Pteridium arachnoideum (Kaulf.) Maxon subsp. campestre (Schrad.) Schwartsb. & P.L.R. Moraes, 2014

Schwartsburd, Pedro B., De Moraes, Pedro L. R. & Lopes-Mattos, Karina L. B., 2014, Recognition of two morpho-types in eastern South American brackens (Pteridium-Dennstaedtiaceae-Polypodiopsida), Phytotaxa 170 (2), pp. 103-117 : 109-112

1. Pteridium arachnoideum (Kaulf.) Maxon subsp. arachnoideum . ( Figs. 1D–F , 2A–C )

Pteridium arachnoideum (Kaulf.) Maxon (1924: 89) . Pteris arachnoidea Kaulfuss (1824: 190) , nom. cons. Allosorus arachnoideus (Kaulf.) Presl (1836: 153) , as “(Desv.) C. Presl”. Pteris aquilina Linnaeus (1753: 1705) var. arachnoidea (Kaulf.) Eaton (1861: 203) . Cincinalis arachnoidea (Kaulf.) Trevisan de Saint-Léon (1874:31) . Pteridium aquilinum (L.) Kuhn (1879:11) var. esculentum ( Forster 1786: 74) Kuhn (1882: 347) f. arachnoideum (Kaulf.) Hieronymus (1909: 246) . Pteridium aquilinum (L.) Kuhn var. arachnoideum (Kaulf.) Brade (1920: 56) . Filix-foemina aquilina (L.) Farwell (1931: 290) var. arachnoidea (Kaulf.) Farwell (1931: 290) . Pteridium caudatum ( Linnaeus 1753: 1705) Maxon (1901: 631) subsp. arachnoideum (Kaulf.) Lellinger (2003: 150) . Pteridium esculentum (G. Forst.) Cockayne (1908: 34) subsp. arachnoideum (Kaulf.) Thomson (2012: 45) . Lectotype (designated here):— BRAZIL. “Habitat in Brasília”, without date, C.A. de Chamisso s.n. (LE!). ( Figs. 1D–F , 2A–C )

= Aspidium brasilianum Presl (1822: 176) , nom. rej. Cystopteris brasiliana (C. Presl) Presl (1836: 93) . Hypolepis brasiliana (C. Presl) Kuhn (1882: 347) . Lectotype (designated by Schwartsburd & Prado 2011):— BRAZIL. Rio de Janeiro: “ Ad Rio Janeiro Brasilia legit def.” [In via ad S. João Marcos ad Engenho da Varge, Capit. Rio de Janeiro], [March 1818], J.B.E. Pohl s.n. [3794] (lectotype PRC!, isolectotype W!).

= Pteris psittacina Presl (1822: 185) , nom. rej. Allosorus psittacinus (C. Presl) Presl (1836: 153) , as “ psitaccinus ”. Pteris aquilina L. var. psittacina (C. Presl) Baker (1870: 403) . Pteridium psittacinum (C. Presl) Maxon (1933: 141) . Pteridium aquilinum (L.) Kuhn subsp. psittacinum (C. Presl) Christensen (1934: 166) . Lectotype (designated by Schwartsburd & Prado 2011):— BRAZIL. Rio de Janeiro: “ Ad Rio Janeiro Brasilia” [Circa Rio de Janeiro in collibus], [December 1818], J.B.E. Pohl s.n. (lectotype PRC!, isolectotype W!).

= Cheilanthes aquilinaris Fée (1873: 37 , t. 91, fig. 1). Hypolepis aquilinaris (Fée) Christ (1901: 636) . Lectotype (designated here):— BRAZIL. Rio de Janeiro: “Brasilia fluminensis”, [Haut Itatiaia], [6 June 1871], A.F.A. Glaziou 5330 (lectotype B!-20 0074529, isolectotypes C- n.v., HBG -n.v., K!-000640338, NY-fragment [00144358, image!], P-00633378 [ex Herb. Fée, image!], P-00633379 [image!], P-00633380 [ex Herb. Glaziou, image!], P-00633381 [ex Herb. Glaziou, image!], S-05-9822 [image!], S-10- 34455 [image!], US-00066403 [image!]). syn. nov.

= Pteridium aquilinum (L.) Kuhn var. umbrosum H. Christ ex Rosenstock (1907: 90) , nom. illeg. (non Luerssen 1889: 107). Syntypes:— BRAZIL. Rio Grande do Sul: Santa Cruz, Fazenda Tangerina, withou date, L.C. Jürgens & A. Stier 95 (S? n.v.), Mun. Rio Pardo, Fazenda Soledade, without date, L.C. Jürgens & A. Stier 118 (NY [image!], S? n.v., possible syntype MVM! [“ Jürgens & Stier 190 b ”]). syn. nov.

Plants terrestrial, thicket forming. Rhizomes long-creeping, branching, with two circles of perforated dictyosteles, lanose. Fronds (1.2–)2–3(–4.5) × (1–)1.3–1.8(–3) m, petioles stramineous, proximally with epipetiolar roots, adaxially sulcate, up to 2 m long, glabrous, laminae rhombic, proximally 3–4-pinnate-pinnatifid, medially less dissected, distally pinnatifid, pinnae and pinnules distally with free lobes between the segments, compound distal segments inequilateral, irregularly dissected, caudate at apex, simple distal segments linear, up to 3(–4) cm long, costae abaxially terete, with reddish catenate hairs, 5–7-celled, 0.3–0.5 mm long, adaxially glabrous, costules abaxially strongly flattened with wing-like appearance, with reddish catenate hairs, adaxially glabrous, veins abaxially strongly raised, lanose, with lax arachnoid hairs, 0.6–0.8 mm long, adaxially glabrous, laminar tissue between the veins abaxially glabrous and totally visible, adaxially glabrous, stomatal guard-cells 27–34 µm long, infertile pseudo-indusia 0.2–0.3 mm wide, the marginal cells horizontal.

Distribution and ecology: —Eastern Brazil, Uruguay, Paraguay and central/north-eastern Argentina. From sea level to 2200 m elev., in open habitats (Pampas, Campos Gerais, altitudinal fields, coastal sandy Restinga, crop lands, pastures, disturbed areas), forming extensive thickets, rarely in the edge of forested areas and clearings ( Fig. 3 ).

Representative specimens examined: — BRAZIL. Ceará: Pacoti, Serra do Baturité , [-4.2832°, -38.9314°], 700- 800 m, 9 April 2011, P. B . Schwartsburd & M. F . Moro 2490 ( NY, SP, VIC) . Paraíba: Alhandra , [-7.4397°, -34.9157°], 16 December 1985, A. J. R . Silva s.n. ( UFP 7135 ) . Pernambuco: Jaqueira, Usina Colônia, Córrego do Guariba e Serra do Quengo , 08°43’S, 35°50’20”W, 700 m, 18 March 2011, P. B . Schwartsburd & Seu Dejau 2342 ( SP, UFP, VIC) . Alagoas: Ibateguara, Engenho Coimbra , [-9.0114°, -35.8866°], 380–400 m, 19 December 2000, M. R . Pietrobom-Silva & A. C. P . Santiago 4680 (UFP). Bahia: Near Poções, [Lucaia], [11] March 1817, Wied s.n. (BR-5418671, K, MEL-2353758). Distrito Federal : 20 km East of Brasília, Chapada da Contagem, [-15.8732°, -48.1567°], 700–1000 m, 19 August 1964, H. S . Irwin & T. R . Soderstrom 5301 ( NY, SP) . Minas Gerais: Alto Caparaó , P. N . Caparaó , [-20.4080°, -41.8344°], 1970 m, 11 July 2009, P. B . Schwartsburd et al. 2092 ( VIC) . Mato Grosso do Sul: Ivinhema , [-22.2360°, -53.7825°], 22 November 2003, A . Sciamareli et al. 06 ( UPCB) . Rio de Janeiro: Itatiaia , P. N . Itatiaia , 22°21’46”S, 44°43’40”W, 2200 m, 14 July 2009, P. B . Schwartsburd et al. 2128 ( NY, VIC) . São Paulo: Ilha dos Alcatrazes , [-24.1005°, -45.6952°], 50 m, 26 October 2011, P. B . Schwartsburd & L . Rossi 2570 ( SP, VIC) . Paraná: Ponta Grossa , P. E . Vila Velha, Fortaleza , [-25.2305°, -49.9927°], 5 March 2006, P. B . Schwartsburd et al. 1008 ( UPCB) . Santa Catarina: Praia Grande , P. N . Aparados da Serra, [-29.2025°, -50.0321°], 200 m, 5 August 2009, P. B . Schwartsburd et al. 2255 ( NY, SP, VIC) . Rio Grande do Sul: São Leopoldo , [-29.7640, -51.1825 °], 22 January 1933, A . Sehnem s.n. (SP-50626).— URUGUAY. Artigas: Cuaró , [-30.6174°, -56.9125°], December 1924, C . Osten 17349 ( MVM) . Durazno: En Rio Negro, [-33.0460°, -57.0656°], 3 August 1922, C . Osten 16517 ( MVM) . Treinta y Tres: Yerbal , [-33. 2244°, -54.4026°], November 1819, M. B . Berro 1263 ( MVM) . Lavalleja: Minas, Arequita , [-34.2865°, -55.2642°], 7 November 1819, M. B . Berro 1264 ( MVM) . Flores: Cueva del Tigre, en Guaycurú , [-33.4862°, -56.8385°], 30 October 1896, C . Osten 3297 ( MVM) . San José: Serra Mahoma, [-34.0898°, -56.9454°], 1939, Chebataroff 2607 ( MVM) . Maldonado: Cerro del Pan de Azucar , [-34.8100°, -55.2590°], 28 March 1885, Anonymous [Arechavaleta?] (MVM-4198) .— PARAGUAY. Amambay: National Park Cerro Corá , 22°39’51”S, 55°19’18”W, 350 m, without date, E. M . Zardini & P . Báez 52308 ( NY) . Caazapá: Estancia Tapytá of Shell Forestry Ltd. , 26°16’26”S, 55°45’47”W, 150 m, 14 December 1999, E. M . Zardini & P . Báez 52891 ( NY) .— ARGENTINA. Misiones: Aristóbulo del Vale, Reserva UNLP , 8 January 2003, G . Marquez 25 ( VIC). Córdoba: Sierra Grande , [-31.4857°, -64.7422°], 1 February 1936, A. P . Rodrigo 594 ( NY) .

Remarks:— Plants from western South America (including north-western Brazil) and Central America, commonly ascribed to Pteridium arachnoideum s.l., are morphologically different and shall be treated in at least one other subspecies of P. arachnoideum . These plants present the laminar tissue between the veins abaxially with farinose appearance, not visible, copiously furnished with gnarled hairs, whereas in all 191 specimens of P. arachnoideum subsp. arachnoideum s. str. analysed, the gnarled hairs are totally absent. Instead, this part is visible and completely glabrous ( Figs. 1F , 2B ), conflicting with the descriptions of Moran (1995), Thomson & Martin (1996: Figs. 4B, 5E, F), and Mickel & Smith (2004). Although Thomson & Martin (1996) regarded P. aquilinum var. arachnoideum in a broad sense, they indeed observed the same pattern (on page 46): “In contrast, accessions of var. arachnoideum from three localities in Brazil (...) and one from Uruguay (...) lacked intervein hairs of any kind on the lower surface...”.

In central South America, there is a dry region named the Dry Diagonal (or Diagonal of Open Areas) connecting the Argentinian/Bolivian Chaco, through the Cerrado (Brazilian savannah), up to the Caatinga (Brazilian semi-desert vegetation), and separating South America into two blocks of wetter regions (mainly dominated by forested areas) ( Morrone & Coscarón 1996, Fig 3 ). Pteridium arachnoideum s.l. is practically absent in the Dry Diagonal, even though it is a species from open areas (personal observation throughout central Brazil, see also Tryon 1941: Map 12), probably requiring wetter environmental conditions to stablish populations. Apparently, P. arachnoideum subsp. arachnoideum s. str. and the subspecies from western South America and Central America are geographycally segregated by the Dry Diagonal.

2. Pteridium arachnoideum (Kaulf.) Maxon subsp. campestre (Schrad.) Schwartsb. & P.L.R. Moraes , comb. et stat. nov. ( Figs. 1A–C , 2D–G )

Pteris campestris Schrader (1824: 871) . Lectotype (designated here):— BRAZIL. Bahia: “Brasilia, Prov. Bahiensis”, [near Ilhéus], 1817, Wied s.n. (lectotype LE! [ex Herb. Schrader], isolectotypes BR!-5419005 [ex Herb. Martii], BR!-5418022 [fragment,ex Herb. l’État]). ( Figs. 1A–C , 2D–G )

= Aquilina gardneri C. Presl ex Ettingshausen (1865: 91 , t. 53, fig. 6, t. 54, fig. 3). Pteris gardneri C. Presl ex Ettingshausen (1864: 42) , nom. illeg., non Pteris gardneri ( Fée 1852: 139) Hooker (1858 [1852]: 206). Type:— BRAZIL. State unknown: “In Brasilia”, without date, G. Gardner, coll. Pl. Bras. 1224 (holotype W- n.v., isotype PRC! [ex Herb. Presl]). syn. nov.

Plants terrestrial, thicket forming. Rhizomes long-creeping, branching, with two circles of perforated dictyosteles, lanose. Fronds 1.0–1.5(–2.0) × 0.6–1.0 m, petioles stramineous, proximally with epipetiolar roots, adaxially sulcate, up to 0.8 m long, glabrous, laminae rhombic, proximally 3-pinnate-pinnatifid, medially less dissected, distally pinnatifid, pinnae and pinnules distally without free lobes between the segments, compound distal segments equilateral, regularly dissected, not caudate at apex, simple distal segments linear, up to 1.0(–1.5) cm long, costae abaxially terete, with reddish catenate hairs, 5–7-celled, 0.3–0.5 mm long, adaxially glabrous, costules abaxially slightly flattened, with reddish catenate hairs, adaxially glabrous, veins abaxially slightly raised, hirsute, with conspicuous stiff acicular hairs, 0.2–0.3 mm long, adaxially glabrous, laminar tissue between the veins abaxially with farinose appearance, not visible, totally covered by conspicuous gnarled hairs, adaxially glabrous, stomatal guard-cells 28–35 µm long, infertile pseudoindusia 0.3–0.4 mm wide, the marginal cells vertical.

Distribution and ecology: —Endemic to north-eastern Brazil, at or near sea level in open habitats with white sand soil (Restinga and Mussununga; Saporetti-Junior et al. 2012), a few collections inland up to ca. 1000 m, also from sandy soil spots ( Fig. 3 ).

Representative specimens examined: — BRAZIL. Ceará: Queimadas, São Benedito, Serra da Ibiapaba , [- 7.1021°, -40.1778°], 7 January 1942, P . Bezerra 403 ( IPA) . Paraíba: Mamanguape , BR 101 , próximo ao km 55, [- 6.8526°, -35.1327°], 17 September 1979, P . Martins et al. s.n. ( EAC 6936 , UFP 7218 ) . Pernambuco: Igarassu, Refúgio Ecológico Charles Darwin , 07°48’37”- 07°49’27”S, 34°27’25”- 34°56’52”W, 18 October 1999, A. C. P . Santiago 38 (PEUFR). Bahia: Jacobina, Monte Taboa , ca. 2 km da cidade, 11°11’26”S, 40°30’33”W, 656 m, 3 August 2001, F. R . Nonato et al. 927 ( HUEFS, SP, VIC) .

Remarks: —Apart from us, some authors from the 19 th Century had recognized this taxon as distinct from the other South American brackens, for example: Schrader (1824 —as Pteris campestris ), Presl (herbarium identifications—as Aquilina gardneri ), and Ettingshausen (1864, 1865 —as Pteris gardneri and A. gardneri ).

Pteridium arachnoideum subsp. campestre is a smaller taxon than P. arachnoideum subsp. arachnoideum s. str., forming much smaller thickets. It has smaller fronds (1–1.5 × 0.6–1 m vs. 2–3 × 1.3–1.8 m), 3-pinnate-pinnatifid laminae (vs. 3–4-pinnate-pinnatifid), pinnae and pinnules without free lobes between the distal segments (vs. free lobes always present), compound distal segments equilateral, regularly dissected, not caudate at apex (vs. inequilateral, irregularly dissected and caudate at apex), simple distal segments up to 1(–1.5) cm long (vs. to 3(–4) cm long), costules abaxially slightly flattened (vs. strongly flattened, with wing-like appearance), veins abaxially slightly raised and hirsute, with stiff acicular hairs, 0.2–0.3 mm long (vs. strongly raised and lanose, with lax arachnoid hairs, 0.6–0.8 mm long), laminar tissue between the veins abaxially with farinose appearance, not visible, copiously furnished with gnarled hairs (vs. without farinose appearance, visible and glabrous), infertile pseudo-indusia 0.3–0.4 mm wide with the marginal cells vertical (vs. 0.2–0.3 mm wide, marginal cells horizontal) ( Figs. 1A–C , 2E–G vs. Figs. 1D–F , 2B, C , and see also Ettingshausen 1865: t. 53, 54).

Pteridium caudatum also occurs in Brazil but is restricted to the Amazonian region in the north-west ( Tryon 1941, Prado & Moran 2009). Besides geography and the distinguishing characteristics given in the key, P. arachnoideum subsp. campestre differs from P. caudatum by compound distal segments equilateral, regularly dissected and not caudate at apex (vs. inequilateral, irregularly dissected and caudate), and by simple distal segments which are up to 1(–1.5) cm long (vs. to 4(–7) cm long) ( Figs. 1A–C , 2E–G ).

Pteridium arachnoideum subsp. campestre differs from P. aquilinum subsp. pseudocaudatum ( Clute 1900: 39) Hultén (1941: 44) by compound distal segments equilateral, regularly dissected and not caudate at apex (vs. inequilateral, irregularly dissected and caudate), simple distal segments that are up to 1(–1.5) cm long (vs. to 3 cm), and laminar tissue between the veins that is abaxially furnished with gnarled hairs (vs. glabrous). Finally, Pteridium arachnoideum subsp. campestre differs from P. aquilinum subsp. feei (W. Schaffn. ex Fée 1857: 73) Thomson et al. (2008: 13) by laminar tissue between the veins abaxially furnished with gnarled hairs (vs. glabrous) and infertile pseudo-indusia with glabrous margins (vs. margins ciliate) ( Figs. 1A–C , 2E–G ).

Figures

FIGURE 1. A–C. Pteridium arachnoideum subsp. campestre: A. pinnule (Nonato 927), B. segment, abaxially (Schwartsburd 2411), C. segment, cross section, abaxial side up, showing veins abaxially with stiff acicular hairs, and laminar tissue between the veins abaxially with gnarled hairs (Schwartsburd 2411), D–F. Pteridium arachnoideum subsp. arachnoideum s. str.: D. pinnule (Schwartsburd 2490), E. segment, abaxially (Schwartsburd 2490), F. segment, cross section, abaxial side up, showing veins abaxially with lax arachnoid hairs, and laminar tissue between the veins abaxially glabrous (Schwartsburd 2490). “s.d.s.”: simple distal segments, “c.d.s.”: compound distal segments. Drawn by R. Pinto.

FIGURE 2. Light microscopy of specimens of Pteridium subjected to diaphanization:A–C: P. arachnoideum subsp. arachnoideum s. str. (Schwartsburd 2255), D–G: P. arachnoideum subsp. campestre (Schwartsburd 2411). A, D: stomatal guard-cells, pointed by black arrows, B, E: veins (“V”) and laminar tissue between the veins, abaxially (glabrous in P.arachnoideum subsp. arachnoideum (B), and obscured by gnarled hairs in P. arachnoideum subsp. campestre (E)), C, F: margins of the infertile pseudo-indusia. G: detail of a gnarled hair, pointed by black arrow. Bars = 50µm for all micrographs. Photograph by K.L.B. Lopes-Mattos.

FIGURE 3. Distribution of Pteridium taxa in eastern South America. Black circles: P. arachnoideum subsp. arachnoideum s. str., white triangles: P. arachnoideum subsp. campestre, A. Scheme of the Dry Diagonal (shaded area, by R. Pinto) in South America. B. Detailed distribution of Pteridium taxa in north-eastern Brazil, elevation in gray scale (from white to black) for each 500 m.