Phyllanthus rosellus (Müller Argoviensis) Müller Argoviensis (1873:53)

Torres, Alícia Marques & Silva, Marcos José Da, 2024, Reinstatement and lectotypification of Phyllanthus rosellus (Phyllanthaceae), an endemic species from the state of Minas Gerais, Brazil, Phytotaxa 645 (3), pp. 259-269 : 260-266

Phyllanthus rosellus (Müller Argoviensis) Müller Argoviensis (1873:53) .

≡ Phyllanthus lathyroides f. rosellus Müller Argoviensis (1863:42) ≡ Diasperus rosellus (Müller Argoviensis) Kuntze (1891:601) .

Type: — BRAZIL. Minas Gerais, Ouro Preto , 1833, A. C. Vauthier n. 83 (lectotype: G-DC00435075 !, designated here; isolectotypes: G-DC00316107 !, G-DC00316109 !, MPU014869 !). Remaining syntype:— BRAZIL. Minas Gerais, Ouro Preto, L. Riedel n. 487, 2809 (not found). ( Figures 1 , 2 , 3 )

Description: — Erect subshrubs 0.5–1.5 m tall, monoecious with phyllantoid branching. Main stem blackish, nondecorticating, papillose, glabrous. Cataphylls 2–3.5 mm long, triangular or triangular-lanceolate, apex acute, slightly papillose or not, margin serrate, membranaceous, glabrous, persistent; branchlets 2–4.5 cm long, unisexual, cylindrical, straight, arranged along the main stem or its branchlets, with or without papillae. Stipules 2.5–3 mm long, narrowly triangular or triangular-linear, membranaceous, margin entire or slightly serrate, discreetly papillose. Leaves 2.2–3.5 mm long, petiole ca. 0.2 mm long, cylindrical, papillose; blade 2.2–3.5 × 1–1.5 mm, oblong-ovate or oblong, base asymmetrical-cordate, apex obtuse, abaxial and adaxial surfaces with rounded papillae, margin entire membranaceous, with 4-5 pairs of secondary brochidodromous veins. Staminate cymules 1(-2)-florous, located along the staminate branchlets and solitary pistillate flowers, situated from ½ of the pistillate branchlets. Staminate bracts 1 × 0.7 mm, triangular, apex acute, margin entire, membranaceous, glabrous, pink. Pistillate bracts 1–1.5 × 0.4–0.8 mm, triangular apex acute, margin slightly serrate, membranaceous, glabrous, pink. Staminate flowers 5–6.8 mm long, pedicel 3–5 mm long, cylindrical, non-papillose; sepals 5, 1–1.8 × 0.5–1 mm, uniseriate, obovate, apex rounded or obtuse, with an evident and pink midrib, margin entire, membranaceous; disk with 5 obtriangular segments, verruculose surface; stamens 3, completely free, filaments ca. 1 mm long, anthers ca. 0.5 mm long, horizontally dehiscent. Pistillate flowers 4–6 mm long, pedicel 3–5 mm, cylindrical, non-papillose; sepals 5, 3–3.5 × 2–2.5 mm, uniseriate, obovate, obtuse or rounded apex, pink, pinnately netted, membranaceous, margin entire; disk entire, slightly cupuliform, margin entire; ovary ca. 1 × 1 mm long, globose; styles 0.5–1 mm long, free, bifid, curved, stigmas capitate. Capsules 2–3 × 1.5–2 mm, globose, smooth; fruiting pedicel 3–5 mm long. Seeds 1–1.5 × 0.5 mm, trigonous, brownish, forehead slightly verruculose, with randomly distributed warts.

Material examined:— BRAZIL. Minas Gerais: Belo Horizonte, Serra da Piedade, 1800-2000m, 13 January 1971 (fl.,fr.), H. S. Irwin, R. M. Harley & E. Onishi 30219 (NY); Moeda, Serra da Moeda, 20º11’33”S, 43º58’45”W, 1466 m. a.s.l., 19 June 2023, (fl.) A. M. Torres et al. 274 (BOTU, UFG); Conceição do Mato Dentro, 15 August 2012, (fl.,fr.), E. Tameirão Neto & C. V. Vidal, 5142 (BHCB); Ibd., Parque Estadual da Serra do Intendente, 22 May 2019 (fl.), S. G. Rezende 7426 (BHCB); Delfinópolis, Paraiso Selvagem, trilha para cachoeira Salto Solitário, 20º26’04”S, 46º38’73”W, 840 m. a.s.l., 11 March 2003, (fl., fr.), J. N. Nakajima, et al. 3476 (HUFU); Ibd., Serra da Gurita, próximo à estrada Delfinópolis — Sacramento, 20º17’21,8”S, 46º52’04,8”W, 900 m. a.s.l., 01 August 1996, (fl.), V. C. Souza et al. 9796 (ESA, RB); Estrada para Pedreira Souza, região da represa de Furnas, 17 February 2006, (fl.), A. A. Arantes, et al. 1723 (HUFU); Ouro Preto, Serra da Brígida, APA Estadual Cachoeira das Andorinhas, Experimento com topsoil (área degradada), 29 January 2018, (fl.,fr.), C. M. G. Onésimo, M. C. T. B. Messias 11 (OUPR); Rio Preto, localidade de Santa Luzia, nascentes de São Gabriel, 21º58’S, 43º52’W, 1000 m. a.s.l., 26 February 1999, (fl., fr.), R. Mello-Silva et al. 1649 (NY, SP); São Roque de Minas, Tiradentes, Parque Nacional da Serra da Canastra, 10 January 1998, (fl., fr.), R. Romero et al. 4955 (HUFU); São Thomé das Letras, 30 July 1987, (fl.), L. S. Kinoshita-Gouvêa et al. 19109 (UEC); Tiradentes, Serra de São José, 21º05’11”S, 44º09’91”W, 1120 m. a.s.l., 16 January 1994, (fl., fr.), A. M. Giulietti, et al. 13713 (ESA); Nova Lima, Mina Capitão do Mato, Região da Mina, 20º07’41”S, 43º54’42”W, 1325 m. a.s.l., 14 February 2020, (fl., fr.), S. G. Rezende & A. G. Justo 8432 (BHCB); Lima Duarte, Parque Estadual da Serra do Ibitipoca, campos entre a Gruta do Viajante o Pico do Pião, 10 March 2004, (fl.), R. C Forzza, et al. 3115 (RB); Datas, Rod. MG — 2, Rio S. Antônio, 8 August 1972, (fl.), G. Hatschbach 30087 (MBM); Iguarapé, Pico Itatiaiuçu 20º07’17”S, 44º21’43,7”W, 1340 m. a.s.l., 08 December 2008, (fl.), F. F. Carmo 3760 (BHCB); Nova Lima, Morro do Chapéu, 24 February 1983, (fl.) P. M. Andrade 1307 (BHCB); Catas Altas, Morro da Água Quente, Mina Tamanduá , 20º08’14”S, 43º25’01”W, 905– 980 m. a.s.l., 19 February 2019, (fl.) S. G. Rezende 6538 (BHCB); Congonhas, Mina da Fábrica, Cava João Pereira , 30 January 2013, (fl.), F. S. Souza et al. 1906 (BHCB); Itabirito, RPPN Córrego Seco, 20º14’39”S, 43º51’25”W, 1329 m. a.s.l., 15 November 2016, (fl.), J. A. M. Souza et al. 36 (BHCB); Caeté, Serra da Piedade, 19º49’S, 43º40’W, 1620 m. a.s.l., 28 April 1985, (fl.), Lusia Cunha et al. 5849 (BHCB); Itabirito, Região da Geardal, próximo a BR 040, Mina Várzea do Lopes, 20º18’6.5”S, 43º55’57.3”W, 1260 m. a.s.l., 02 February 2007, (fl.), M. S. Mendes et al. s.n (BHCB); Brumadinho, Inhotim, Campo Rupestre na Montanha Dolomita, 20º06’56”S, 44º13’57”W, 1022 m. a.s.l., 3 December 2009, (fl.), H. E. S. Costa & R. C. Mota 31 (BHCB); Caeté, Serra da Piedade, 1600 m. a.s.l., 04 December 1997, (fl.), M. F. de Vasconcelos s.n (BHCB); Tiradentes, Serra São José, s.d. 1997, (fl.), A. E. Brina s.n (BHCB); Belo Horizonte, Parque da Serra do Curral, Trilha ecológica na crista da Serra, 19º57’49”S, 43º54’58”W, 1414 m. a.s.l., 13 July 2017, (fl., fr.), A. D. C. Lopes & J. R. Stehmann 69 (BHCB); Barão de Cocais, Pilha do cavalo, Mina Brucutu , 19º53’08,04”S, 43º26’11,22”W, 845 m. a.s.l., 16 December 2002, (fl.), A. M. Oliveira et al. 171 (BHCB); Catas Altas, RPPN Santuário do Caraça, Pico da Carapuça, 20º05’23”S, 43º28’18”W, 1887 m. a.s.l., 28 August 2008, (fl.), C. T. Oliveira & L. L. Giacomin 116 (BHCB); Nova Lima, PE Rola Moça/C, 20º3’60”S, 44º2’0”W, 1450 m. a.s.l., 3 December 2008, (fl.), F. F. Carmo 3603 (BHCB); Nova Lima, Mina Capitão do Mato, Região da Mina, 20º07’41”S, 43º54’42”W, 1325 m. a.s.l., 14 February 2020 (fl.), S. G. Rezende & A.G. Justo 8432 (BHCB); Belo Horizonte, ICB Campus UFMG, November 1977, (fl.), J. A. Oliveira s.n (BHCB); Lima Duarte, Parques Estadual do Ibitipoca, 05 May 1987, (fl.), H. C. de Souza et al. 16132A (BHCB); Ouro Preto, ca. 4 km NE da cidade de Ouro Preto, próximo à base sul da Serra da Brigida, cerca de ¼ km da Cachoeira das Andorinhas, 1100–1200 m. a.s. l., 29 November 1965, (fl.), G. Eiten 7019 (NY).

Distribution and habitat:—Species cited by Webster (2002) for Argentina and Brazil (MG, SC, SP and RJ). However, the analysis of the collections mentioned by the author revealed that those mentioned for Argentina, and for the states of São Paulo, Santa Catarina and Rio de Janeiro, in Brazil, correspond to P. niruri . In this way, we restricted the distribution of P. rosellus to the state of Minas Gerais, southeastern Brazil ( Fig. 4 ). It lives in “cerrados típicos” “campos limpos” e “Campos Rupestres” e “florestas estacionais”, in addition to transition areas of Cerrado and Atlantic Forest, on sandy soils or on rocky outcrops between 840 and 2000 meters of elevation.

Preliminary conservation status:— Phyllanthus rosellus is being categorized as Least Concern (LC), criterion B1, for presenting an Extent of Occurrence (EOO) estimated at 79,232.597 km 2. Additionally, more than 30 populations of the species are known, some of which were found in protected areas, such as: Serra do Intendente State Park (Delfinópolis), APA Estadual Cachoeira das Andorinhas (Ouro Preto) and Serra Canastra Park National (São Roque de Minas), the which ensures, in a certain way, its conservation. Despite this, it grows in Atlantic Forest and Cerrado Biomes, which are considered the most degraded by extensive livestock farming, mining and intense deforestation for agropastoral activities ( Ribeiro et al. 2009, Myers et al. 2000, Mittermeier et al. 2004).

Notes:— Müller Argoviensis (1863) established P. lathyroides f. rosellus based on tiny leaves, solitary flowers with a strong pink color and pedicels 4–6 mm long. Ten years later, Müller Argoviensis (1873) elevated it to species level based on short branches (7–15 cm long) and unisexual, tiny leaves (3–4 mm long), large stipules (2–3 mm long), long pedicels of flowers of both sexes (4–6 mm), and solitary flowers with a strong pink color. Kuntze (1891), using the principle of priority, transferred the species of Phyllanthus known at the time to the genus Diasperus . However, this decision was not accepted, since the International Code of Botanical Nomenclature adopted the genus category from the date of publication of Species Plantarum (1753), where the genus Phyllanthus was described.

Allem (1977) subordinated P. rosellus as a synonym of P. niruri , reporting that both species overlapped in the size of leaves and pedicels, and color of the sepals. Despite this, Webster (2002), in agreement with Müller Argoviensis (1873), treated P. rosellus as a distinct species from P. niruri , arguing that the species differed from P. niruri by its tiny leaves, strongly pink solitary flowers and larger pedicels (4–5 mm length), but highlighting that specimens of P. niruri with tiny leaves are difficult to separate from P. rosellus . In contrast, Martins et al. (2014), in agreement with Allem (1977), reduced P. rosellus to a synonym of P. niruri , arguing that the size of the leaves and floral structures, as well as the color of the sepals, are variations present in P. niruri .

During the analysis of the type collections, protologues and field collections, it was observed that some qualitative characteristics cited for the reinstatement of P. rosellus , for example, size of stipules and pedicel, in addition to solitary flowers vary between populations. However, we assume that the specimens from the state of Minas Gerais are clearly distinguishable from P. niruri , due to their unisexual branches, cataphylls with strongly serrate margins, tiny leaves (2.2–3.5 mm long), staminate flowers distributed along the branchlets and flowers of both sexes with a strongly pink color, which is why we consider P. rosellus distinct from P. niruri ( Table 1 ).

Although the distribution of P. rosellus is restricted to the state of Minas Gerais, it does not occur sympatrically with P. niruri . P. niruri according to Webster (1955, 2002) is distributed from United States to Argentina, including West Indies, and has been introduced or naturalized in countries in Europe and Africa ( Bouman et al. 2022). In Brazil it occurs from north to south, in all phytogeographical domains ( Silva & Sales 2007, Torres et al. 2022b). Although P. niruri is a very variable species in the size of the leaves (5.5–9.2 mm long), the shape of the sepals of both flowers (the staminate obovate or suborbicular, the pistillate elliptical, obovate or combinations), fusion of the stamens (joined up to half the filaments or completely free) color of the sepals (whitish, greenish or slightly pink), can be recognized and differentiated from the others of Phyllanthus subsect. Phyllanthus , by the association of bisexual branchlets, distributed along the main stem or its ends, staminate and pistillate flowers with pedicels 2–4 mm long, and 3–5 mm long, respectively, capitate stigmas and verruculose seeds.

According to the circumscription of Webster (1955, 2002) and Bouman et al. (2022) Phyllanthus sect. Phyllanthus subsect. Phyllanthus includes seven species. Subsequently, Torres & Silva (2022, 2023a, b, c) established five new species for this subsection and proposed the synonymization of P. bolivianus Pax & K. Hoffm (1921:18) and P. mimicus G. L. Webster (1955:52) under P. niruri , thus increasing the number of species from 7 to 10. Now, after the reinstatement of P. rosellus , the subsection comprises 11 species, which can be differentiated by the key bellow:

Figures

FIGURE 1. Phyllanthus rosellus, A. Habit. B. Cataphylls. C. Leaf. D. Staminate flower. E. Pistillate flower. F. Fruit. G. Seed [Drawings by Cristiano Gualberto, from A. M. Torres et al. 274 (UFG) and R. C. Forzza, et al. 3115 (RB)].

FIGURE 2. Phyllanthus rosellus. A. Habit. B. Stem. C. Cataphylls. D and E. Fertile branches, showing small leaves and male flowers on the adaxial surface. F and G. Detail of the unisexual branchlet, showing the pink staminate flowers, with three free stamens. H. Pistillate flower. I. Detail of the pistillate disk and styles J. Seed [Photos A, and F by João Paulo Zorzanelii, B, D, E and G by Paulo Sampaio and C, H, I and J by Alícia Torres].

FIGURE 3. Lectotype of Phyllanthus rosellus, specimen G00435075. Used with permission from ©: Conservatoire et Jardin Botaniques de la Ville de Genève.

FIGURE 4. Distribution of Phyllanthus rosellus in Brazil. A. Map of Brazil highlighting the state of Minas Gerais in gray. B. Map of the state of Minas Gerais, showing its border states. C. Map of the state of Minas Gerais, showing the distribution points of the species. State abbreviations: ES= Espírito Santo; GO=Goiás; MG= Minas Gerais; SP= São Paulo; RJ= Rio de Janeiro.