The uncommon southern African and Malagasy genus Sartidia in the Aristidoideae, Poaceae resembles the closely related Aristida but has a C3 photosynthetic system, 3–5-veined lower glumes, and a ventrally grooved caryopsis. We present a revision of Sartidia in Madagascar with two species. Sartidia isaloensis is described as new based on its interrupted inflorescence structure, small spikelets, and short awns. A leaf anatomical study and a δ13C analysis confirm that S. isaloensis is a C3 species. Sartidia perrieri is likely extinct in the wild. We present descriptions, typification, illustrations, distribution maps, an identification key, and IUCN conservation assessments. A key to the Aristidoideae in Madagascar is also included.
The Aristidoideae are a small but widespread group of arid climate tropical grasses usually recognisable by their 3-branched awns, which are glabrous in Aristida L. and Sartidia De Winter, and spectacularly ciliate in Stipagrostis Nees. The subfamily is a sister group to all other lineages in the PACMAD clade, a monophyletic group that also includes subfamilies Panicoideae, Chloridoideae, Micrairoideae, Arundinoideae, and Danthonioideae, and encompasses all C4 grass species (Grass Phylogeny Working Group 2001; Grass Phylogeny Working Group II 2012). Aristidoideae comprises ca. 365 species, most of which belong to the large genus Aristida (Clayton et al. 2013; Simon et al. 2013). This subfamily has received attention as a model group for the study of C4 photosynthesis, which has evolved at least twice in the group (Cerros-Tlatilpa and Columbus 2009; Christin and Besnard 2009). The C3 Sartidia is sister to the C4 Stipagrostis (Watson and Dallwitz 1992), forming a lineage that is sister to Aristida. In this second lineage, the early diverging C3 Aristida longifolia Trin. is sister to ca. 250 C4 species (Cerros-Tlatilpa and Columbus 2009). The diversifications of Sartidia and Aristida and other grass species of Malagasy grasslands are currently under study (Vorontsova 2013; Besnard et al. 2014). Our ultimate aim is to reconstruct the vegetation history of the extensive open areas on the High Plateaux and establish the presence and composition of any natural savannas, a controversial subject in Madagascar nature conservation (Bond et al. 2008; Willis et al. 2008; Quéméré et al. 2012; Vorontsova and Rakotoarisoa 2014; Parr et al. 2014).
The southern African and Malagasy genus Sartidia is species poor, rare, and understudied. Its six infrequently collected species (including the one described here) look deceptively similar to common Aristida and have been assumed to be part of Aristida until de Winter (1963, 1965), Bourreil (1967), and more recently Balkwill et al. (2011) who recorded consistent differences in its leaf and embryo anatomy: chlorenchyma cells not radially arranged around bundles, poorly differentiated bundle sheath cells, small embryo, and a ventrally grooved caryopsis. The only visible macromorphological differences between the two genera are the 3–5-veined lower glumes in Sartidia, somewhat broader than the 1-veined Aristida glumes, and the somewhat darker red drying colour of the vegetative parts and glumes in Sartidia.
Sartidia occurs in mid-elevation (ca. 800–2,000 m) dry forest and savanna mosaics where annual rainfall is between 250 and 1,500 mm (Bourreil 1967; Balkwill et al. 2011). Such habitats in tropical African regions are generally dominated by C4 grasses such Aristida and Stipagrostis. How can the C3 Sartidia succeed in these warm, semi-arid environments where photorespiration is expected to be high and should favour C4 grasslands (Sage et al. 2012)? The recently described Sartidia dewinteri J. Munday & L. Fish is restricted to serpentine soils (Balkwill et al. 2011), suggesting that adaptations to hostile environments could allow it to outcompete the high-biomass C4 species. Specificity in the ecological requirements could also account for the rare occurrence of Sartidia. Field observations of the new species on a vertical sandstone wall within a gorge suggest that it could be restricted to habitats protected from fire or partly sheltered from direct sunlight. More investigations into the ecology of this C3 lineage are necessary to identify the causes of the narrow distribution ranges of Sartidia.
The only Malagasy species known prior to this work was Sartidia perrieri (A. Camus) Bourreil, recorded from a single collection made in 1914 (Perrier de la Bâthie 10751). A survey of undetermined Aristida specimens at the Parc Botanique et Zoologique de Tsimbazaza herbarium in Antananarivo (TAN) and at the Muséum National d'Histoire Naturelle herbarium in Paris (P) revealed a few collections distinct from all known species of Aristida, similar to Sartidia, yet different from Sartidia perrieri. This new species was collected by the authors in 2013.
We describe a new species of Sartidia and present a revision of Sartidia in Madagascar. A summary key to the Aristidoideae in Madagascar is presented. This morphological study also builds a platform for ongoing molecular phylogenomic work on herbarium specimens of Sartidia and relatives (Besnard et al. 2014).
Fig. 1.
Sartidia perrieri. A. Habit. B. Ligule. C. Panicle. D. Spikelet. E. Lower glume, dorsal view (midvein and one of the side veins visible). F. Upper glume, dorsal view (midvein and one of the side veins visible). G. Upper glume, ventral view. H. Immature spikelet with the glumes removed. I. Callus. Scale bars: A = 6 cm; B = 1 mm; C = 4 cm; D = 2 cm; E–G = 1 cm; H = 0.6 cm; I = 0.5 mm. Drawn from Perrier de la Bâthie 10751 (P) by Agathe Haevermans.
Materials and Methods
Herbarium collections were studied at P, K, and TAN herbaria. Tissue harvested from a recently collected herbarium specimen (Razanatsoa et al. 578, K) was used to characterize leaf anatomy and photosynthetic type of S. isaloensis. Leaf pieces of approximately 5 mm in length were rehydrated for 24 hr then fixed in Carnoy's fixative (4:1 EtOH:acetic acid) and embedded in Methacrylate embedding resin (Technovit 7100, Heraeus Kulzer GmbH, Wehrhein, Germany). Embedded leaves were sectioned between 6–8 mm thick on a manual rotary microtome (Leica Biosystems, Newcastle, UK) and stained with Toluidine Blue O (Sigma-Aldrich, St. Louis, MO, USA). Stained leaf sections were photographed using microscopy imaging software and a camera mounted on a microscope (CellA; Olympus DP71; BX51, respectively. Olympus, Hamburg, Germany). Images were stitched together (DoubleTake 2.2.9, Echo One, Frederikssund, Denmark) to recreate the continuous width of the whole cross-section.
Dried leaf tissue was prepared for δ13C analysis by the University of Sheffield, Faculty of Science biOMICS facility. The δ13C value is presented as an isotopic ratio in parts per thousand (per mil, ‰), reported relative to the isotopic standard Pee Dee Belemnite (PDB).
Taxonomic Treatment
Key to the Aristidoideae Genera and Sartidia Species in Madagascar
1. 3-branched awns covered in white cilia Stipagrostis (a rare introduction)
1. 3-branched glabrous awn 2
2. Lower glume with 1 vein; plant drying brown; common species Aristida ca. 9 species)
2. Lower glume with 3 veins; plant drying reddish or almost black; rare species 3 (Sartidia)
3. Panicles 6–10 cm long, uninterrupted, dense; lateral awns 2–3.5 cm long 1. Sartidia perrieri
3. Panicles 10–20 cm long, interrupted, loosely contracted; lateral awns 1–1.7 cm long 2. Sartidia isaloensis
1. Sartidia perrieri (A. Camus) Bourreil, Compt. Rend. Hebd. Séances Acad. Sci., Ser. D. 265: 904. 1967. Aristida perrieri A. Camus, Bull. Soc. Bot. France 73: 434. 1926.— TYPE: MADAGASCAR. Prov. Antananarivo: environs d'Antsirabe, prairies, 1,900 m, Jan 1914, Perrier de la Bâthie 10751 (lectotype: P02260115!, chosen here; isolectotypes: K000832639!, K000832640!, P00446503!, P02260114!, P00446293!).
Erect tufted rough perennial ca. 50 cm tall, with short rhizomes, the culms not branched, glabrous. Leaf sheaths glabrous to finely scaberulous, becoming fibrous with age. Ligule a ciliate fringe ca. 0.5 mm long, the trichomes elongating and curling with age. Leaf blades 15–20 cm × 1.5–2 mm, wiry, rolled, erect, glabrous to finely scaberulous, drying dark red to almost black. Inflorescence a densely contracted panicle 6–10 × 4–5 cm, the branches to 3 cm long, pubescent, the pedicels 1.6–6 mm long. Spikelets narrowly ovate, 2–2.5 cm long not including the awns. Glumes unequal, longer than the lemma, membranous, finely scaberulous. Lower glume 2–2.5 cm long, with 3 clear veins and sometimes two additional faint veins, apically acute to long-acuminate. Upper glume 1–1.5 cm long, with one clear vein and two faint side veins, apically acute to obtuse. Floret 1–1.2 cm long including the callus but not including the awns, finely scaberulous towards the apex, the callus pungent (sharp), curved, ca. 1.5 mm long, with a dense covering of callus hairs ca. 0.5 mm long, the lemma passing into an awn column 2–4 mm long, with ca. 2 twists. The awns sub equal, 2–3.5 cm long, the central awn slightly exceeding the side awns, finely scaberulous towards the apex, broadly curved and somewhat retrorse at maturity (Fig. 1).
Distribution —A single collection is known from an area of 1,900 m near Antsirabe (Fig. 2).
Habitat —Sandstone rocks in tapia forest.
IUCN Conservation Assessment—The collection made in 1914 notes that only a single individual was found and H. Perrier de la Bâthie had not seen anything similar. This label annotation is likely to have been the cause of the note of its great rarity in the original description (Camus 1926). The Antsirabe area is heavily populated and grazed, with agricultural expansion likely to have been quite advanced before 1914. Searches for this plant have been conducted with no success by the Missouri Botanical Garden and the Kew Madagascar Conservation Centre. Sartidia perrieri is assessed here as likely “Extinct in the Wild” [EW] following IUCN Categories and Criteria (IUCN 2012).
Notes —A species with instantly recognisable clusters of large spikelets, Sartidia perrieri appears highly distinct from the smaller and more Aristida-like new species (see below). The lectotype has been selected because of its annotation by Aimée Camus, comprehensive material and an illustration demonstrating a 3-veined lower glume attached to the sheet.
Fig. 2.
Distribution of Sartidia perrieri (black circle) and Sartidia isaloensis (white squares). Drawn by Paweł Ficinski.
Fig. 3.
Sartidia isaloensis. A. Young habit with straight leaves. B. Mature habit with curly leaves. C. Ligule. D. Panicle. E. Spikelet. F. Lower glume, dorsal view (three veins visible). G. Upper glume, dorsal view (a single raised midvein visible). H. Immature spikelet with the glumes removed. I. Callus. Scale bars: A, B = 6 cm; C = 5 mm; D = 5 cm; E–G = 1 cm; H = 2 mm; I = 0.8 mm. A, C–I drawn from Morat 3609 (P); B drawn from Bosser 16673 (P) by Agathe Haevermans.
2. Sartidia isaloensis Voronts., Razanatsoa & Besnard, sp. nov.—TYPE: MADAGASCAR. Prov. Fianarantsoa: Isalo National Park, 1.7 km from Namaza camp on the trail to the Blue and Black Pools, narrow ledge above town spring vertical sandstone wall, 816 m, 17 Dec 2013, J. Razanatsoa, M. S. Vorontsova, H. P. Linder, O. P. Nanjarisoa 578 (holotype: TAN!; isotypes: BR!, K!, MO!, P!).
Similar to Sartidia perrieri but differs by its longer interrupted inflorescences and smaller spikelets with shorter awns. Resembles Aristida but has three veins in each glume.
Erect tufted perennial ca. 50 cm tall, with short rhizomes, the culms not branched or branched near the base, glabrous. Leaf sheaths glabrous to hirsute, becoming fibrous with age. Ligule a ciliate fringe ca. 0.5 mm long, the trichomes elongating and curling with age. Leaf blades 15-25 cm × 1.5-2.5 mm, wiry, flat or rolled, erect becoming curly at the base, glabrous to finely scaberulous, drying reddish to almost black, sometimes brown. Inflorescence a loosely contracted terminal interrupted panicle 10-20 × 1.5-2.5 cm, the branches less than 1 cm long, finely scaberulous, the pedicels 0.5–7 mm long. Spikelets narrowly ovate, 1–1.5 cm long not including the awns. Glumes unequal, longer than the lemma, membranous, finely scaberulous on the midvein. Lower glume 0.7–1.5 cm long, 3-veined, the side veins sometimes faint, apically acute to awned, the awnlet to 4 mm long. Upper glume 0.7–1 mm, 1-veined, apically acute to awned, the awnlet to 3 mm long. Floret 0.5–0.7 cm long including the callus but not including the awns, finely scaberulous on the whole surface or towards the apex, the callus acute, 0.7–0.8 mm long with callus hairs ca. 1 mm long, the lemma passing into an awn column 2– 4 mm long, with ca. 2 twists. The awns subequal, 1–1.7 cm long, the central awn sometimes slightly exceeding the side awns, finely scaberulous towards the apex, the side awns straight and perpendicular to the panicle at maturity (Fig. 3).
Distribution—Two localities are known on the high plateau, ca. 800–1,500 m (Fig. 2).
Habitat —Arid exposed locations on sandstone cracks.
IUCN Conservation Assessment —Assessed here as endangered under the criteria EN B1(a,b): known to exist at fewer than five locations, and subject to continuous environmental degradation (IUCN 2012).
Leaf anatomy and photosynthetic system —The leaf anatomy of S. isaloensis is characteristic of a C3 species. Chloroplasts are abundant in the mesophyll cells while there is a paucity of organelles in bundle sheath cells (Fig. 4). There are numerous mesophyll cells between veins and few minor veins, which together create the large interveinal distances characteristic of C3 plants (Fig. 4a; Hattersley and Watson 1975; Renvoize 1987; Sinha and Kellogg 1996). Sartidia isaloensis has a d13C value of -27.55%o, which confirms that this species uses the C3 photo synthetic pathway (Smith and Brown 1973; Cerling et al. 1997).
Notes —This species seems to have been collected only four times prior to this study. It is remarkably similar to Aristida tenuissima A.Camus, Aristida similis Steud., and Aristida rufescens Steud.; identification of reliable distinguishing characters beyond the 3-nerved lower glume in Sartidia is problematic. Sartidia isaloensis appears to be more stout than Aristida, with a more compact inflorescence, redder vegetative parts, and generally darker in colour. Sequences of the chloroplast (rbcL, ndhF, matK, trnL-trnF, rps16 intron) and nuclear (ITS) regions are similar to those of all accessions of Sartidia analysed and consistently different from the numerous species of Aristida and Stipagrostis analysed (Besnard et al. 2014).
Additional Specimens Examined —Madagascar. Prov. Antananarivo: S of Iarinandriana (Iharinandriana), steppe on a hill, ca. 1,500 m, Aug 1962, J. Bosser 16672 (TAN [2 sheets], P [P02257507, P02257506, P03346021]); S of Iarinandriana (Iharinandriana), steppe on a hill, ca. 1,500 m, Aug 1962, J. Bosser 16673 (P [P02257504, P03346020, P02257505]). Prov. Fianarantsoa: Col des Tapias, Isalo National Park, on rocks, ca. 1,000 m, Dec 1959, J. Bosser 13908 (TAN [2 sheets], P [P02215574]); Isalo National Park, 20 km N of Ilakaka, on rocks in a degraded habitat, ca. 900 m, Mar 1970, P. Morat 3609 (TAN, P [P03346064]).
Fig. 4.
Leaf cross sections of Sartidia isaloensis demonstrating anatomy typical of a C3 species: many mesophyll cells between a few large veins. A. Cross section of leaf blade; scale bar = 100 µm; B. Cross section of a leaf blade margin; scale bar = 100 µm. BS = Bundle Sheath; M = Mesophyll; LE = Lower Epidermis; UE = Upper Epidermis; S = Sclerenchyma; VT = Vascular Tissue. Material from the type collection Razanatsoa et al. 578 (K).
Acknowledgments.
Work in Madagascar could not have happened without Hélène Ralimanana, Franck Rakotonasolo, Roger Rajaonarison, Nanjarisoa Olinirina Prisca (Kew Madagascar Conservation centre, Antananarivo), and Stuart Cable (K). We would like to thank Madagascar National Parks (MNP) for granting approval for our work in Isalo, Direction Générale des Forêts (DGF) for the permits, and Parc Botanique et Zoologique de Tsimbazaza (PBZT) for supporting the permit applications. We are grateful to Philippe Morat for discussions about his previous collection of S. isaloensis. This work was financed by the UK SynTax award scheme supported by BBSRC and NERC and by the National Geographic Society Global Exploration Fund GEFNE10–11. Visit to P by MSV was supported by the SYNTHESYS program grant FR-TAF-2694. GB was supported by the LABEX entitled TULIP managed by Agence Nationale de la Recherche (ANR-10-LABX-0041). The authors would also like to thank the curators of TAN, P, and K herbaria, and the manuscript reviewers.
