Borreria heteranthera E.L. Cabral & Sobrado

Sobrado, Sandra V. & Cabral, Elsa L., 2015, Intraspecific variation of insertion / length of stamens in homostylous flowers of a new species and three other species of Borreria: an unusual case in Rubiaceae, Phytotaxa 206 (1), pp. 53-73 : 59-69

Borreria heteranthera E.L. Cabral & Sobrado , sp nov. ( Figs. 1 A–C , 3 A–L , 4 A–C , 9 A–C )

Type: — BRAZIL, Pará, Canaã dos Carajás, S 11A, 6°20’47” S, 50°25’52” W, 737 m, 25 April 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 1099 (holotype BHCB 158091!; isotype CTES!).

Borreria heteranthera is similar to B. semiamplexicaule in being an annual herb, with two pairs of unequal involucral bracts, and papillate seeds; the former differs from the latter in having non-sheathing bracts (vs. sheathing in B. semiamplexicaule ), the external pair of bracts 9–40 (50) × 1–10 mm (vs. 8–27 × 2–3.5 mm), the internal pair of bracts 4–10 (12) × 0.5–3 mm (vs. 4.4–8 × 2–3.2 mm), and two long and two short filaments (vs. two long filaments and two subsessile anthers).

Annual erect herb, (15–) 20–50 cm tall; stems with (2–)4–5 opposite lateral branches or rarely simple, subquadrangular at the base, quadrangular and winged in young growth, glabrous, internodes 4–8 cm long. Stipular sheaths 2–4 mm long, scabrid to puberulous; setae (4–)5, 1–4 mm long, glabrous and colleter-tipped. Leaves opposite, pseudo-petiolate; blades ovate to elliptic, 25–50(–70) × 8–10(–20) mm, attenuate at base, acute at apex, membranaceous, glabrous above, puberulous or scabrid underneath, margin scaberulous, main nerve weakly marked; secondary veins inconspicuous. Inflorescences with 1 terminal and 1–2(–3) axillary glomerules, on principal stems and opposite lateral branches, pauciflorous; bracts 4, unequal, not sheathing, the larger and external pair of bracts 9–40(–50) × 1–10 mm, the smaller and internal pair of bracts 4–10(–12) × 0.5–3 mm. Flowers 4-merous, subsessile (pedicels 0.4–0.5 mm long). Hypanthium obpiriform, 1–1.5 mm long, scabrulous. Calyx lobes subtriangular, 1–2.5 mm long, with external side and margins scabrulous, with vinaceous hairs. Corolla infundibuliform, 2–4 mm long, white, yellow-green when dry; tube 2.3–2.8 mm long, externally glabrous, internally with a ring of moniliform hairs near the base; lobes triangular, 0.8–2 mm long, shorter than the tube, with 2–3 teeth at the apex outside, with a few scattered moniliform hairs at base inside. Stamens exserted, filaments dimorphic, inserted at the sinuses of the corolla lobes, papillate, the 2 longer filaments 0.5–1 mm long, the 2 shorter filaments 0.25–0.5 mm long; anthers oblong, 0.4–0.6 × 0.3–0.4 mm. Style exserted, 3–5 mm long, bifid, style branches 0.5–1 mm long, papillate; nectary disc bipartite. Capsules subsessile (pedicels 0.6–1 mm long), ovoid, 1.5–2 × 1.7–2 mm, glabrous, with 2 septicidally dehiscent valves. Seeds ovoid, 1.5–1.6 × 0.6–0.7 mm, dark brown; dorsal surface convex, ventral surface with a deep groove, covered by hyaline strophiole and some sparse raphids; testa reticulo-papillate, cells digitate, periclinal walls convex with a subcircular depression and a little excrescence at the apex, anticlinal walls curved or sinuous ( Fig. 9 A–C ).

Distribution:— Borreria heteranthera is endemic to Serra dos Carajás , an isolated mountain range on the eastern Amazon area, in Pará State, Brazil. It grows particularly at the Serra Norte and Sul from Parabuapebas and Canaã dos Carajás municipalities.

Ecology and Phenology: —Growing in campos ruprestres and gramineous flat fields on canga, and in shrubby vegetation with iron-rich rocks outcrops, on mountain summits, at 600–800 m elevation; flowering and fruiting from February to May. The vegetation of this area is characterized by evergreen, semideciduous, and deciduous forests, and by patches of saxicolous shrubby vegetation called canga ( Secco & Mesquita 1983) or campos rupestres (i.e., rochy outcrops; Silva et al. 1996).

Conservation status: —According to the IUCN criteria ( IUCN 2012) Borreria heternathera should be classified as endangered [EN B2ab(ii, iii, iv)]. The extent of occurrence (EOO) is calculated to be 15.424 km 2, and the area of occupancy (AOO) is estimated at 20.000 km 2 (cell sized 2 km) in a fragmented area. The species is known from several localities, representing two locations from the northern of Pará State. The region where Serra dos Carjás is located is experiencing mining activity, especially linked to the exploitation of ferrous material, threatening the local natural vegetation.

Additional specimens examined:— BRASIL. Pará: Canaã dos Carajás : Serra Sul, Corpo B, 6°21’19” S, 50°23’26” W, 700 m, 19 March 2009, P. L. Viana, L. M. Versieux, L. C. Garcia, V. T. Giorni, L. V. C. Silva & D. S. Silva 4150 (BHCB); Corpo D, 6°23’54” S, 50°22’12” W, 700 m, 17 March 2009, P. L. Viana, L. M. Versieux, L. C. Garcia, V. T. Giorni, L. V. C. Silva & D. S. Silva 4094 (BHCB); Serra do Tarzan, 6°19’12” S, 50°6’3” W, 600–800 m, 19 February 2010, L. V. Costa, D. T. Souza, A. J. Arruda, F. Dayrell, F. Costa & T. Aaimeida 819 (BHCB); S11-A, 6°19’5” S, 50°26’44” W, 735 m, 27 March 2012, A. J. Arruda, P. L. Viana, F. M. Santos, P. B. Mayer, T. J. Battituci & L. J. Arruda 909 (BHCB); S11-A, 6°20’47” S, 50°25’52” W, 737 m, 25 April 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 1098 (BHCB, CTES). Parauapebas: Flona dos Carajás, Serra Sul –S11, Corpo D, 6°23’40” S, 50°21’51” W, 733 m, 20 March 2012, P. L. Viana, F. S. Marino, A. J. Arruda, T. B. Jorge & P. M. Burkowski 5226

(BHCB, CTES); N4 -WS, 6°4’24” S, 50°11’35” W, 554 m, 24 March 2012, A. J. Arruda, P. L. Viana, F. M. Santos, P. B. Mayer, T. J. Battituci & L. J. Arruda 822 ( BHCB, CTES) ; N4 -WS, 6°4’22” S, 50°11’42” W, 505 m, 24 March 2012, A. J. Arruda, P. L. Viana, F. M. Santos, P. B. Mayer, T. J. Battituci & L. J. Arruda 826 ( BHCB, CTES) .

Borreria hispida Spruce ex K. Schum. , in Mart., Fl. Bras. 6(6): 62. 1888. Spermacoce neohispida Govaerts, World Checkl. Seed Pl. 2(1): 18. 1996. Type :— BRAZIL. Pará: Santarem, April 1850, R. Spruce 663 (lectotype M!, designated here; Isolectotypes BM!, FI (JSTOR-image)!, K (JSTOR-image)!, MPU (JSTOR-image)!, NY!, RB!, R!, S (JSTORimage)!, TCD (JSTOR-image)!, W!. ( Figs. 1 D–F , 2 A–B , 5 A–J , 9 D–F ).

Borreria hispida Spruce ex K. Schum. var. glabrescens K. Schum. in Mart., Fl. Bras. 6(6): 62. 1888. Type:— BRAZIL. “Goyaz prope Porto Real” [now Tocantins: Porto Nacional], s.d., W. J. Burchell 8675 (lectotype NY, designated by Delprete (2010: 1221); isolectotypes BR!, F!).

Annual erect o rarely semi-prostrate herb, 7–30 cm tall; stems ramose at the base or simple with 4–5 opposite lateral branches, tetragon, slightly winged, glabrous with tiny papilla at the angle or densely hispid at the young braches, internodes 10–20(–40) mm long. Stipular sheaths subtriangular, 1–4 mm long, glabrous or hispid; setae 4–5, 1–4 mm long, hispid and colleter-tipped. Leaves opposite or sometimes pseudoverticillate (due to axillary brachiblasts), sessile or rarely pseudopetiolate; blades linear-lanceolate to lanceolate, 5–19(–30) × 1–7(–9) mm, attenuate at base, acute at apex, papery, glabrous, puberulous to pubescent above, densely pilose below, principally on secondary veins, margins revolute, scabrous. Inflorescences with 1 terminal and 4–5 axillary glomerules, on principal stems and opposite lateral branches, pauciflorous; bracts 4(–6), unequal, not sheathing, ovate-lanceolate, base subcordate, the larger and external pair of bracts 6–10 × 2–4 mm, 2–4, the smaller internal bracts 4–8 × 1–3 mm long, absent in axillary glomerules. Flowers 4-merous, subsessile (pedicels 0.1–0.2 mm long). Hypanthium obconic, 0.75–0.8 mm long, glabrous, puberulous or with sparse hispid hairs. Calyx lobes lanceolate to triangular, 1–3 mm long, glabrous, scabrulous or hispid, with hyaline apiculus, 0.5–0.65 mm long. Corolla infundibuliform, 2.25–2.5 mm long, white; tube 1–2 mm long, glabrous outside, with a ring of moniliform hairs at 1/3 from the base inside; lobes triangular, 0.5–1 mm long, with 2–3 teeth at the apex outside. Stamens exserted, with dimorphic filaments, the 2 longer filaments inserted at the sinuses of the corolla lobes, 0.3–0.5 mm long, the 2 shorter filaments inserted at the top of the corolla tube, 0.05–0.1 mm long, anthers oblong 0.35–0.3 × 0.25– 0.2 mm. Style exserted, 1–2 mm long, bifid; style branches 0.45–0.8 mm long, stigmatic surface papillate; nectary disc bipartite. Capsules subsessile (pedicels 0.2–0.8 mm long), subglobose, 0.8–2 × 0.9–1 mm, hispid at the sepals, with 2 septicidally dehiscent valves. Seeds oblong, 0.6–0.8 × 0.3–0.4 mm, round at both ends, base acuminate, dark brown; dorsal surface convex, ventral surface flat with a broad groove covered by strophiole exceeding the apex of the seed with some raphids; testa surface papillate, cells digitate, periclinal wall convex with rounded ends, anticlinal walls sinuous ( Fig. 9 D–F ).

Distribution:—Central and northern Brazil, French Guiana, Guyana, Suriname and Venezuela; at 800–1000 m elevation.

Ecology and Phenology: —Open grasslands, savannas and rocky fields or granitic outcrops, occasionally along roadsides. Flowering and fruiting from November to July.

Remarks:— Schumann (1888) described Borreria hispida and cited two collections in Flora Brasiliensis: Leprieur s.n. from French Guiana, and Spruce 663 from Pará, Brazil. The specimen collected by Leprieur could not be located in this study. Spruce 663 at the Martius herbarium in Munich (M) is well-preserved and has at least 10 duplicates distributed in numerous herbaria. For this reason, we select Spruce 663 at M as the lectotype of this taxon. Besides this, we consider important to remark a controversial situation about the Spruce collection number cited in the protologue of the species. The label of the M specimen has the number “ 663 ” handwritten with a different calligraphy (author unknown) from the original dates. Also, the label has the signature and the annotation “K. Schum.!”. This proves that Schumann saw this specimen, and cited this number in the species protologue. However, not all the available specimens of Spruce collected in “ Prope Santarem, Pará, Brazil, April of 1950 ” has the same number written in its labels (i.e. JSTOR images from FI, K, MPU, S, and TCD herbaria). Also, the BM and NY specimens have labels annotated with this different calligraphy. Taking into account this handwritten annotation from all specimens analyzed, we think that this number does not correspond to Spruce’s collection number. However, we preferred to maintain 663 as Spruce’s collection number because its extensive use in the literature.

Conservation status: —According to the area of occupancy estimated (AOO: 152,000 km 2; cell size 2 km) and following the IUCN criteria (2012), Borreria hispida should be considered as least concern. This is a widespread and well-collected species in several locations from open grasslands and granitic outcrops of the Guianas, Brazil, and Venezuela. The extent of occurrence (EOO) is calculated to be 4,836,460.459 km 2.

Additional specimens examined:— BRASIL. Amapá: Rio Araguari, 20 September 1961, J. M. Pires, W. Rodrigues & G. C. Irvine 51129 (NY); Road to Amapá, 0°17’ N, 51°5’ W, 7 July 1962, J. M. Pires & P. B. Cavalcante 51970 (IAN, NY); Estrada de Curiaú, Macapá, 22 June 1982, B. V. Rabelo & R. Non 1607 (F, UB); 8 April 1982, N. A. Rosa, M. R. Santos & S. S. Silva 4183 (INPA, MG, NY). Amazonas: Rio Negro, June 1910, E. H. G. Ule 8974 (F, MG). Goiás: 10 km S of Guará, 550 m, 18 March 1968, H. S. Irwin, H. Maxwell & D. C. Wasshausen 21332 (NY); idem, H. S. Irwin, H. Maxwell & D. C. Wasshausen 21338 (MO, NY); Pirenópolis, Serra dos Pireneus , 15°49’22” S, 48°53’20” W, 1040 m, 18 March 2006, P. G. Delprete, V. L. Gomes-Klein & O. Yano 9538 (NY, RB); idem, 15°47’59” S, 48°53’51” W, 1070 m, 19 March 2006, P. G. Delprete, V. L. Gomes-Klein & O. Yano 9616 (NY). Maranhão: Balsas, 7°35’ S, 46°5’ W, 300 m, 21 March 1997, R. C. Oliveira & G. P. da Silva 601 (CTES, HEPH); idem, Condominio Kissy Lote 23, 20 March 1999, G. Pereira-Silva 4122 (CEN, CTES, JPB). Pará: Jari, Agua Branca, km 3, 28 July 1969, N. T. da Silva 2499 (NY, UB); Santarum, 21 June 1910, A. Ducke 23140 (MG, RB); Guarai, Rod. Belem-Brasilia, 30 March 1976, G. Hatschbach 38507 (MBM); Itaituba, estrada Santarém-Cuiabá, BR 163, km 771, 9°37’ S, 54°35’ W, 22 April 1983, I. L. Amaral, N. Silva, O. P. Monteiro, J. Lima, L. Brako, W. D. Reese & M. Dibben 878 (INPA, MG, NY, RB); Santarém, Alter do Chão, 21 May 1910, A. Ducke 10796 (F, MG, RB); idem, 8 June 1987, W. E. Magnusson & I. S. Miranda s.n. (INPA 163.615); idem, 23 June 1988, I. S. Miranda s.n. (INPA 163.614); Serra do Cachimbo, 320 m, 20 February 1977, J. H. Jr. Kirkbride & E. Lleras 2953 (MO); Guajara Mirim, 10°44’ S, 65°15’ W, 10 April 1987, M. Nee 34766 (INPA, MO); Ji-Paraná, Reserva Biológica do Jaru, 2°37’12.07” S, 61°36’53.39” W, 4 May 2006, J. F. Ramos & A. M. G. Anjos 2909 (INPA). Tocantins: ca. 15 km S of Araguaína, 300 m, 15 March 1968, H. S. Irwin, H. Maxwell & D. C. Wasshausen 21195 (F, MG, NY, RB); Lagoa da Confusão, Ilha do Bananal, 10°27’5” S, 50°29’58” W, 270 m, 20 March 1999, M. A. Silva, A. D. dos Santos, A. Pires da Silva, N. R. Oliveira, N. G. Souza, R. C. Mendonça & E. Cardoso 4010 (NY); idem, 265 m, 21 March 1999, M. A. da Silva, R. C. Mendonça, N. G. Souza, N. R. Oliveira & E. Cardoso 4033 (NY). GUYANA. East Berbice–Corentyne Region, S Awara Savanna, 5°43’ N, 57°32’ W, 1–25 m, 18 December 1986, J. J. Pipoly, G. Gharbarran & G. Bacchus 9380 (MO); 5°33’ N, 57°40’ W, 10–20 m, 29 October 1989, L. J. Gillespie, C. Kelloff & S. Tiwari 2532 (MO, NY); Rupununi, Dadanawa, 2°49’ N, 59°31’ W, 120 m, 6 June 1995, M. J. Jansen -Jacobs, B. J. H. ter Welle, C. Gustafsson & V. James 3929 (F). FRENCH GUIANA. Kourou, 8 April 1985, C. Feuillet 1657 (MO, P). SURINAME. Saramacca, Tibiti savanne, 13 January 1949, J. Lanjouw & J. C. Lindeman 1799 (NY, U); idem, 20 May 1976, L. B. B. Tenuissen 16144 (U); Sipaliwini Savanna, 24 August 1966, J. van Donselaar 3562 (U). VENEZUELA. Anzoátegui: Bolívar, 10°2’ N, 64°17’ W, 1100 m, 24 November 1981, G. Davidse & A. C. González 19334 (NY, MO). Amazonas: Savanna of Atures, 31 July 1887, A. Gaillard 229 (F, P); vicinity of Sanariapo, near Río Sanariapo, 100 m, 8 September 1944, J. A. Steyermark 58458 (F); Atures, 5°48’ N, 67°20’ W, 80 m, 23 September 1980, O. Huber 5713 (NY); idem, 19 August 1980, O. Huber 5608 (NY); Puerto Ayacucho, 5°39’ N, 67°38’ W, 100 m, 22 November 1984, T. B. Croat 59218 (MO); idem, 23 November 1984, R. L. Liesner 17230 (NY, MO); Atures, 5°34’ N, 67°35’ W, 21 July 1993, A. Gröger 986 (M). Apure: Puerto Paez, 200 m, 12 September 1944, J. A. Steyermark 58533 (F). Bolívar: Cedeño, 6°15’ N, 67°45’ W, 18 April 1984, B. Stergios, D. Taphora & L. Nico 7223 (MO); idem, 7°36’ N, 66°15’ W, 100–200 m, 2 September 1985, J. A. Steyermark, B. Holst & B. Manara 131230 (MO); idem, 4°30’ N, 61°30’ W, 850 m, 1 November 1985, R. L. Liesner 19285 (MO); Gran Sabana, between Kun and waterfall at Ruémerú, south of Mount Roraima, 1065 m, 2 October 1944, J. A. Steyermark 59168 (F, NY). Portuguesa: 9°18’30” N, 69°42’ W, 500 m, 3 November 1982, Anonymous 127263 (MO 3111618); idem, 9°8’ N, 69°42’ W, 900 m, 8 September 1985, B. Stergios, G. Aymard, O. Hubber & W. Morawertz 8709 (MO). Yaracuy: 4 km N of Salom, 1000 m, 20 October 1982, G. Davidse, R. Liesner & J. A. Steyermark 20778 (MO).

Borreria semiamplexicaule E.L. Cabral, Bonpandia 9: 37. 1996. Spermacoce semiamplexicaule (E.L. Cabral) Delprete, J. Bot. Res. Inst. Texas 1(2): 1028. 2007. Type:— BRAZIL, Pará, 25 km NW of camp at Serra Norte, approx. 5°54’ S, 50°27’ W, 13 December 1981, D. Daly, R. Callejas, M. G. da Silva, E. Taylor, C. Rosario & M. dos Santos 1993 (holotype: NY!; isotype: CTES!). ( Figs. 1 G–H , 2 C , 6 A–M , 7 A–F , 9 G–I ).

Annual herb, erect, 15–50 cm tall; stems simple or with opposite lateral branches starting from the base, subtetragonal, slightly winged, glabrous, internodes 3–8 cm long. Stipular sheaths 2–4 mm long, puberulous at the upper third; setae 4–6, 0.8–3 mm long; stipular sheath from the terminal glomerule with 3–4 setae. Leaves opposites, sessile; blades elliptic to linear, 10–40 × 2–12 mm, attenuate at base, acute at apex, membranaceous, margin with rough papillae, midrib conspicuous on the lower surface, secondary veins less evident. Inflorescences with 1 terminal and 2–6 axillary glomerules, pauciflorous; bracts 4–6, unequal, sub-sheathing to sheathing, base cordate to auriculate, the 2 larger external bracts 8–27 × 2–3.5 mm, the 2–4 smaller internal bracts 4–8 × 2–3 mm. Flowers 4-merous, subsessile (pedicels 0.35 mm long). Hypanthium obconic, 1.12–1.33 mm long, glabrous. Calyx lobes triangular, 1–3 mm long, margins with rough papillae or with red scabrous hairs. Corolla infundibuliform, 4–4.5 mm long, pale blue, rare white; tube 3.5–4.4 mm long, glabrous outside, with a ring of moniliform hairs near the base inside; lobes triangular, 1.2–1.4 mm long, externally with 2–3 tooth on the apex, with sparse moniliform hairs inside. Stamens exserted, filaments dimorphic, inserted at the sinuses of the corolla lobes, the 2 longer stamens with filaments 0.82–1 mm long, the 2 shorter stamens with subsessile anthers, these oblong, 1–1.2 × 0.23–0.35 mm. Style exserted, 3–4 mm long, stigma bifid, stigmatic branches 0.3–0.8 mm long, papillate; nectary disc bipartite. Capsules subsessile (pedicels 0.34–0.44 mm long), ovoid, 2.2–2.8 × 2–2.7 mm, glabrous, with 2 septicidally dehiscent valves. Seeds ovoid, 1.5–2 × 0.7–0.85 mm, blackish to dark brown; dorsal surface convex, ventral surface with a groove covered by a hyaline strophiole; testa surface reticulo-papillate, cells digitate. The cells have warty irregular projections with a subcircular depression at the apex ( Fig. 9 G–I ).

Distribution:—In the states of Pará, Goiás, Tocantins, and Mato Grosso, Brazil; at 200–800 m elevation.

Ecology and Phenology: —Flooded grassy fields, campos rupestres on ferrous rocky outcrop, in transitions between low forests to ombrophilous dense forest, near water courses, and also on lateritic soils. Always associated with marsh and wetlands. Flowering and fruiting from February to (probably) June.

Remarks:—This species was originally known from Pará and was recently reported by Delprete (2010) to occur in northern of Tocantins, Brazil. The specimen from Mato Grosso is the first record of this species for this state.

Conservation status: —The extent of occurrence (EOO) is calculated to be 368,675.3 km 2, and the area of occupancy (AOO) is estimated at 68.000 km 2 (cell size 2 km). Therefore, following IUCN red list categories and criteria ( IUCN 2012), Borreria semiamplexicaule should be regarded as endangered [EN B2ab(ii, iii, iv)]. The planned mining activities, mainly in the area of Serra dos Carajás (Pará), are the main threat for the species. Moreover, is important to mention that the excessive farming activity in all other locations is also considering a threat for the species. This is presumed due to the soil quality that enables such activities.

Additional specimens examined:— BRASIL. Mato Grosso: Alta Floresta, 9°00’ S, 55°00’ W, 246 m, 27 January 2007, D. Sasaki, C. P. Vicenti, L. M. Paz & J. H. Piva 1426 (INPA); Santa Cruz do Xingu, 9°4’25” S, 52°36’33” W, 266 m, 3 March 2011, D. C. Zappi, E. Lucas, S. Frisby, W. Milliken, D. R. Silva, C. R. A. Soares, A. F. Forte & J. H. Piva 3069 (RB); idem, D. C. Zappi, E. Lucas, S. Frisby, W. Milliken, D. R. Silva, C. R. A. Soares, A. F. Forte & J. H. Piva 3073 (RB). Pará: Marabá, Serra dos Carajás, Serra Norte , 21 May 1969, P. Cavalcante 2083 (MG); idem, 6°00’ S, 50°18’ W, 700 m, 21 May 1969, P. Cavalcante 2094 (MG, NY); idem, 18 April 1970, P. Cavalcante & M. Silva 2618 (NY); idem, 20 August 1973, J. M. Pires & B. C. Passos 13197 (RB); idem, 2 June 1983, N. F. F. Silva, N. A. Rosa, R. P. Bahía & J. C. Santos 1332 (INPA, MG); idem, N-4, 14 March 1984, A. S. L. da Silva, N. A. Rosa, R. P. Bahia & M. R. Santos 1762 (INPA, MG, NY); idem, 15 March 1984, A. S. L. da Silva, N. A. Rosa, R. P. Bahia & M. R. Santos 1816 (MO, NY); idem, 24 April 1985, N. A. Rosa, M. F. da Silva, R. Salamão & R. P. Bahia 4701 (MG); idem, 4 February 1985, Nascimiento O. C. & R. P. Bahia 1155 (MG); idem, 3 June 1986, P. M. de Lima Marli & G. M. Barroso 122 (RB). Conceição do Araguaia: approx. 8°3’ S, 50°10’ W, 350–620 m, 11 February 1980, T. Plowman, G. Davidse, N. A. Rosa, C. S. Rosário & M. R. dos Santos 8407 (MO); idem, approx. 8°2’ S, 50°4’ W, 200 m, 21 February 1980, T. Plowman, G. Davidse, N. A. Rosa, C. S. Rosário & M. R. dos Santos 8971 (MG, MO). Canaã dos Carajás : N1, Floresta Nacional dos Carajás , 600–800 m, 19 February 2010, L. V. Costa, D. T. Souza, A. J. Arruda, F. Dayrell, F. Costa & T. Aaimeida 830 (BHCB); idem, L. V. Costa, D. T. Souza, A. J. Arruda, F. Dayrell, F. Costa & T. Aaimeida 840 (BHCB); S11-A, 6°20’48” S, 50°25’57” W, 711 m, 21 March 2012, A. J. Arruda, P. L. Viana, F. M. Santos, P. B. Mayer & T. J. Battituci 759 (BHCB, CTES); 6°23’32” S, 50°22’18” W, 20 March 2012, P. M. Burkowski, A. J. Arruda, P. L. Viana, F. M. Santos & T. J. Battituci 1127 (BHCB); Serra Sul, 6°19’6” S, 50°27’9” W, 673 m, 21 March 2012, P. M. Burkowski, A. J. Arruda, P. L. Viana, F. M. Santos & T. J. Battituci 1144 (BHCB); S11B, 6°20’32” S, 50°25’4” W, 724 m, 25 April 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 1095 (BHCB). Parauapebas: Flona dos Carajás, Corpo A , 6°19’4” S, 50°26’44” W, 735 m, 21 March 2012, P. L. Viana, F. S. Marino, A. J. Arruda, T. B. Jorge & P. M. Burkowski 5257 (BHCB, CTES); 6°23’33” S, 50°21’25” W, 730 m, 22 March 2012, P. L. Viana, F. S. Marino, A. J. Arruda, T. B. Jorge & P. M. Burkowski 5269 (BHCB, CTES); Serra Norte-N7, 6°9’27” S, 50°10’12” W, 699 m, 22 March 2012, P. L. Viana, F. S. Marino, A. J. Arruda, T. B. Jorge & P. M. Burkowski 5306 (BHCB); Serra Norte, 6°11’8” S, 50°7’56” W, 23 March 2012, P. M. Burkowski, A. J. Arruda, P. L. Viana, F. M. Santos & T. J. Battituci 1175 (BHCB); 6°11’8” S, 50°7’56” W, 23 February 2012, P. M. Burkowski, A. J. Arruda, P. L. Viana, F. M. Santos & T. J. Battituci 1178 (BHCB); 6°5’43” S, 50°11’29” W, 24 March 2012, P. M. Burkowski, A. J. Arruda, P. L. Viana, F. M. Santos & T. J. Battituci 1187 (BHCB); 6°1’52” S, 50°17’25” W, 688 m, 26 March 2012, P. M. Burkowski, A. J. Arruda, P. L. Viana, F. M. Santos & T. J. Battituci 1235 (BHCB); 6°1’52” S, 50°17’25” W, 688 m, 26 March 2012, P. M. Burkowski, A. J. Arruda, P. L. Viana, F. M. Santos & T. J. Battituci 1239 (BHCB); N1, 6°00’49” S, 50°17’51” W, 683 m, 19 April 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 926 (BHCB); 6°00’49” S, 50°17’51” W, 683 m, 19 April 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 928 (BHCB); N2, 6°3’35” S, 50°14’50” W, 690 m, 19 April 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 958 (BHCB, CTES); N3, 6°2’30” S, 50°12’28” W, 694 m, 27 March 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 966 (BHCB); N4-WS, 6°4’17” S, 50°11’5” W, 738 m, 23 March 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 786 (BHCB); 6°4’17” S, 50°11’5” W, 738 m, 23 March 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 790 (BHCB); 6°6’8” S, 50°11’9” W, 717 m, 21 April 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 966 (BHCB); N3, 6°1’44” S, 50°12’7” W, 656 m, 21 April 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 1003 (BHCB); N1, 6°1’54.6” S, 50°17’19.08” W, 25 May 2012, L. V. Costa, A. J. Arruda, M. O. Pivari & A. O. Santos 967 (BHCB); N6, 6°7’50” S, 50°10’27” W, 697 m, 25 March 2012, A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 846 (BHCB); Santarém, 2°29’7” S, 54°48’35” W, 15 April 2005, J. G. Jardim, S. H. N. Monteiro, R. P. Oliveira & J. B. F. da Silva 4530 (HUEFS).

Borreria xanthophylla Bremek., Recueil Trav. Bot. Néerl. 31: 306. 1934.— Spermacoce xanthophylla (Bremek.) Govaerts, World Check. Seed Pl. 2: 19. 1996. Type:— SURINAME, Litanie River, Mount Teeboe, 9 August 1904, Versteeg 784 (holotype: U 0007599! [digital image!], isotype: U U0007600 [digital image!], photo MO!). ( Figs. 1 J–L , 2 D , 8 A–N , 9 J–L ).

Annual herb, 10–20 cm tall; stems creeping or occasionally erect, 30–60 cm long, 3–5 opposite lateral branches, subquadrangular to tetragonal, winged, glabrous or sometimes hispid at the angles of young branches; internodes 5–9 cm long. Stipular sheaths triangular, 1.25–3 mm long, hispid to villous; setae 3–4, 1–4 mm long, villous, the central ones longer, colleter-tipped. Leaves opposite, pseudo-petiolate; blades ovate, 25–70 × 8–20 mm, attenuate at base, acute at apex, chartaceous, margins scabrous, pubescent above and underneath. Inflorescences with 1 terminal and 3–4 axillary glomerules, on principal stems and on opposite lateral branches; glomerules multi-flowered; bracts 6–8, unequal, sheathing and covering all the glomerules, pseudo-petiolate, foliaceous pubescent, the 4 larger external bracts, ovate, 11–16 × 11–14.5 mm; the 2(–4) smaller internal bracts suborbicular or elliptic, 8–12 × 5–11 mm. Flowers 4-merous, subsessile (pedicels 0.5–0.6 mm long). Hypanthium narrowly ovate, 1.5–2 mm long, with sparse hispid hairs. Calyx lobes triangular, 0.8–1.2 mm long, united at base in a short tube, 0.55–0.7 mm long, hispid. Corolla infundibuliform, 3.75–4 mm long, pale blue-purple; tube 2.2–3 mm long, glabrous outside, with a ring of moniliform hairs at lower third inside, lobes triangular, 0.7–1 mm long, with some papillae near the tips outside, with sparse hairs near the anther insertions inside. Stamens 4, unequal, the 2 longer ones slightly exserted, inserted at the corolla lobes sinuses, filaments 0.12–0.2 mm long, the 2 shorter ones included, inserted at 0.86–1 mm below the sinuses of the corolla lobes, anthers subsessile, oblong 0.5–0.6 × 0.44 mm. Style exserted, 3.35 mm long, stigma bifid, stigmatic branches 1.07 mm long, stigmatic surface papillate; nectary disc bipartite. Capsules subsessile (pedicels 0.6–1.5 mm long), oblong, 3.6 × 1.8–2 mm, hispid at the sepals, with 2 septicidally dehiscent valves. Seeds oblong-ellipsoid, 2.4–3.2 × 0.9–1.35 mm, round at both ends, brown; dorsal surface convex, ventral surface slightly flat with a longitudinal narrow groove forming a straight line from one end to the other; testa surface rugulose-papillate; cells digitate, periclinal walls convex and slightly striate at the round end, anticlinal walls curved or sinuous ( Fig. 9 J–L ).

Distribution:—Only known from French Guiana and Suriname; at 200–400 m elevation.

Ecology and Phenology: —Edges of shrubby vegetation on rocks, at the edges and on top of granitic inserbergs. Flowering and fruiting from July to December.

Conservation status: —According to the extent of occurrence calculated (EOO: 25,091.008 km 2) this species could be considered as a threatened species. However, the area of occupancy (AOO) is estimated at 28.000 km 2 (cell sized 2 km) in a severely fragmented area; besides, the species is known from nine collections from French Guiana. Therefore, following IUCN criteria ( IUCN 2012), the species can be referred to as an endangered (EN B2ab(ii, iii, iv).

Additional specimens examined:— FRENCH GUIANA. Savane du Rocher , 15 December 1914, R. Benoist 1507 (P) ; Frontière Guyane-Brésil , 13 April 1983, C. Feuillet 1011 ( MO) ; Pic du Grand Croissant, Basin de L’Armantabo , 3°31’ N, 52°22’ W, 150 m, 14 April 1993, J. J. de Granville 11748 ( MO) ; Montagne Emérillons , Région des Emérillons, 3°15’ N, 53°5’ W, 200 m, 17 May 1995, J. J. de Granville & G. Cremers 12942 ( MO, NY) ; Mitaraka Sud , sommet inselberg, 2°16’ N, 54°31’ W, 660 m, 5 March 2001, C. Sarthou 839 ( MO, NY) ; Monts d’Arawa : zone de la savane-roche centrale, 2°49’ N, 53°22’ W, 220 m, 4 July 2002, J. J. de Granville, F. Crozier & C. Sarthou 15017 ( BR, MO, NY) ; idem, “savane-roche” [inselberg] central, 2°49’ N, 53°22’ W, 200 m, 13 July 2002, J. J. de Granville, F. Crozier & C. Sarthou 15234 ( MO) ; Mont Saint-Marcel , zone centre-est du massif, 2°23’ N, 53°00’ W, 420 m, 19 July 2002, J. J. de Granville, L. Aliker & C. Sarthou 15349 ( MO) ; inserbergs du haut Marouini-A: Inselberg de la D.Z., 2°54’ N, 54°1’ W, 0.5 m, 20 June 2004, J. J. de Granville & F. Crozier 16244 ( MO) ; Nouragues Field Station , 4°5’ N, 52°41’ W, 120 m, 13 August 2004, S. A. Mori, T. Lobova, N. Pitcairn, C. Geiselman & B. Vlásákova 25775 ( MO) .

Figures

FIGURE 1. Scanning electron microscopy (SEM) micrographs of pollen grains. Borreria heteranthera (A–C from A. J. Arruda, P. L. Viana, F. M. Santos, P. B. Mayer, T. J. Battituci & L. J. Arruda 826). A. Equatorial view. B. Polar view. C. Detail of mesocolpium and a section of the colpus. Borreria hispida (D–E from R. Spruce 663; F from A. Gröger 986). D. Equatorial view. E. Polar view. F. Detail of mesocolpium and a section of the colpus. Borreria semiamplexicaule (G–H from P.M. Burkowski, A. J. Arruda, P. L. Viana, F. M. Santos & T. J. Battituci 1187; I from D. Daly, R. Callejas, M. G. da Silva, E. Taylor, C. Rosario & M. dos Santos 1993). G. Equatorial view. H. Polar view. I. Detail of apocolpium. Borreria xanthophylla (J–L from J. J. de Granville, F. Crozier & C. Sarthou 15017). J. Equatorial view. K. Polar view. L. Detail of apocolpium. Scale bar 10 μm.

FIGURE 2.Scanning electron microscopy(SEM)micrographsofthe pollen wallstratification,the innernexine surface andtheendoaperture morphology. A–B. Borreria hispida (from R. Spruce 663). A. Inside of pollen fragment with an endocingulum (EN) and nexine surface finely granular with broad and deep endocracks. B. Detail of a section of the endocingulum (EN) and the columellar infratectum (CI). C. Borreria semiamplexicaule (from D. Daly, R. Callejas, M. G. da Silva, E. Taylor, C. Rosario & M. dos Santos 1993). View of inner nexine surface finely granular with superficial irregular endocracks. Note the columellar infratectum (CI). D. Borreria xanthophylla (from J. J. de Granville, F. Crozier & C. Sarthou 15017). View of inner side of a portion of broken pollen showing the columellar infratectum (CI) and the finely granular inner nexine surface.

FIGURE 3. Borreria heteranthera E.L. Cabral & Sobrado. A. Habit. B. Stipular sheath. C. Terminal glomerule. D. Detail of external bract. E. Detail of internal bract. F. Flower. G. Hypanthium, style and stigma. H. Open corolla. I. Capsule. J. Internal view of mericarp to display septicidal dehiscence. K. Ventral view of seed. L. Dorsal view of seed. (A, B, F–H from P. L. Viana, L. M. Versieux, L. C. Garcia, V. T.Giorni, L. V. C. Silva & D. S. Silva 4094; C, I–L from A. J.Arruda, P.L. Viana, F.M. Santos, P. B. Mayer, T. J. Battituci & L. J. Arruda 909; D, E from A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 1099). Illustration by L. Simón.

FIGURE 4. Borreria heteranthera E.L. Cabral & Sobrado. A. Habit. B. Detail of terminal glomerule. C. Flowers. Photographs by A. J. Arruda.

FIGURE 5. Borreria hispida Spruce ex K. Schum.A. Habit. B. Stipular sheath. C. Terminal glomerule. D. Flower. E. Hypanthium, style and stigma. F. Open corolla. G. Capsule. H. Internal view of mericarp to display septicidal dehiscence. I. Ventral view of seed. J. Dorsal view of seed. (A–J from R. Spruce 663). Illustration by L. Simón.

FIGURE 6. Borreria semiamplexicaule E.L. Cabral. A. Habit. B. Stipular sheath. C. Terminal glomerule. D. Abaxial view of glomerule to display inflorescence bracts organization. E. Detail of external bract. F. Detail of internal bract. G. Flower. H. Hypanthium, style and stigma. I. Open corolla. J. Capsule. K. Internal view of mericarp to display septicidal dehiscence. L. Ventral view of seed. M. Dorsal view of seed. (A–C, G–I from Daly D. 1993, D–F from P. L. Viana, F. S. Marino, A. J. Arruda, T. B. Jorge & P. M. Burkowski 5269, L–M from P. L. Viana, F. S. Marino, A. J. Arruda, T. B. Jorge & P. M. Burkowski 5257, J–K from A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 928). Illustration by L. Simón.

FIGURE 7. Borreria semiamplexicaule E.L. Cabral. A. Flooded grassy fields with outcrop of ferrous rocks. B. Habit. C. Terminal glomerule. D. Detail of flower displaying the staminal organization. E. Terminal glomerule displaying the bipartite nectariferus disc. F. Detail of the sheathing bracts. Photographs A–D by P. L. Viana and E–F by A. J. Arruda.

FIGURE 8. Borreria xanthophylla Bremek. A. Habit. B. Stipular sheath. C. Terminal glomerule. D. Detail of terminal glomerule to display fruits. E–F. Detail of external bracts. G. Detail of internal bract. H. Flower bud. I. Hypanthium, style and stigma. J. Open corolla. K. Capsule. L. Internal view of mericarp to display septicidal dehiscence. M. Ventral view of seed. N. Dorsal view of seed. (A–N from J. J. de Granville, F. Crozier & C. Sarthou 15017). Illustration by L. Simón.

FIGURE 9. Scanning electron microscopy (SEM) micrographs of seeds. Borreria heteranthera (A–C from A. J. Arruda, P. L. Viana, F. M. Santos, P. B. Mayer, T. J. Battituci & L. J. Arruda 826). A. Dorsal view. B. Ventral view. C. Detail of the reticulo-papillate testa and digitate cells. Borreria hispida (D–F from W. J. Burchell 8675). D. Dorsal view. E. Ventral view. F. Detail of the papillate testa surface and digitate cells. Borreria semiamplexicaule (G–I from A. J. Arruda, F. M. Santos, L. J. Arruda & T. J. Battituci 1095). G. Dorsal view. H. Ventral view. I. Detail of the reticulo-papillate testa. Borreria xanthophylla (J–L from J. J. de Granville, F. Crozier & C. Sarthou 15017). J. Dorsal view. K. Ventral view. L. Detail of the rugulate-papillate testa and digitate cells. Scale bar 200 μm.