Croton hadrianii Baillon (1864: 313)

Sodré, Rodolfo Carneiro & Silva, Marcos José Da, 2018, Rediscovery of Croton hadrianii (Euphorbiaceae), a well distributed but longforgotten species in Brazilian Amazon, Phytotaxa 349 (2), pp. 141-151 : 142-149

Croton hadrianii Baillon (1864: 313) ( Figs. 1 , 2 )

Lectotype (designated here):— BRAZIL. Without locality, 1783–1792, A. R. Ferreira s.n. (comm. Étienne Geoffroy Saint-Hilaire) ( P 00623573 !, isolectotypes P 00623574 !, F 1039147 !).

Shrubs 0.5 − 2 m tall, erect, monoecious, erect, dichotomously branched; adult branches blackened, young branches yellow-greenish to ferrugineous, both covered with shortly stipitate stellate-porrect trichomes, indument tomentose to the touch; latex clear. Leaves usually alternate, subopposite or subverticillate near the dichotomies or in the terminations of the branches; stipules 0.2 − 0.6 × 0.3 − 0.5 mm, ovate, with subglobose or ovoid glands at the base, stellate-porrect trichomes on both surfaces; petioles 0.8 − 1.7 cm long, with two sessile acropetiolar patelliform glands, yellowish, 1.3 − 1.7 mm diam.; blades 4.6 − 14 × 2.3 − 5.5 cm, oval-lanceolate or lanceolate, less commonly oblong or elliptic, apex acute or discreetly acuminate, base obtuse, sometimes rounded, rarely acute, margin doubly crenulate or often serrulate, rarely serrate, with patelliform glands in the sinuses, directed towards the adaxial surface, membranaceous, slightly discolorous, adaxial surface dark green with sessile stellate-porrect trichomes, abaxial surface light green with stipitate stellate-porrect trichomes, indument tomentose to the touch; venation brochidodromous, with 5 − 8 pairs of secondary veins, impressed on both surfaces. Inflorescences 2 − 5.2 cm long, terminal or in dichotomy of branches, bisexual, with 2 − 4(− 6) pistillate flowers sparsely distributed in the proximal portion, numerous staminate flowers in the distal portion in cymules, with 1 − 4 flowers, and a short sterile zone between pistillate and staminate flowers or continuous along the inflorescence axis; staminate bracts 0.7 − 1.1 × 0.3 − 0.4 mm, triangular, lanceolate or linear; pistillate bracts 0.5 − 1.2 × 0.3 − 0.6 mm, ovate or oblong; both bracts with ellipsoid glands at the base, with stellate-porrect and multiradiate trichomes, the latter present on pedicels, external surface of the staminate calyx, both surfaces of the pistillate sepals, and gynoecium. Staminate flowers 5.3 − 6.4 mm long; pedicels 0.7 − 1.6 mm long; calyx 5-lobed, united in the basal 1/3 to 1/4 of their length, lobes 1.6 − 2 × 1 − 1.2 mm, oblong-ovate or triangular, apex acute; petals 5, 2.1 − 2.6 × 1.3 − 1.5 mm, oblong or elliptic, barbellate near the base on the internal surface, villous at the apex; stamens 9 − 11, 3.3 − 3.5 mm long, glabrous or villous on the base; disk with five segments ovate, yellowish. Pistillate flowers 5.5 − 8 mm long; pedicels 0.2 − 1 mm long; sepals 5 − 7, subequal, 2 − 5 × 0.8 − 2.9 mm, obovate or oblong, apex acute or obtuse, light green; petals 0.1 − 0.9 × 0.05 − 0.2 mm, lanceolate or linear, whitish, glabrescent; disk with five to seven segments; ovary 1.6 − 1.8 × 1.9 − 2.2 mm, subglobose; styles (2 −)4-fid, 4 mm long. Capsules 4.8 − 5 × 5 − 5.3 mm, subglobose, light green, fruiting calyx with variable dimensions, half the length of the fruit or slightly exceeding its length; seeds 3.8 − 4.1 × 3 − 3.1 mm, widely ellipsoid or orbicular, dark brown, without spots, slightly foveolate, caruncle 1.8 − 2 mm, triangular, yellowish, sessile.

Additional specimens examined: — BRAZIL. Mato Grosso: Alta Floresta, Complexo Hidrelétrico Apiacás , PCH Cabeça-de-boi, Acesso Península, 10°21’18”S, 56°58’40”W, 292 m, 18 December 2014, fl., C. R. A. Soares-Lopes et al. 8198 ( HERBAM) ; Complexo Hidrelétrico Apiacás , UHESA Salto Apiacás, do outro lado do rio, 10°17’53”S, 57°18’20”W, 252 m, 4 February 2015, fl., fr., C. R. A. Soares-Lopes 8484 ( HERBAM) ; 9 January 2015, fl., fr., C. R. A. Soares-Lopes 8310 ( HERBAM) ; Linha de Transmissão Interna , 10°20’29”S, 56°58’35”W, 288 m, 22 January 2015, fl., C. R. A. Soares-Lopes 8401 ( HERBAM) ; Aripuanã, Região da Serra Morena e Vale do Ouro , a direita da estrada de terra que liga as sedes dos municípios de Aripuanã e Castanheira (MT-420), 10°33’18.8”S, 58°53’3.2”W, 473 m, 08 April 2017, fl., fr., R. C. Sodré & A. O. Souza 3133 ( UFG), 3134 ( UFG), 3135 ( UFG), 3136 ( UFG) ; Cáceres, Estação Ecológica Serra das Araras , 15°49’30”S, 57°17’28”W, 760 m, 11 June 2011, fl., fr., C. M. S. C. Brazão & N. A . U.S. Silva 125 ( UFMT) ; Novo Mundo, Parque Estadual Cristalino, 9°35’16”S, 55°55’8”W, 332 m, 13 December 2006, fl., fr., D. Sasaki et al. 1196 ( HERBAM) ; 9°35’3”S, 55°11’31”W, 379 m, 26 January 2008, fl., fr., D. Sasaki et al. 1931 ( HERBAM) ; 9°41’18”S, 55°26’33”W, 459 m, 2 February 2008, fl., D. Sasaki et al. 2128 ( HERBAM) ; Paranaíta, UHE Teles Pires , 9°20’29”S, 56°46’37”W, 246 m, fl., 27 December 2011, C. R. A. Soares et al. 4928 ( HERBAM) ; 9°20’50”S, 56°46’57”W, 223 m, 14 March 2012, fl., fr., C. R. A. Soares et al. 5522 ( HERBAM) ; Peixoto de Azevedo, BR 080 , cachoeirinha do Rio Peixoto, cerca de 63 km de Matupá em direção ao Rio Xingu , 10°25’S, 54°28’W, 24 April 1997, fl., fr., V. C. Souza et al. 15610 ( ESA, UFMT) ; Porto Estrela, Estação Ecológica Serra das Araras , ca. 1 km a direita da porteira de entrada da reserva, acessada pela Fazenda Coqueiro , 15°46’36.3”S, 57°15’9.6”W, 810 m, 05 December 2016, fl., fr., R. C. Sodré & N. A. G. Escobar 2872 ( UFG), 2873 ( UFG), 2874 ( UFG), 2875 ( UFG), 2876 ( UFG), 2877 ( UFG), 2878 ( UFG), 2879 ( UFG), 2880 ( UFG), 2881 ( UFG) ; Poxoréo, Mata Velha, 03 February 2000, fl., fr., M. Macedo et al. 7171 ( UFMT). Pará : Jacareacanga , UHE São Manoel–Sete Quedas , 9°19’5”S, 56°46’4”W, 11 March 2016, fl., L. P. Zanzini et al. 76 ( HERBAM) ; UHE Teles Pires , 9°20’44”S, 56°46’33”W, 202 m, 3 February 2012, fl., fr., C. R. A. Soares et al. 5216 ( HERBAM) ; 9°22’2”S, 56°46’45”W, 310 m, 23 April 2012, fl. e fr., C. R. A. Soares et al. 6089 ( HERBAM). Marabá, Alto da Serra , arredores do N5 , 12 May 1982, fl., fr., R. S. Secco et al. 124 ( US) ; Serra dos Carajás setor n 4, 25 March 1977, fl., fr., M. G. Silva & R. Bahia 2917 ( INPA) ; 14 March 1984, fl., A. S. L. da Silva et al. 1761 ( INPA). Parauapebas, Serra dos Carajás, 25–30 km NW of Serra Norte mining camp., 5°55’S, 50°26’W, 5 December 1981, fl., fr., D. C. Daly et al.1712 ( HRB, INPA) ; Serra Norte, Projeto Carajás, 02 July 1986, fl., R. B. Torres & J. W. B. Machado 18446 ( UEC). Rondônia : Itapuã do Oeste , Floresta Nacional do Jamari , 12 km from km 602 of BR-364 in Itapuã do Oeste along Estrada Principal , Trilha da Pedra Grande , 9°11’53.59S, 63°4’53.51”W, 15 March 2012, fl., fr., W. Castro et al. 154 ( RON) ; Linha do Módulo de Pesquisa Potosi-PPBio, 9°16’21”S, 62°54’14”W, 19 April 2015, fl., fr., H. Medeiros et al. 1625 ( RON) ; 28.7 km a partir do km 602 da BR-364 em Itapuã do Oeste , 18, 7 km na trilha da Pedra Grande, 9°11’17.56S, 62°56’55.57”W, 26 March 2016, fl., fr., D. S. Costa et al. 860 ( RB). Porto Velho, estrada Porto Velho – Cuiabá, BR 364 , km 159, 9 February 1983, fl., fr., L. O. A. Teixeira et al. 1414 ( INPA) ; canteiro de obras da AHE Jirau, portão de acesso ao alojamento provisório, 9°18’42”S, 64°36’22”W, 120 m, 05 January 2009, fl., fr., G. Pereira-Silva 13973 ( CEN, RON) ; Jaci-Paraná, margem direita do rio Madeira, em frente à corredeira de Jirau , 9°19’17”S, 64°43’35”W, 85 m, 23 March 2010, fl., G. Pereira-Silva et al. 15140 ( CEN, HUEFS, RON) .

Distribution and ecology: — Croton hadrianii was described by Baillon (1864) for Brazil based on an unnumbered collection of Alexandre Rodrigues Ferreira obtained during an expedition to the states of Mato Grosso, Pará and Amazonas. Although there is no information on the label of the type collections about the precise locality of collection, we confirmed the occurrence of Croton hadrianii for the states of Mato Grosso, Pará and Rondônia ( Figure 3 ). It grows in cerrado vegetation on shallow and stony soils, between 85 and 810 m elevation.

Flowering and fruiting:—Specimens were collected with flowers and fruits from December to July.

Preliminary conservation status: — Croton hadrianii has its conservation status interpreted here as Least Concern (LC) in according to IUCN (2017) since it has an Occurrence Extension (EOO) of approximately 500,000 km 2 and has been found in more than ten locations. In addition, the species occurs in Conservation Units such as Serra das Araras Ecological Station and Cristalino State Park, in Mato Grosso state, and in Carajás National Forest in Pará state.

Etymology:—The specific epithet “hadrianii ” ascribed by Baillon (1864) to this species seems to have been a reference to Adrien de Jussieu, since there is a label in the lower left of the type collection P 00623573 with the number 32 and the abbreviation “Ad. Dej.”, an allusion to Adrien de Jussieu.

Typification:—Analyzing the nomenclatural types of C. hadrianii we verified that there are two duplicates of the same collection in P, both in perfect state of conservation, with the barcordes P00623573 and P00623574; there is also a type fragment in F. Thus, we propose here the collection P00623573 as lectotype of the species, since it has mature pistillate and staminate flowers besides fruits and, therefore, faithfully reflects the original description of the species.

Systematic position, characterization, and taxonomic notes:— Croton hadrianii was described by Baillon (1864) as a member of Croton section Hesperidium Baillon (1864: 306) . However, van Ee et al. (2011) placed it in C. section Geiseleria , since it has the main diagnostic features of that section, such as shrubby habit, stellate trichomes, glands at the apex of the petiole or at the base of the leaf blade, leaf margin crenate or serrate with glands in the indentations, and pistillate flowers with unequal, usually free and eglandular sepals. We agree with van Ee et al. (2011) on the systematic position of the species under discussion.

Croton hadrianii can be recognized and differentiated from the other species of Croton sect. Geiseleria by characters such as branches and leaves with tomentose indument to the touch, petioles with relatively large sessile patelliform glands (1.3 − 1.7 mm in diam), crenate or sometimes serrate leaf margin with sessile patelliform glands on the abaxial surface, inflorescences with 2 − 4(− 6) pistillate flowers sparsely distributed at the base, followed immediately by staminate flowers, the latter in cymules with 1 − 4 flowers, or separated by a short sterile space, as well as pistillate flowers with five to seven slightly unequal, sepals, and (2 −)4-fid styles.

In his synopsis on Croton in the Brazilian Amazon, Secco (2008) recognized 31 species, ten of them belonging to C. sect. Geiseleria . Later one, he also described C. strobiliformis Secco (2009: 249) and C. campinarensis Secco et al. (2012b: 2) , both in section Geiseleria , as new species, and cited C. pycnadenius Müller Argoviensis (1873: 216) ( Secco & Berry 2013) for the Brazilian Amazon. To update the section for Amazonian Brazil, we provide below a key to the species of Geiseleria section occurring in Amazonian biome according to IBGE (2004), including C. hadrianii and C. wittianus Ule (1908: 75) , which although not treated by Secco (2008), was described for the region by Ule (1908). We also provide images for most of these species ( Figures 4 and 5 ).

Key to the species of Croton sect. Geiseleria occurring in the Brazilian Amazon

1. Leaves with sessile patelliform glands at the apex of the petiole or base of the blade......................................................................2

- Leaves with stipitate patelliform, cylindrical or obconic glands at the apex of the petiole or base of the blade...............................5

2. Inflorescence with 2–4(–6) pistillate flowers; styles usually 4-fid or multifid; fruiting pedicel 0.5 − 1 mm long..............................3

- Inflorescence with 6–12 pistillate flowers; styles 2-fid; fruiting pedicel 1.5 − 2 mm long.................................................................4

3. Petioles 8 − 17 mm long; leaf blades 4.6 − 14 × 2.3 − 5.5 cm, frequently oval-lanceolate or lanceolate, margin doubly crenulate or often serrulate, densely pubescent on both surfaces......................................................................................................... C. hadrianii

- Petioles 2 − 5 mm long; leaf blades 2 − 6.5 × 1.2 − 2.5 cm, frequently elliptic, margin subentire, sparsely pubescent on both surfaces ................................................................................................................................................. C. spiraeifolius Jablonski (1965: 164)

4. Leaf blades glabrous or sparsely pubescent on the adaxial surface; pistillate calyx with lobes united up to halfway from base ....... ....................................................................................................................................................... C. hostmannii Miquel (1848: 477)

- Leaf blades densely pubescent on the adaxial surface; pistillate calyx with free sepals...................................................................... ................................................................................................................................... C. subincanus Müller Argoviensis (1865: 139)

5. Inflorescences with a distinct sterile zone between pistillate and staminate flowers; pistillate flowers with 6 − 8 sepals..................6

- Inflorescences without a distinct sterile zone between pistillate and staminate flowers; pistillate flowers with 5 sepals.................7

6. Stamens 11; ovary densely pubescent; styles 8 − 16-fid.............................................................. C. krukoffianus Croizat (1944: 453)

- Stamens 5, ovary glabrous or glabrescent; styles 2 − 4-fid..................................................... C. sipaliwinensis Lanjouw (1939: 698)

7. Bracts with glands..............................................................................................................................................................................8

- Bracts without glands.......................................................................................................................................................................11

8. Leaf blades narrowly elliptic or linear-lanceolate, margin entire ou subentire; staminate bracts 2.5 − 4 mm long; staminal filaments villous, anthers with acute apex; capsules oblong, pedicel 2.5 − 5 mm long....................................... C. mollis Bentham (1854: 375)

- Leaf blades ovate to lanceolate, margin serrate, serrulate or crenate; staminate bracts 1.5 − 2.2 mm long; staminal filaments glabrous, anthers with obtuse or truncate apex; capsules globose, pedicels 1 − 2 mm long.....................................................................9

9. Shrubs 1.5 − 3 m tall; leaf margin with glands in the sinuses; inflorescences 4.8 − 15 cm long, laxly flowered; bracts with stipitate patelliform glands....................................................................................................................... C. asperrimus Bentham (1854: 376)

- Subshrubs 0.5 − 1 m tall; leaf margin usually without glands in the sinuses; inflorescences 0.9 − 6 cm long, densely flowered; bracts with pyriform glands........................................................................................................................................................................10

10. Stems often tomentose; petiole with obconic or shortly stipitate patelliform glands; bracts with sessile glands................................ ................................................................................................................................................ C. glandulosus Linnaeus (1759: 1275)

- Stems hirsute; petiole with narrowly cylindrical glands; bracts with stipitate glands ... C. hirtus L’Héritier de Brutelle (1784: 17)

11. Inflorescences 5 − 20 mm long; styles 0.9 − 1 mm long; staminate pedicels and calyx glabrous or glabrescent ................................... ...................................................................................................................................................... C. trinitatis Millspaugh (1900: 57)

- Inflorescences 30 − 130 mm long; styles 2.3 − 6.5 mm long; staminate pedicels and calyx densely pubescent externally...............12

12. Leaf blades lanceolate or narrowly elliptic, 0.5 − 1.5 cm wide, base acute, margin entire or subentire................................................ .................................................................................................................................................................. C. wittianus Ule (1908: 75)

- Leaf blades ovate, elliptic or oval-lanceolate, 1.9 − 6.8 cm wide, base cordate, margin serrate or crenate......................................13

13. Leaf margins without glands; pistillate sepals equal, narrowly triangular or lanceolate; fruiting calyx not exceeding half of the fruit length ........................................................................................................................................................................... C. pycnadenius

- Leaf margins with glands; pistillate sepals unequal, at least the two largest, ovate or obovate; fruiting calyces about as long as the fruit...................................................................................................................................................................................................14

14. Petioles 0.5 − 1 cm long; bracts caducous; styles 4-fid; stamens 14 or 15 ................................................................ C. campinarensis

- Petioles 1.5 − 7 cm long; bracts persistent; styles 2-fid; stamens 11.................................................................................................15

15. Leaves chartaceous, venation semi-craspedodromous; inflorescences densely flowered; styles connate into a column at the base .. ................................................................................................................................................................................... C. strobiliformis

- Leaves membranaceous, venation brochidodromous; inflorescences laxly flowered; styles free ....................................................... ...................................................................................................................................................... C. parodianus Croizat (1944: 452)

Figures

FIGURE 1. Croton hadrianii. A. Flowering branch. B. Stipule showing the multiratiate trichomes and glands at the base. C. Detail of the base of leaf showing the acropetiolar glands. D. Detail of the margin of the adaxial surface of a leaf showing a patelliform gland in one of the sinuses. E. Staminate cymule showing bud, bract and scar of a staminate flower. F. Staminate bract showing glands at the base. G. Staminate flower. H. Staminate petal, showing the internally surface barbellate at the base. I. Stamen. J. Pistillate flower. K. Fruit. L. Seed, ventral surface showing raphe and caruncle. M. Seed, dorsal surface. Drawn by Cristiano Gualberto from R.C. Sodré & N.A.G. Escobar 2872.

FIGURE 2. Croton hadrianii A. Habit. B. Flowering branch. C. Detail of the acropetiolar glands. D. Inflorescence exhibiting fruits, staminate buds and flowers. E. Pistillate flower. F. Staminate buds and flowers. G. Young fruit. Photographs taken by the first author.

FIGURE 3. Distribution map of Croton hadrianii AM =Amazonas state, GO = Goiás, MS = Mato Grosso do Sul, MT = Mato Grosso, PA = Pará, RO = Rondônia, and TO = Tocantins.

FIGURE 4. Some species of Croton section Geiseleria occurring in the BrazilianAmazon. A–C. C. asperrimus. A. Habit.B. Inflorescence showing young fruits, pistillate flowers, staminate flowers, and buds. C. Pistillate flowers. D and E. C. campinarensis. D. Habit. E. Flowering branch, highlight the inflorescence in the upper left. F and G. C. glandulosus. F. Habit. G. Inflorescence showing pistillate flowers, staminate flower and buds. H and I. C. hirtus. H. Habit. I. Fruits at base of inflorescence. Photographs taken by the first author, except D and E, which were kindly provided by André Luiz de Rezende Cardoso.

FIGURE 5. Some species of Croton section Geiseleria occurring in the Brazilian Amazon. A and B. C. krukoffianus. A. Flowering branch. B. Inflorescence showing young fruits, staminate flowers and buds. C–E. C. parodianus. C. Habit. D. Inflorescence exhibiting young fruits, pistillate flowers, staminate flowers and buds. E. Fruits. F–H. C. pycnadenius. F. Habit. G. Inflorescence showing pistillate flower, staminate flowers and buds. H. Fruit. I–K. C. trinitatis. I. Habit. J. Inflorescence showing pistillate flowers, staminate flower and buds. K. Fruits. Photographs taken by the first author, except D and E, which were kindly provided by Marcelo Fragomeni Simon.