Systematic Botany (2010), 35(1): pp. 96–101 © Copyright 2010 by the American Society of Plant Taxonomists A New Species of Tarigidia (Poaceae, Panicoideae, Paniceae) from Puerto Rico and Additional Evidence for a Hybrid Origin of the Genus Andrea S. Vega,1,4 Zulma E. Rúgolo de Agrasar,2 and Franklin S. Axelrod3 1 Cátedra de Botánica Agrícola, Facultad de Agronomía, Universidad de Buenos Aires, Av. San Martín 4453, C1417DSE, Buenos Aires, Argentina 2 Instituto de Botánica Darwinion, Labardén 200, C.C. 22, B1642HYD, Buenos Aires, Argentina 3 Herbario del Departamento de Biología, Facultad de Ciencias Naturales, Universidad de Puerto Rico, PO Box 70377 San Juan, Puerto Rico 00936-8377 4 Author for correspondence (avega@agro.uba.ar) Communicating Editor: Lynn Bohs Abstract—A new species of Tarigidia from Puerto Rico is described and illustrated. Additional micromorphological characters of the inflorescence and spikelets are included. This species constitutes the first report of the genus Tarigidia in the New World. Tarigidia axelrodii grows together with Anthephora hermaphrodita and Digitaria bicornis, showing intermediate characters. This species gives additional evidence to support Loxton’s hypothesis that Tarigidia is derived from hybridization between Anthephora and Digitaria and also supports the phylogenetic hypothesis showing close relationships between Anthephora and Digitaria. Resumen—Se describe e ilustra una nueva especie de Tarigidia en Puerto Rico. Se incluyen caracteres adicionales de la inflorescencia y espiguillas. Esta especie constituye el primer registro del género Tarigidia en América. Tarigidia axelrodii crece junto a Anthephora hermaphrodita y Digitaria bicornis, mostrando caracteres intermedios. Esta especie provee evidencia adicional apoyando la hipótesis de Loxton sobre el origen híbrido de Tarigidia a partir de Anthephora y Digitaria y, al mismo tiempo, sustenta la hipótesis filogenética donde se sugieren estrechas relaciones entre Anthephora y Digitaria. Keywords—Anthephora, Digitaria, hybrid origin, phylogeny, Tarigidia. Materials and Methods The genus Tarigidia Stent (1932), an anagram of Digitaria Haller emend. A. S. Vega & Rúgolo (Vega and Rúgolo de Agrasar 2001), comprises only one species distributed in Namibia and South Africa (Gibbs Russell et al. 1990). According to Clayton and Renvoize (1986), who place both genera in subtribe Digitariinae Butzin, Tarigidia combines the characters of Digitaria and certain genera of subtribe Cenchrinae Dumort. Cenchrinae is characterized by the presence of bristles or scales subtending the spikelet and deciduous with it. Loxton (1974) suggested that Tarigidia arose by hybridization between the genera Digitaria and Anthephora Schreb., without providing any plausible evidence. Until now, Tarigidia has been considered monotypic. The single species T. aequiglumis (Gooss.) Stent, is a perennial and possible intergeneric hybrid between Anthephora pubescens Nees and an unidentified species of Digitaria sect. Erianthae Henrard (Loxton 1974). Hybridization between these genera is considered a rare phenomenon that occurs under natural conditions and caryopsis production of T. aequiglumis has never been reported (Goossens 1932; Stent 1932; Loxton 1974; Watson and Dallwitz 1992). According to Chippindall (1955), in general appearance Tarigidia looks like a species of Anthephora, but in the latter genus the spike-like panicle is not branched. In T. aequiglumis the inflorescence is variable, with a woolly spike or a contracted panicle. Spikelets of Tarigidia are similar to Digitaria, but differ from it in having the lower glumes well developed. The aim of the present paper is to report a new species of Tarigidia, T. axelrodii A. S. Vega & Rúgolo, whose parents possibly may be Digitaria bicornis (Lam.) Roem. & Schult. and Anthephora hermaphrodita (L.) Kuntze. This species constitutes the first report of the genus Tarigidia in the New World and provides additional information both for the hybrid origin of the genus and for the hypothesis of a phylogenetic alliance between Digitaria and Anthephora. Morphology—The description is based primarily on living and herbarium material deposited at BAA, MO, NY, SI, UPRRP, and US (acronyms after Holmgren et al. 1990). Micromorphology—Micromorphological observations were based on herbarium material. The main axis of the inflorescences, spikelets and their bracts, as well as the caryopses, were selected and cleaned in xylene for 1 hr with an ultrasonic cleaner (Cleanson, model CS 1106, Argentina). The material was air-dried, mounted and coated with a gold-palladium (40% - 60%) alloy by a Thermo VGScientific and then observed using a Phillips XL 30 (Phillips, The Netherlands) Scanning Electron Microscope (SEM) at the Museo Bernardino Rivadavia, Argentina. Taxonomic Treatment Tarigidia axelrodii A. S. Vega & Rúgolo, sp. nov.—TYPE: PUERTO RICO. Cabo Rojo: Bo. Boquerón, Rt 301, km 11, behind information center opposite salinas, at end of nature trail, salt flats, 17°57.53' N, 67°11.93' W, ca. 1 m, 9 Nov 2008, F. Axelrod & R. Thomas 14068 (holotype: US!; isotypes: BAA!, MO!, NY!, SI!, UPRRP!). A Tarigidiae aequiglume differt habitu annuo statura minore, usque ad 50 cm alto; axe inflorescentiae quadrangulari, scabroso, racemis (4 vel)5–8, divergentibus, deciduis, alternis; spiculis binis, inaequaliter subsessilibus, heteromorphis, cleistogamis; spiculae inferiores glumis dissimilis, gluma inferiore (0.5–)1–1.5(–2.5) mm longa, cartilaginea, 1–3-nervata, glabra vel margine piloso; gluma superiore 3–3.5 mm longa, 3-nervata, pilosa; lemmate sterili cum pilis filiformibus ad marginem; lemmate fertili cartilagineo, margine membranaceo; staminibus 3, antheris 1.8–1.9 mm longis; caryopside oblonga, 2.2–2.4 mm longa. Spiculae superiores lemmate sterili in dorso pilis filiformibus, setaceis, rigidis munita. Annual plants ca. 50 cm tall. Culms 1–2.3 mm diam., terete, decumbent, rooting at the lower nodes, glabrous. Nodes compressed, conspicuous, brown, glabrous. Leaf sheaths 3.5–6 cm long, hirsute, the hairs with a swollen base. Ligules 2–2.7 mm long, membranous, truncate, the margin erose. Base of the 96 2010] VEGA ET AL.: NEW SPECIES OF TARIGIDIA leaf-blade (behind the ligule) hirsute. Leaf blades 6.3–8.5 cm long, 5.5–7 mm wide, lanceolate, flat, papyraceous, the apex acuminate, the adaxial surface scabrous, the abaxial surface scabrous and the midrib is sparsely hirsute with hairs that have a swollen base. Peduncle 35 cm long, glabrous. Panicle (3.2–) 4–7.5 cm long, (0.8–)1–2 cm wide, with (4–)5–8 alternate racemes on an axis (1–)3–4.5 cm long, quadrangular, scabrous, sinuous. Racemes ending in a spikelet, rigid, divergent, deciduous. Rachis 0.6–1 mm wide, winged, the wings reduced toward the apex of the racemes, the margin scabrous. Pedicels 0.3–1 mm long, scarcely developed, scabrous. Spikelets 4.5–5 mm long, 1.2–1.3 mm wide, paired, heteromorphous, cleistogamous, with purplish tints at maturity. Lower spikelets of the racemes scarcely pilose, with 5 nerves visible on the back, the back glabrous, pilose on the margins. Pedicellate spikelets with 3 or 5 nerves visible on the sterile lemma backs, with both sericeous and long hirsute hairs, these setiform, whitish, spreading at maturity. Subsessile spikelets with 3 nerves on the sterile lemma backs, the indumentum composed of sericeous hairs. Lower glume (0.5–)1–1.5 (–2.5) mm long, 1–3-nerved, narrow-triangular, the apex acuminate, the margin scabrous, glabrous, occasionally pilose, in this case the hairs largely exceeding its length. Upper glume 3–3.5 mm long, 3-nerved, lanceolate, pilose in internerve and marginal zones, the hairs exceeding its length. Lower sterile floret reduced to a lemma as long as the spikelet, the apex acute, 7-nerved, the nerves prominent, smooth, the midnerve distant from contiguous lateral and marginal nerves, glabrous on both sides of midnerve and alternately pilose and glabrous on the remaining zones, the indumentum not exceeding the length of the lower lemma. Upper fertile floret ca. 4 mm long, 1 mm wide, cartilaginous with membranous margins, striate, narrowly-lanceolate, apiculate, the apex scabrous, stramineous with purplish tints at maturity. Upper lemma 3-nerved, the midnerve distant from marginal nerves, without a germination flap. Upper palea 2-nerved. Lodicules 2, truncate. Stamens 3; anthers 1.8–1.9 mm long, yellow with purplish tints. Ovary glabrous; stigmas plumose, purplish. Caryopsis 2.2–2.4 mm long, 1–1.3 mm wide, ellipsoid; embryo 1.4 mm long; hilum 0.3 mm diam, circular, brown. Figures 1–3. Etymology—The specific epithet is dedicated to Dr. Franklin S. Axelrod, collector of the type of this new species, specialist in the vascular plants of Puerto Rico and Herbarium Collections Manager at UPRRP. Additional Specimens Examined—PUERTO RICO. Cabo Rojo: Bo. Boquerón, Rt 301, km 11, behind information center opposite salinas, salt flats, 17°57.53' N, 67°11.93' W, ca. 1 m, 12 Nov 2007, F. Axelrod & J. Turnquist 13906 (BAA, UPRRP). Associated Species—Tarigidia axelrodii (Axelrod & Thomas 14068) was found in a population of Anthephora hermaphrodita in a large patch in an open area in sand flats near the sea. Digitaria bicornis was growing about a kilometer away. Vouchers for these associated species are: Anthephora hermaphrodita - PUERTO RICO. Mpio. Cabo Rojo: Bo. Boquerón, Rt. 301, km 11, nature trail though salt flats behind information center and opposite salinas, open area at edge of salt flats, 17°57.53' N 67°11.93' W, 1 m, 9 Nov 2008, F. Axelrod & A. Axelrod 14069 (UPRRP). Digitaria bicornis - PUERTO RICO. Mpio. Cabo Rojo: on the hill E of the lighthouse at Cabo Rojo, dry thickets in salt spray, 0–30 m, 3 Dec 1989, C. M. Taylor 9705 (UPRRP). Distribution and Morphological Features in Species of Tarigidia—So far as is known Tarigidia is composed of only 97 two species: T. aequiglumis and T. axelrodii. In Table 1 the morphological characters of T. aequiglumis (derived from Goossens 1932; Chippindall 1955; Clayton et al. 2006 onwards) are compared with those of T. axelrodii. Tarigidia and Relationships with Digitaria and Anthephora—Tarigidia axelrodii shows characters intermediate between Digitaria bicornis and Anthephora hermaphrodita, the possible parents. Cytogenetics and molecular studies are being undertaken to confirm this hypothesis (Vega et al. in prep.). The existence of Tarigidia aequiglumis and T. axelrodii, both proposed on the hypothesis of hybridization between Digitaria and Anthephora, supports the phylogenetic hypothesis that includes Digitaria, Anthephora, and two other small genera [Chaetopoa C. E. Hubb. and Chlorocalymma Clayton (L. Aagesen pers. comm.)] in the same well supported clade (Morrone et al. in press). Taxa in this clade share a 24 bp deletion within the plastid ndhF sequences (Morrone et al. in press). Digitaria bicornis and A. hermaphrodita were observed growing in or near the same site where this new species was found. In November 2007 and 2008 two collections were made of T. axelrodii. Caryopses collected from this population were seeded and the resulting plants have been successfully maintained under cultivation at the Jardín Botánico Lucien Hauman, Facultad de Agronomía, Universidad de Buenos Aires (Argentina). At the end of December 2008, the dry season began in the southwest corner of Puerto Rico. The populations of T. axelrodii and A. hermaphrodita had died back and only a handful of old inflorescences with caryopses persisted. Digitaria bicornis was not to be seen, although it is generally widespread within about a kilometer or so of the site in Cabo Rojo. Digitaria bicornis has also been collected in Fajardo, Juana Díaz, Lajas, Loíza, Mayagüez, Río Grande, Anegada, Guana Island, and Great Camano Island, at 1–550 m, flowering and fruiting in June through April (Vega & Rúgolo de Agrasar unpubl.). Anthephora is mainly distributed in Africa and temperate Asia. Only one species, A. hermaphrodita, is extensive in the neotropics (Clayton et al. 2006 onwards). Digitaria is a genus of worldwide distribution in tropical, subtropical, and temperate areas (Watson and Dallwitz 1992). In particular, D. bicornis (sect. Biformes Henrard) is a weed introduced into the New World from the Old World and grows from sea level to 1,500 m in disturbed areas, in dry riverbeds, on eroded slopes with bare soil, and in semideciduous forests. This species is characterized by the presence of heteromorphous spikelets and this character is also shared by T. axelrodii. Digitaria bicornis differs from T. axelrodii in having the following characters: panicle digitate or subdigitate, 6–17 cm long, with 2–7 nondeciduous racemes, on an axis 0.3–0.9 cm long; rachis triquetrous (3-angled), narrowly winged, straight; pedicels unequal in length; subsessile spikelets 2.7–2.8 mm long, 0.8–0.9 mm wide; pedicellate spikelets 3–3.3 (–3.6) mm long, 0.9–1 mm wide; lower glumes 0.3–0.5 mm long, nerveless, triangular, apex obtuse; upper glumes 2–2.5 mm long; anthers 0.7–0.8 mm long. Species of Digitaria can be recognized by their cartilaginous upper florets, with fertile lemmas having a germination flap and noninrolled membranous margins, scarcely exposing the fertile palea. The cartilaginous and striate upper floret of T. axelrodii is similar to that in D. bicornis. Margins of the upper lemma are membranous, flat, and noninrolled (Fig. 2G). 98 SYSTEMATIC BOTANY [Volume 35 Fig. 1. Tarigidia axelrodii (Axelrod & Thomas 14068, US). A. Habit. B. Ligule. C. Main axis after raceme dispersal. D. Raceme, view from the back of the rachis. E. Raceme, view from the spikelets. F. Heteromorphous paired spikelets: subsessile (left) and shortly pedicelled (right). G. Spikelet, view from the upper glume. H-I. Lodicules of the lower flower, dorsal and ventral view. J. Upper floret, view from the back of the upper lemma. K. Upper floret, view from the back of the upper palea. L. Upper palea, lodicules, caryopsis, and the remains of anthers and stigmas. M. Caryopsis, scutellar view. N. Caryopsis, hilar view. 2010] VEGA ET AL.: NEW SPECIES OF TARIGIDIA 99 Fig. 2. SEM photographs of Tarigidia axelrodii spikelets. A. Rachis fragment with a pair of spikelets. B. Terminal spikelet of a raceme. C. Back of the occasionally pilose lower glume in a terminal spikelet of a raceme. D. Back of the lower glume. E. Upper floret (not containing a mature caryopsis). F. Caryopsis, hilar view. G. Middle portion of the upper floret view from the back of the palea. Note flat and membranous margins of the upper lemma (arrow). H. Striate upper lemma in dorsal view. I. Lodicules of the upper flower. Abbreviations: hh. hirsute hairs; lg. lower glume; ll. lower lemma; lo. lodicule; p. pedicel; pa. papilla; ps. shortly pedicelled spikelet; ra. rachis; ss. subsessile spikelet; ul. upper lemma; up. upper palea. 100 SYSTEMATIC BOTANY [Volume 35 Fig. 3. Main axis and racemes of Tarigidia axelrodii. A. Fragment of the main axis in a mature inflorescence showing abscission scars after raceme dispersal. B. Detail of an abscission scar, frontal view. C. Base of a raceme showing congested clusters of spikelets. Abbreviations: as. abscission scars; ma. main axis. Epidermal cells of upper lemma and palea are 1-papillate and this papilla occupies an eccentric position (Fig. 2H). In relation to caryopsis dispersal in D. bicornis, as well as in most species of the genus, the unit of dispersal is the spikelet. Another dispersal mechanism is exhibited by species with Table 1. “tumbleweed” inflorescences and marks a well supported morphology-based clade that is composed of members of Digitaria sections Parviglumae Henrard and Pennatae (Stapf) Henrard, and D. subg. Leptoloma (Chase) Henrard (Vega et al. 2009). The pedicellate spikelets of Digitaria bicornis are the first Comparative diagnostic characters between T. axelrodii and T. aequiglumis. T. axelrodii Life cycle duration Height (cm) Blade length (mm) Inflorescence length (cm) Raceme length (cm) Inflorescence type annuals ca. 50 5.5–7 (3.2–)4–7.5 2–4.2 panicle with divergent racemes at maturity Spikelet length (mm) Spikelet paired (appearance) Length relation between lower and upper glumes Lower glume length (mm) Lower glume nerves and indumentum 4.5–5 heteromorphous unequal (0.5–)1–1.5(–2.5) (¼–¹⁄³ of the spikelet) 1–3 glabrous, rarely pilose, in this case largely exceeding its length 3–3.5 (²⁄³–¾ of the spikelet) 7 glabrous on both sides of midnerve and alternately pilose and glabrous on the remaining zones cartilaginous with membranous margins 2.2–2.4 × 1–1.3 Puerto Rico (America) Upper glume length (mm) Lower lemma nerves and indumentum Upper floret Caryopsis length (mm) × width (mm) Geographical distribution T. aequiglumis perennials 80–120 3–4 5–12 0.5–3 contracted panicle, spike-like, or sometimes with long branches not closely appressed to the main axis 4–4.5 homomorphous equal or subequal ca. 2.7–3 (²⁄³ of the spikelet) 1 glabrous or densely villous, shortly ciliate on the margins ca. 2.7–3 (²⁄³ of the spikelet) 5–7 villous between the nerves and near the margins not indurated unknown Namibia and South Africa (Africa) 2010] VEGA ET AL.: NEW SPECIES OF TARIGIDIA to disarticulate, followed by the subsessile spikelets. The rachis of the racemes of digitate or subdigitate panicles is persistent after diaspore dispersal (i.e. the panicles persist on the plant). Tarigidia shows a type of dispersal not observed in Digitaria. In T. axelrodii the branches of the inflorescences provided with spikelets constitute the units of dispersal; they are rigid, straight, and disarticulate easily at the base. The denuded 101 main axis persists showing circular abscission scars after the racemes disperse (Fig. 3A-B). Another characteristic not observed in Digitaria is the disposition of the spikelets: due to the poor development of pedicels and internodes between them along the rachis, the spikelets form dense clusters at the base and congested pairs toward the apex of the racemes (Fig. 3C). Key to the Genera ANTHEPHORA, TARIGIDIA, and DIGITARIA 1. Racemes persistent; diaspores formed either by the spikelets or complete inflorescences; spikelets solitary, paired or in groups of 3 or more, each one disarticulating from the pedicels, not surrounded by an involucre of stiffly coriaceous narrowly elliptic several-nerved bracts; lower glumes reduced to a membranous margin or developed, nerveless, rarely 1-nerved, not joined to those of other spikelets, glabrous; upper lemma with a germination flap . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Digitaria 1. Racemes deciduous, constituting the units of dispersal; spikelets grouped in clusters, not disarticulating from the pedicels, surrounded or not by an involucre of stiffly coriaceous narrowly elliptic several-nerved bracts; lower glumes coriaceous, 1–3-nerved, joined or not to those of other spikelets, glabrous or pilose; upper lemma without a germination flap . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2. Racemes 0.35–1.1 cm long, composed of 2–10 fertile spikelets, surrounded by an involucre of 2–10 sterile spikelets represented by stiffly coriaceous, narrowly elliptic several-nerved bracts, free or connate in lower third; lower glumes joined or not to those of other spikelets . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Anthephora 2. Racemes 0.7–4.2 cm long, composed of 2–21 fertile spikelets, not surrounded by an involucre of bracts; lower glumes not joined to those of other spikelets . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Tarigidia Acknowledgments. The authors are grateful to Sandra de VilliersSoltynski for providing references, to Vladimiro Dudás and DG. Tomás E. Aversa for their help with the illustration and figures, respectively, and to Raúl Pozner for the correction of the Latin diagnosis. Literature Cited Chippindall, L. K. A. 1955. A guide to the identification of grasses in South Africa. Pp. 1–527 in The grasses and pastures of South Africa, ed. D. Meredith. Parow, South Africa: Cape Times Ltd. Clayton, W. D. and S. A. Renvoize. 1986. Genera Graminum. Grasses of the world. Kew Bulletin. Additional Series 13: 1–389. Clayton, W. D., K. T. Harman, and H. Williamson. 2006 onwards. GrassBase - The Online World Grass Flora. http://www.kew.org/ data/grasses-db.html [version: 29 January 2008, accessed 07 April 2009]. Gibbs Russell, G. E., L. Watson, M. Koekemoer, L. Smook, N. P. Barker, H. M. Anderson, and M. J. Dallwitz. 1990. Grasses of Southern Africa. Memoirs of the Botanical Survey of South Africa 58: 1–437. Goossens, A. P. 1932. The genus Anthephora Schreb. Transactions of the Royal Society of South Africa 20: 189–200. Holmgren, P. K., N. H. Holmgren, and L. C. Barnett. 1990. Index herbariorum. Part I: The herbaria of the world. Regnum Vegetabile vol. 120. Bronx: New York Botanical Garden. Loxton, A. E. 1974. A note on a possible bigeneric hybrid between Digitaria and Anthephora. Bothalia 11: 285–286. Morrone, O., L. Aagesen, M. A. Scataglini, D. Salariato, S. S. Denham, M. A. Chemisquy, S. Sede, L. M. Giussani, E. A. Kellogg, and F. O. Zuloaga. In press. Phylogeny of the Paniceae (Poaceae: Panicoideae) integrating chloroplast DNA sequences and morphology, in A Summit of Cladistics. XXVII Meeting of the Willi Hennig Society and VIII Reunión Argentina de Cladística y Biogeografía, eds. C. Szumik and P. Goloboff. Cladistics. Stent, S. M. 1932. Notes on African grasses: XII. A new genus from the Orange Free State. Kew Bulletin 1932: 151–152. Vega, A. S. and Z. E. Rúgolo de Agrasar. 2001. Morphological interpretation of the spikelet in Digitaria atra (Poaceae: Panicoideae: Paniceae) and emended generic description. American Journal of Botany 88: 1670–1674. Vega, A. S., G. H. Rua, L. T. Fabbri, and Z. E. Rúgolo de Agrasar. 2009. A morphology-based cladistic analysis of Digitaria (Poaceae, Panicoideae, Paniceae). Systematic Botany 34: 312–323. Watson, L. and M. J. Dallwitz. 1992. The grass genera of the world. Wallingford, U.K.: C. A. B. International.