (refer to Fig. 2) most parts of the study area and Tribolium in the containing the smallest number of endemic species. Fynbos and Succulent Karoo biome (Fish et al. 2015).

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are found respectively in the tropical region (Online Resource 2) and the Mopane bioregion of the study area. Secale strictum (J.Presl) J.Presl subsp. africanum (Stapf) K.Hammer, is a peren- nial wild rye found in Renosterveld of the western mountain Karoo (Fish et al. 2015) and within the Hantam-Roggeveld Centre (Van Wyk and Smith 2001). Helictotrichon quinquesetum (Steud.) Schweick., only known from the slopes of Table Mountain, Cape Town (Fish et al. 2015), is the only grass species listed as possibly extinct. It is evident from Table 8 that the majority of grass species with a conservational concern are found in the Cape Floristic Region, followed by the Hatam–Roggeveld Centre. Habitat loss is identified as the major threat to South African plants, i.e. infrastructure development, urban expansion, cultivation of crops, commercial afforesta- tion and mining (SANBI 2017). In terms of the conservation of genetic resources for possible future use, it is suggested that representative seed samples are collected from these species and stored in the SA- NFG. The screening and characterisation of these genetic resources will allow for re-introduction when certain populations go locally extinct. In addition, these efforts will allow these genetic resources to be included into breeding programs that can produce more adapted species or for rehabilitation of degraded

Fig. 5 The distribution of C3 and C4 photosynthetic pathways rangelands. in Poaceae indigenous to South Africa, Lesotho and Eswatini. Sourced mainly from Gibbs Russell et al. (1990) and mapped on the bioregions of Rutherford et al. (2006) Conclusion Pentameris and Tribolium are considered having a The important role that members of the Poaceae plays lower grazing value than Ehrharta (Van Oudtshoorn in sustainable pasture production systems compels the 2012). SA-NFG to conserve SA’s indigenous grass genetic The conservational assessment for grass species resources, not only those used in current pasture published in the Red List of South African Plants systems, but also genetic material that could be (SANBI 2017) is listed in Table 8 together with beneficial in future breeding programs and/or adapted regions or centres of endemism (sensu Van Wyk to specific agro-ecological conditions. A modern and Smith 2001). The genus Pentameris holds a classification framework was therefore used to docu- true conservational concern with 24 species listed, ment indigenous grass species, recorded in various present in all categories. There are two Panicum southern African taxonomic reviews and botanical spp. and one Secale L. sp., both important genera databases. Linking various attributes with phyloge- in pasture production also listed, respectively as netic classification and vegetation types assisted in rare and critically endangered. Panicum sancta- distinguishing taxa with pasture potential and to luciense and Panicum dewinteri, both perennials, prioritise future collection and conservation efforts.

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Fig. 6 The collection intensity for the endemic grass species present in South Africa, Lesotho and Eswatini. Sourced from Fish et al. (2015) and mapped on the bioregions of Rutherford et al. (2006)

Results showed that the inclusion of PHYTOBAS these arid regions, containing important pasture (South African National Vegetation Data Archive) species such as Chloris, Cynodon and Eragrostis, added valuable data since 13 additional QDGCs were should be considered. The majority of grass species in added to the dataset. Attention is drawn to the value of SA are tufted, an attribute of the majority of key grass historical vegetation data and the proposed call for pasture species. Tribes with well-known pasture online open access is supported. The collection species contains only C4 species (Andropogoneae, intensity map shows that the central Bushveld has Eragrostideae and Cynodonteae) whereas Paniceae high collections, but that in large parts of the central have a mixture of C3 and C4 species (i.e. genus arid region no collections were done. There are eight Panicum). Species with a C4 photosynthetic pathway subfamilies, 25 tribes, 151 genera and 685 species is found in all the bioregions of SA whereas C3 species present in SA. Subfamilies Anomochlooideae, Phar- have low occurrences in the central arid region. oideae, Puelioideae (basal lineage) and Micrairoideae Panicoideae contains more climax species compared (PACMAD clade) are not represented in SA. Only 6% to other subfamilies, especially within the tribes of world grass species (i.e. 685 spp.) are found in SA, Paniceae and Andropogoneae. The 257 endemic grass with Panicoideae having the largest number of species species found largely in the Cape Floristic Region and (256 spp.). Aristidoideae, Panicoideae and Chlori- in the Drakensberg Alpine Centre need an in depth doideae are represented in most of the bioregions assessment to determine the role the SA-NFG plays in whereas Bambusoideae is found only in one bioregion, their conservation as possible future pasture genetic namely the Drakensberg Grassland. The infrequent resources. This is an urgent outcome for the 24 species presence of Panicoideae in the western and central arid of Pentameris that holds a true conservational con- regions should be taken into account when focusing on cern. The collection of viable seed of two Panicum the collection of potentially drought tolerant grass spp. and one Secale sp., listed respectively as rare and species. Instead, the presence of Chloridoideae in critically endangered and the possible extinct Secale

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Table 8 Grass species and infraspecific taxa on the ‘Red List endemism (sensu Van Wyk and Smith 2001) the particular of South African Plants’ in order of the least to highest risk of taxon is endemic, or if more widespread, confined to in the extinction (SANBI 2017). The superscript following some study area names indicates to which specific local region or centre of Rare Vulnerable (continued)

Capeochloa setaceaCFR Elytrophorus globularis Dregeochloa calviniensis Helictotrichon barbatumSKR Panicum sancta-lucienseMC Helictotrichon namaquenseKBC Pentameris caulescensCFR Helictotrichon rogerellisiiCFR Pentameris clavataCFR Oryza longistaminata Pentameris glacialisCFR Pentameris calcicola var. hirsutaCFR Pentameris hirtiglumisCFR Pentameris longiglumis subsp. longiglumisCFR Pentameris holciformisCFR Pentameris longipesAC Pentameris horridaCFR Pentameris trifidaCFR Pentameris longiglumis subsp. gymnocoleaCFR Sartidia jucundaSBC Pentameris swartbergensisCFR Tribolium ciliareCFR Pentameris unifloraCFR Near threatened Endangered

Eulalia aurea Helictotrichon roggeveldenseHRC Oxyrhachis gracillimaPC* Pentameris bachmanniiCFR Panicum dewinteriSBC Pentameris dentataHRC Pentameris asperaCFR Pentameris eckloniiCFR Pentameris calcicola var. calcicolaCFR Pentameris pholiuroidesCFR Pentameris limaKBC Pentameris scandensCFR Stipagrostis geminifoliaGC

Vulnerable Critically endangered

Capeochloa cincta subsp. sericeaAC Pentameris barbata subsp. orientalisCFR Catabrosa drakensbergenseDAC Pentameris elegansCFR Ehrharta setacea subsp. unifloraCFR Pentameris ellisiiCFR Ellisochloa papposaCFR Secale strictum subsp. africanumHRC Tribolium pleuropogonCFR Helictotrichon quinquesetum (possibly extinct)CFR Rare, not exposed to any direct or potential threat; Near Threatened, likely to become at risk of extinction; Vulnerable, high risk of extinction; Endangered, very high risk of extinction; Critically Endangered, extremely high risk of extinction; AC, Albany Centre; CFR, Cape Floristic Region; DAC, Drakensberg Alpine Centre; GC, Gariep Centre; HRC, Hantam–Roggeveld Centre; KBC, Kamiesberg Centre; MC, Maputaland Centre; PC, Pondoland Centre; SBC, Soutpansberg Centre; SKR, Succulent Karoo Region *In the study area confined to the centre, but not endemic as it also occurs elsewhere in Africa/ strictum subsp. africanum is a critical undertaking for production, mitigate the possible effect of climate the SA-NFG. change on the valuable grass genetic resources, and consequently pasture production. It is proposed that a The SA-NFG conserve at present only a quarter of strategy be developed for the SA-NFG to collect and indigenous grass species with the current collection conserve seed of Paniceae since this tribe contains already facing serious risks. This will prompt decision valuable pasture grass species, thus focusing on makers to reinvest in the SA-NFG, focusing on speciose subtropical genera such as Anthephora, conserving genetic resources for improved animal Brachiaria, Digitaria, Panicum and Setaria. 123 892 Genet Resour Crop Evol (2020) 67:875–894

Furthermore, temperate genera containing important Compliance with ethical standards pasture species i.e. Bromus, Hordeum and Festuca as Conflict of interest The authors declare that they have no well as endemic species with grazing value, such as conflict of interest. Ehrharta, should also be the focus of seed collection efforts by the SA-NFG. The need for more emphasis on the description and formal recognition of infraspecific taxa, including ecotypes, are also high- References lighted. It is further proposed that stakeholders in biodiversity conservation strategize plant collections Barker NP (1993) A biosystematic study of Pentameris (Arun- excursions to those areas, previously not sampled. dineae, Poaceae). Bothalia 23:25–47 Beck HE, Zimmermann NE, McVicar TR, Vergopolan N, Berg A, Wood EF (2018) Present and future Ko¨ppen–Geiger The current systems of germplasm conservation at climate classification maps at 1-km resolution. Nature the SA-NFG is under revision. A long term storage 5:180214 facility is being prepared for purely conservation Bouchenak-Khelladi Y, Verboom GA, Savolainen V, Hodkin- purposes, while active collections of important pasture son TR (2010) Biogeography of the grasses (Poaceae): a phylogenetic approach to reveal evolutionary history in species as well as indigenous species with agronomic geographical space and geological time. Bot J potential will be made available for research purposes. 162:543–557 The reason for the long term storage of all grass Buckler ES, Thornsberry JM, Kresovich S (2001) Molecular genetic resources was brought about by the changes in diversity, structure and domestication of grasses. Genet Res 77:213–218 bioclimatic conditions predicted for southern Africa. Capstaff NM, Miller AJ (2018) Improving the yield and nutri- The conservation of these resources at the SA-NFG tional quality of forage crops. Front Plant Sci 9:535 could, under future bioclimatic conditions, result in Da Silva SC, Sbrissia AF, Pereira LET (2015) Ecophysiology of potential rehabilitation of degraded areas, or reintro- C4 forage grasses—understanding plant growth for opti- mising their use and management. Agriculture 5:598–625 ductions with better adapted ecotypes of the same Ellis RP (1974) The significance of the occurrence of both Kranz species after local extinction of naturally occurring and non-Kranz leaf anatomy in the grass species Al- populations. The indigenous grass database developed loteropsis semialata. S Afr J Sci 70:169–173 for this study will be used to establish biogeographical Ellis RP (1988) Leaf anatomy and systematics of Panicum (Poaceae: Panicoideae) in southern Africa. Monogr Syst patterns of the grass flora as well as for assessing their Bot Mo Bot Gard 25:129–156 pasture potential. These results will be combined with Fish L, Mashau AC, Moeaha MJ, Nembudani MT (2015) the published results for indigenous legumes and used Identification guide to the southern African grasses. An to develop a collective strategy in terms of prioritizing identification manual with keys, descriptions and distri- butions. Strelizia 36. South African National Biodiversity species, identifying key regions and planning charac- Institute, Pretoria terization and evaluation studies. Forani BD, Tainton NM, Booysen PV (1978) The development of a method for assessing veld condition in three grassveld types in Natal. Proc Grassld Soc S Afr 13:27–33 Acknowledgements We thank the South African National Germishuizen G, Meyer NL (2003) Plants of southern Africa: an Biodiversity Institute (SANBI) for making available the annotated checklist. Strelitzia 14. South African National distribution and descriptive data contained in the BODATSA Biodiversity Institute, Pretoria database, the late Dr Bobby Westfall for administrating the data Gibbs Russell GE (1983) The taxonomic position of C3 and C4 contained in the PHYTOBAS National Vegetation Data Archive Alloteropsis semialata (Poaceae) in southern Africa. and Elsa van Niekerk (ARC-PPR) for the graphics. Bothalia 14:205–213 Gibbs Russell GE (1986) Significance of different centres of Funding The Agricultural Research Council of South Africa diversity in subfamilies of Poaceae in southern Africa. funded this study. Palaeoecol of Africa 17:183–192 Gibbs Russell GE, Watson L, Koekemoer M, Smook L, Barker NP, Anderson HM, Dallwitz MJ (1990) Grasses of south- Data availability The datasets generated during and/or ern Africa. In: Leistner OA (ed) Memoirs of the botanical analysed during the current study are available from the survey of South Africa No. 58. Botanical Research Insti- corresponding author on reasonable request. tute, Pretoria Gibson DJ (2009) Grasses and grassland ecology. Oxford University Press, Oxford

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