Defining the genus

Dizygostemon is one of the four genera of the subtribe Stemodiineae (sensu Bentham & Hooker 1876) that occur in Brazil (BFG 2018). It is similar to Achetaria in having the posterior sepal usually much wider than the other four, which are uniformly narrower, the corolla with a papillate lower lip (Fig. 4H), the corolla tube occluded by the inflated palate of the lower lip, touching the upper lip (Fig. 1D, E, 2A, B, C), and the anterior pair of stamens monothecous (Fig.1H left, 3J; Pennel 1940; Ronse 2001; Souza & Giullieti 2009). Dizygostemon can be confused with Stemodia in general aspect and is similar to this genus in the posterior pair of stamens being fertile. It is also similar to Tetraulacium in the four stamens being fertile and in the unequal sepals.

Dizygostemon differs from Achetaria in having the anterior pair of anthers free (Fig. 1G, 4L; vs adherent) and the posterior pair of the anthers fertile with unequal thecae (Fig. 1H right, 4I, J, L; vs sterile with equal thecae) (Giulietti & Wanderley 1973; Souza & Giulietti 2009). It differs from Stemodia in having the corolla tube occluded by the palate (vs not occluded), the anterior pair of stamens monothecous (vs bithecous) and the posterior pair of anthers with unequal thecae (vs equal). It also differs from Tetraulacium in having the corolla tube occluded (vs not occluded), bracteoles present (vs absent) and the posterior pair of stamens bithecous (vs monothecous).

Dizygostemon riparius Scatigna & Colletta, sp. nov. –Fig. 1, 2, 3, 4B, D, F, H, J, L, N, P.

Holotype: Brazil, Maranhão, São Benedito do Rio Preto, margem do Rio Preto, 03°19′28″S, 43°31′02″W, 28 m, planta com flor roxa, 30 Sep 2017, Teles s.n. (UEC[accession number]202426; isotypes: B, K, MAR).

Diagnosis — Dizygostemon riparius is characterized by its glandular villous ovary. It differs from D. floribundus in having stems sparsely to densely tomentose (vs glabrous to strigillose); sepals as long as or slightly longer than corolla tube (vs shorter than half of corolla tube); posterior sepal to 1.5 times as wide as any of other four (vs more than 2 times); ovary glandular villous (vs. glabrous to glandular puberulent); and leaves larger, 1.5–8 × 0.5–4 cm (vs 0.6–1.6 × 0.2–0.7 cm).

Morphological description — Subshrubs, to c. 50 cm tall, aromatic, viscid. Stems crawling to erect, subquad-rangular to clearly quadrangular, canaliculate, branched, frequently presenting adventitious roots, sparsely to densely tomentose, densely covered with non-capitate, flexuous trichomes, interspersed with short, capitate trichomes and sessile glands, denser towards apex. Leaves opposite or rarely 3-whorled, sessile or petiole to 1.5 cm long; blade narrowly ovate to elliptic, 1.5–8 × 0.5–4 cm, base attenuate, margin crenate-serrate, apex acute to obtuse; abaxial surface covered with short, capitate trichomes, sessile glands and more abundant, longer, curved, non-capitate trichomes, these concentrated on veins; adaxial surface covered with short, capitate trichomes and sessile glands interspersed with longer, non-capitate, curved trichomes scattered over surface. Flowers axillary, single or geminate, bracteo-late; pedicel 1–3 mm long, densely covered with short, capitate trichomes, sessile glands and abundant, longer, curved, non-capitate trichomes; bracteoles 2, opposite, narrowly elliptic to lanceolate, 2.9–7 × 1.5–1.7 mm, indumentum similar to leaves; sepals subequal, connate at base, lanceolate, 5.9–7.7 × 2–2.8 mm, posterior one slightly longer and wider than others, apex acute, all five slightly curved outwards, external surface indumentum similar to leaves, internal surface covered exclusively with sessile glands; corolla bilabiate, personate, entirely white or lilac with a pair of white patches on throat, tube 5.2–6.2 mm long, occluded by palate of lower lip, base slightly inflated, externally sparsely tomentose, covered with short, capitate trichomes, sessile glands and longer, curved, non-capitate trichomes, internally tomentose, upper lip 2-lobed, 5–6.2 × 4–4.5 mm, apex truncate to slightly emarginate, externally sparsely tomentose, covered with short, capitate trichomes, sessile glands and more abundant, longer, curved, non-capitate trichomes, lower lip 3-lobed, palate inflated, 3.5–5 × 4–6.5 mm, covered with short, non-capitate trichomes on throat, papillate, lobes 1.8–2.5 × 2–2.5 mm, apex emarginate. Stamens 4, all fertile, didynamous, reaching throat, filaments filiform, apex capitate, anterior pair 3.3–3.7 mm long, posterior pair 4.4–4.6 mm long, both with rare, short, capitate trichomes; anthers of anterior stamens with only one theca, 1–1.1 mm long, glabrous or with rare, sessile glands, anthers of posterior stamens with two thecae, slightly subequal, separated by bi-brachiate connective, 0.7–1 mm long, glabrous or with rare, sessile glands; staminode 1, much reduced. Ovary superior, 2-carpellate, 2-locular, ovoid, 2.8–3 × 1.9–2.1 mm, glandular villous, densely covered with long, glandular trichomes and sessile glands; placentation axillary, ovules numerous; style terminal, solitary, filiform, 4.3–4.6 mm long, sparsely glandular puberulent, persistent; stigma obdeltoid, 0.7–0.8 mm long, curved, glabrous. Capsule ovoid, 5.8–6 × 3.3–3.5 mm, with a deep, longitudinal groove on septum line, sparsely covered with long, glandular trichomes and sessile glands, dehiscence not observed; seeds ovoid, 0.45–0.5 × 0.3–0.31 mm, surface reticulate.

Fig. 1.

Dizygostemon riparius – A: flowering branch; B: prostrate branch with adventitious roots; C: leaf abaxial surface, showing indumentum; D: flower in lateral view subtended by a pair of bracteoles; E: flower in frontal view, showing personate shape; F: calyx with subequal sepals; G: dissected corolla showing androecium; H: types of stamens, anterior on left, posterior on right; I: ovary covered by glandular villous indumentum; J: immature fruit and persistent calyx; K: seed with reticulate surface. – Drawn by Klei Sousa from the holotype (Teles s.n. UEC[accession number]202426). – Scale bars: K = 0.25 mm; G, H, I, J = 1 mm; D, E = 2 mm; C, F = 5 mm; A, B = 1 cm.

Fig. 2.

Dizygostemon riparius – A: flowering branch with 3-whorled leaves; B: flower insertion of lilac-flowered specimen; C: flower insertion of white-flowered specimen; D: habit; E: habitat in Rio Preto River. – Red arrows indicate patches of D. riparius. – Photographs: A, B, C: Ermenson Martins; D, E: Rogério Teles.

Micromorphological study — We observed non-glandular trichomes (type NG) and glandular trichomes (types G1, G2, G3 and G4). The NG type consists of a multicellular, uniseriate trichome with an acute head cell and tiny cuticular granules on the surface (Fig. 3A); its length is variable, reaching 2 mm in Dizygostemon riparius, but scarcely exceeding 0.5 mm in D. floribundus. Type G1 has a broad base, a uniseriate, 2- or 3-celled pedicel, and an apparently 1-celled, round head (Fig. 3B); this type is referred to as capitate throughout the text. Type G2 consists of an obscure, 1-celled pedicel and a wide (60–80 µm in diam.), multicellular head covered with a cuticle layer (Fig. 3C); this type is referred to as sessile glands in the key, diagnosis and descriptions, because this is how it appears under the stereo microscope. Type G3 has a short, 1-celled pedicel and a wide (10–30 µm in diam.), usually clearly 4-celled (sometimes 8- or 16-celled) head (Fig. 3D); this type is also referred to as capitate throughout the text. Type G4 is a variation of the NG type except for the slightly inflated head cell (Fig. 3E). All types of trichomes were found in both compared specimens, but with relatively different distribution and abundance among plant parts.

Fig. 3.

Scanning electron micrographs of trichomes and seed surface of Dizygostemon riparius. – A: type NG; B: type G1; C: type G2; D: type G3; E: types G2 and G4 (white arrow); F: detail of reticulate seed surface, showing periclinal wall ornamentation. – All from the holotype (Teles s.n. UEC[accession number]202426). – Scale bars: B, C, D = 10 µm; F = 20 µm; A, E = 100 µm.

Fig. 4.

Comparative scanning electron micrographs of micromorphological characters of Dizygostemon floribundus (A, C, E, G, I, K, M, O) versus D. riparius (B, D, F, H, J, L, N, P). – A, B: abaxial leaf surface; C, D: adaxial leaf surface; E, F: stem; G, H: corolla lower lip surface; I, J: posterior stamen; K, L: dissected corolla; M, N: seed; O, P: ovary. – Dizygostemon floribundus, from Melo 3449 (ESA); D. riparius, from the holotype (Teles s.n. UEC[accession number]202426). – Scale bars: G, M, N = 50 µm; H, I = 100 µm; A, C, D, E = 200 µm; B, F, J, K, O = 500 µm; L, P = 1 mm.

Table 1.

Occurrence and frequency of each type of trichome on aerial parts of Dizygostemon riparius and D. floribundus. Trichomes: – absent, ± rare, + present, ++ abundant.

Table 2.

Diagnostic characters between Dizygostemon riparius and D. floribundus.

The indumentum and micromorphological aspects of trichomes have been useful for recognizing species within some genera of Gratioleae such as Achetaria (including Otacanthus Lindl.), Philcoxia P. Taylor & V. C. Souza and Stemodia (Ronse 2001; Souza & Giulietti 2009; Scatigna & al. 2017a, 2017b). In this study, these characters were useful in distinguishing Dizygostemon riparius from D. floribundus (Table 1; Fig. 4A–F, O, P).

Both studied specimens were found to possess a reticulate seed surface with smooth to slightly cristate anticlinal walls and more or less papillate external periclinal walls. In Dizygostemon riparius (Fig. 3F, 4N), anticlinal walls are slightly cristate and relatively higher and the periclinal wall is more markedly papillate. In D. floribundus (Fig. 4M), anticlinal walls are smooth and relatively lower and the external periclinal wall is less markedly papillate. In addition, the cells delimited by anticlinal walls are larger and more angu-late in D. riparius.

Phenology — Specimens were observed with flowers and fruits from May to December, especially during the dry season. In São Benedito do Rio Preto, the population was found submerged in the waters of the Rio Preto River from January to June, during the rainy season.

Distribution and ecology — Dizygostemon riparius was recorded in three municipalities of the northeastern portion of Maranhão, Brazil (Fig. 5). Populations grow in periodically waterlogged habitats such as banks and margins of rivers and marshes (Fig. 2E); this riparian life-form is present in some species of Achetaria and Stemodia, which are not described as typical macrophytes (Souza & Giulietti 2009).

Conservation status — Although one of the recorded populations of Dizygostemon riparius is at least partly encompassed by a protected area (Parque Nacional dos Lençóis Maranhenses), we observed strong threats to the quality and extent of its habitat. Threats include inappropriate waste disposal, sand removal, and deforestation of riparian forest, leading to riverbed silting. The species is known from only three locations, with an EOO of 2027 km² and an AOO of 12 km². As based on the IUCN (2012, 2017) criteria, D. riparius should be considered Endangered [EN, B1ab(i,ii,iii)+2ab(i,ii,iii)]. New efforts to track populations of the new species along the river basin may provide additional information for a more accurate evaluation.

Fig. 5.

Distribution map of Dizygostemon riparius in northeastern Brazil. Black triangles represent recorded populations.

Etymology — The specific epithet refers to the riparian habit of the new species, which is found in dense patches along watercourse margins (Fig. 2D, E)

Vernacular name — Dizygostemon riparius is known as “melosa” by local people of São Benedito do Rio Preto because of its viscid aspect when rubbed between fingers. Its leaves, stems and roots release a sharp, refreshing and pleasant aroma and are used to scent clothes and in domestic animals' hygiene.

Remarks — The originally neuter terminations of the epithets of Dizygostemon angustifolius and D. floribundus have been corrected to agree with the masculine gender of Dizygostemon (Art. 23.5, 32.2 and 62.2(a) of the Shenzhen Code; Turland & al. 2018).

Based on the description of Dizygostemon floribundus provided by Schmidt (1862) and an examination of photographs of type specimens, Giulietti & Wanderley (1973) differentiated it from D. angustifolius by leaf blade dimensions, shape and margin. Souza & Giulietti (2009) considered these characters to be highly variable, even among type specimens of D. floribundus, and therefore included D. angustifolius under its synonymy. Dizygostemon floribundus, as currently circumscribed (sensu Souza & Giulietti 2009), has a wide range of morphological variation, especially regarding general indumentum (from glabrous to strigillose), leaf shape (linear, linear-lanceolate, ovate, obovate, oblanceolate), ovary surface (glabrous to glandular puberulent) and corolla dimensions. It occurs in the Caatinga domain in four states of the northeastern region of Brazil, namely Bahia, Ceará, Pernambuco and Piauí. Nevertheless, D. riparius has a unique set of morphological traits not encompassed by this variation; it has sparsely to densely tomentose indumentum (Fig. 4B, D, F), much larger leaves (Fig. 1C, 2A), a glandular villous ovary surface (Fig. 1I, 3E, 4P), and is restricted to the state of Maranhão, within the Cerrado domain. We observed two morphotypes in the population of D. riparius from São Benedito do Rio Preto, one with a lilac corolla with white patches on the lower lip (Fig. 1A, B) and the other with an entirely white corolla (Fig. 2C); in D. floribundus, the corolla is reportedly pale lilac (Souza & Giulietti 2009). For additional diagnostic characters, see Table 2.

Giulietti (1973) and Giulietti & Wanderley (1973) used only a few characters to recognize Dizygostemon angustifolius as a distinct species. Conversely, Souza & Giulietti (2009) examined a limited number of specimens when proposing its synonymization. It is possible that the broad concept of D. floribundus covers even more undescribed species. To properly assess this issue, we recommend thorough examination of several specimens, considering both morphological and geographic ranges, and the use of additional characters such as the types of trichomes and their distribution in the plants, as has proven useful within Achetaria, Philcoxia and Stemodia (Ronse 2001; Souza & Giulietti 2009; Scatigna & al. 2017a, 2017b).

Additional specimens examined — Brazil: Maranhão: Barreirinhas, PARNA dos Lençóis Maranhenses, Povoado de Santo Inácio, campos brejosos abertos, 02°34′49″S, 42°47′32″W, 7 m, 16 May 2015, Mota & al. 3099 (MG[digital image]); Primeira Cruz, Rodovia MA-402 margem direita (Barreirinhas-São Luís), zona rural, margem de lagoa temporária, 02°44′04″S, 43°22′57″W, 25 Sep 2014, Mota & Viana 2776 (MG[digital image]); São Benedito do Rio Preto, 10 Aug 2016, Brandão & Soeiro s.n. (SLUI[accession number]4587); idem, margem do Rio Preto, 03°19′28″S, 43°31′02″W, 1 Oct 2017, Planta com flor branca, Teles s.n. (ESA, HUEFS, UEC[accession number]202423); idem, margem do Rio Preto, 03°19′28″S, 43°31′02″W, planta com flor roxa, 1 Oct 2017, Teles s.n. (UEC[accession number]202425); idem, planta com flor branca, amostra de material cultivado, 21 Oct 2017, Brandão s.n. (UEC[accession number]202422); idem, planta com flor roxa, amostra de material cultivado, 21 Oct 2017, Brandão s.n. (UEC[accession number]202424).