Ochnaceae on São Luís Island, Maranhão, Brazil

Abstract

The family Ochnaceae belongs to Malpighiales and has about 550 species included in 34 genera, with pantropical distribution. For Brazil, 207 species are reported, 16 have been recorded in Maranhão state. On São Luís Island, a well sampled area in the state, there were records of two genera, Ouratea and Sauvagesia, and three species: O. fieldingiana, O. hexasperma, and S. erecta. To confirm the occurrence of these species and provide new data about the family in Maranhão, this study aimed to provide a complete taxonomic treatment of the Ochnaceae on São Luís Island, since the region still lacks taxonomic treatments of specific taxa. Field expeditions were carried out to collect plants, and specimens at MAR and SLUI, and on virtual herbaria, were analyzed. As a result, six species were identified, including five in Ouratea and one in Sauvagesia namely: O. cassinifolia, O. castaneifolia, O. cearensis, O. hexasperma and O. racemiformis, and S. erecta. Specimens that had been identified as O. fieldingiana were redetermined as O. castaneifolia. Ouratea cassinifolia, O. cearensis, and O. racemiformis are new records for the island.

Key words:
Malpighiales; new occurrences; Ouratea ; Sauvagesia ; taxonomic treatment

Resumo

Ochnaceae pertence à ordem Malpighiales e possui cerca de 550 espécies incluídas em 34 gêneros, com distribuíção pantropical. Para o Brasil, são reportadas 207 espécies, 16 são registradas no Maranhão. Para a Ilha de São Luís, a área mais bem amostrada do estado, os registros apontam a ocorrência de dois gêneros, Ouratea e Sauvagesia, e de três espécies, O. fieldingiana, O. hexasperma, e S. erecta. Visando confirmar a ocorrência destas espécies e levantar novos dados sobre a família no Maranhão, este trabalho teve como objetivo fornecer um tratamento taxonômico das Ochnaceae da Ilha de São Luís, visto que a região ainda é carente de tratamentos taxonômicos mais aprofundados em táxons específicos. Para atingir este objetivo, foram realizadas expedições de coleta e análise das coleções dos herbários MAR e SLUI, além dos espécimes disponíveis em herbários virtuais. Como resultados, foram identificadas seis espécies, incluíndo cinco em Ouratea e uma em Sauvagesia, a saber: O. cassinifolia, O. castaneifolia, O. cearensis, O. hexasperma, O. racemiformis e S. erecta. Os espécimes que vinham sendo identificados como O. fieldingiana foram reconhecidos como O. castaneifolia, além disso O. cassinifolia, O. cearensis e O. racemiformis são novos registros para a ilha.

Palavras-chave:
Malpighiales; novas ocorrências; Ouratea ; Sauvagesia ; tratamento taxonômico

Introduction

The family Ochnaceae De Candolle (1811a: 209) was initially included in the order Malpighiales due to having dentate leaves and stipules (Cronquist 1988; Judd et al. 2009; Chacon 2011). Subsequently, molecular analyses confirmed this phylogenetic position (Xi et al. 2012). The family has a pantropical distribution and comprises around 550 species distributed in 34 genera (Schneider et al. 2021). In Brazil, Ochnaceae occur in all regions and there are 207 species and 13 genera (Flora e Funga do Brasil 2022, continuously updated). The Northeast Region is the third richest in species (58 spp.); the North (107 spp.) and Southeast (75 spp.) regions are the richer, respectively (Flora e Funga do Brasil 2022, continuously updated). In Maranhão, there are records of 16 species distributed in two genera: Ouratea Aublet (1775: 397), the largest genus in the family (Schneider et al. 2021); and Sauvagesia Linnaeus (1753: 203).

Ochnaceae comprise shrubs, subshrubs, trees, and more rarely herbs. They have paired, perennial or deciduous stipules and simple, alternate leaves that usually have serrate or partially serrate margins. The flowers are hermaphroditic, actinomorphic or zygomorphic, dichlamydeous, dialypetalous and dialysepalous, and have articulate pedicels, anthers with poricidal or longitudinal dehiscence, staminodes present or absent, a superior ovary, and a syncarpous gynoecium (Amaral et al. 2014). The leaf structure of Ochnaceae is very characteristic, making the family relatively easy to identify in the field (Marinho et al. 2018). Some characters are essential to recognize species, especially for Ouratea. In this genus, the leaves are usually serrate, and the leaf blade shape is highly variable but always simple, with a coriaceous or chartaceous texture. Most of the species have evident veins, the midvein is sulcate or prominent, and the venation is eucamptodromous with parallel intersecondary veins between the secondary veins that are visible or not visible on both surfaces and frequently inconspicuous (Silva 2015). Sauvagesia can be characterized by its highly variable habit, from annual or perennial herbs to shrubs and subshrubs; opposite leaves with serrated or long ciliated margins. The flowers, axillary or in congested terminal inflorescences, are extremely fragile to the touch, ranging from white to magenta. The fruits are capsular and protected by the calyx and persistent corona (Zappi 2018).

Although identifying Ouratea is easy using leaf morphology, the species of Ouratea are difficult to identify, and most of the specimens of the genus deposited in collections are undetermined. Maranhão has an ecotone region between the Cerrado and Amazonia, which are the two domains with the greatest diversity of Ochnaceae, and there are no taxonomic treatments of the family for the state. We believe a taxonomic treatment of the family in the region is very relevant. Thus, the objective of this work is to provide a taxonomic treatment of the Ochnaceae on São Luís Island.

Material and Methods

São Luís Island, also called Grande Island, Maranhão Island and Upaon-Açu, is around 831.7 km² and includes the municipalities of Paço do Lumiar, Raposa, São José de Ribamar and the capital of the state, São Luís (Bandeira 2017). It is in the extreme northern part of the state (02°35’11”S, 44°13’32”W) and occupies the center of the Golfão Maranhense archipelago (Muniz et al. 1994). The island is one of the most collected areas of the state according to data on speciesLink (<http://www.splink.org.br/>).

This work is based on field observations and a study of new collections and specimens deposited in herbaria. The fieldwork was conducted between December 2019 and November 2022, in four municipalities on São Luís Island, with the goal of collecting material for herbaria and data and images of species in the field. In some protected areas on the island, collecting was more frequent, such as Sítio do Rangedor State Park and the Itapiracó Environmental Protected Area; collecting was permitted under license number A16-2021 of the process 2105140013, which was issued by SEMA (acronym in Portuguese for the Secretaria de Estado do Meio Ambiente e Recursos Naturais). Other localities sampled were the dunes of São Marcos Beach, Sítio Santa Eulália, and Sítio do Físico. All the specimens collected were processed according to the techniques described by Mori et al. (1989) and deposited in the MAR herbarium at the Federal University of Maranhão, São Luís campus.

The herbaria on São Luís Island were consulted: MAR, at the Federal University of Maranhão; and SLUI, at the State University of Maranhão. Additionally, data from specimens available on virtual herbaria were consulted using the Herbário Virtual Reflora (<http://reflora.jbrj.gov.br/>) and speciesLink (<http://www.splink.org.br/>). Further, the herbaria at New York (NY, <http://sweetgum.nybg.org/science/vh/>) and Washington (US, <http://collections.nmnh.si.edu/search/botany/>) in the United States of America, which have numerous specimens from Maranhão, were consulted virtually.

The species were identified through a comparative analysis of type material and identification keys in Zappi (2018), Silva (2015), and on Flora e Funga do Brasil 2022 (continuously updated). The morphological descriptions are based on fresh and dry specimens, and the terminology follows the illustrated dictionary by Gonçalves & Lorenzi (2011).

Results and Discussion

We identified two genera, Ouratea and Sauvagesia, and six species of Ochnaceae on São Luís Island: O. cassinifolia (De Candolle 1811b: 421) Engler (1876: 319), O. castaneifolia (De Candolle 1811b: 417) Engler (1876: 309), O. cearensis (Tieghem 1902: 235) Sastre & Offroy (2016: 86), O. hexasperma (A. Saint-Hilaire 1825: 61) Baillon (1873: 366), O. racemiformis Ule (1915: 335), and S. erecta Linnaeus (1753: 203). Records previously determined as O. fieldingiana Engler (1876: 309) on the island were identified during this work as O. castaneifolia. Although O. cassinifolia, O. cearensis and O. racemiformis were deposited in collections, they had not been identified and are new records for the island. All six species described were collected during fieldwork in different locations on the island, including O. cassinifolia that was represented by only two unidentified specimens in the MAR herbarium. Ouratea hexasperma is widely distributed on the island and was present in most of the collection localities. On the other hand, the rarest species were O. cassinifolia, which was found only once in the field, and S. erecta, which was mostly found in flooded or wet areas.

Taxonomic treatment

1. Ochnaceae DC., Nouv. Bull. Sci. Soc. Philom. Paris, sér 2(2): 209. 1811b.

Ochnaceae are herbs, shrubs, subshrubs, or trees with alternate, simple leaves that are petiolate or sessile and have entire or fimbriate, persistent or caducous stipules. Leaf blades are coriaceous or semicoriaceous with serrate, partially serrate, or entire margins; not have glands, trichomes, or secretory structures;secondary venation eucamptodromous. Flowers are solitary or in paniculate or racemose inflorescences, which are terminal or lateral, with persistent or caducous bracts and bracteoles. Flowers are hermaphroditic, dichlamydeous, pedicellate, actinomorphic or zygomorphic, and vary in color. Androecium can have staminodes and the stamens vary from 5 to 10 to numerous, are sessile or subsessile, and have rugose or smooth anthers with poricidal or longitudinal dehiscence. Gynoecium is syncarpous, and a gynophore is present or absent. Carpels 3‒8, ovary superior, 1-style, and each locule has one to numerous ovules. Fruits are capsules or schizocarps with succulent mericarps.

The family is distributed throughout the tropics of the world and comprises around 550 species and 34 genera (Schneider et al. 2021). In Brazil, Ochnaceae are found in all regions and the family is represented by 207 species and 13 genera. In Maranhão, there are records of two genera, Ouratea and Sauvagesia, and 16 species, which are most common in areas with poor soils, such as coastal restingas and sandy areas of the Cerrado and Amazônia.

Taxonomic key to the Ochnaceae species on São Luís Island, Maranhão, Brazil

• 1. Herb; leaves sessile, stipules fmbriate; fowers solitary; stamens 5, staminodes present; fruits capsules 1.6. Sauvagesia erecta

• 1’. Shrubs or treelets; leaves petiolate, stipules entire; fowers arranged in inforescences; stamens 10, staminodes absent; fruits schizocarps.

  • 2. Leaves with an entire to repand margin; inforescence racemose; fower white 1.1. Ouratea cassinifolia

  • 2’. Leaves with an entirely or partially serrate margin; inforescence paniculate or thyrsoid; fowers yellow.

    • 3. Leaves with an entirely serrate margin; bracts and bracteoles greater than 10 1.2. Ouratea castaneifolia

    • 3’. Leaves with a serrate margin on distal half; bracts and bracteoles less than 3.

      • 4. Inforescence thyrsoid; pedicel of central fower red; ovary 5–6-carpelar 1.4. Ouratea hexasperma

      • 4’. Inforescence paniculate; pedicels yellowish green; ovary 5-carpelar.

        • 5. Shrub; canopy paucifoliate; leaves with decurrent base; central branch of inforescence red, up to 12 cm long; bracts narrowly triangular; sepals patent 1.3. Ouratea cearenses

        • 5’. Tree; canopy with numerous leaves; leaves with rounded base; central branch of inforescence green, curved upward, up to 19 cm long; bracts cymbiform; sepals adpressed to the fower 1.5. Ouratea racemiformis

1.1. Ouratea cassinifolia (DC.) Engl., Fl. bras. 12(2): 319. 1876. Fig. 1a-c

Figure 1
a-g. Species of Ouratea on São Luís Island, Maranhão – a-c. O. cassinifolia – a. branch with leaves (adaxial view) and flowers, detail showing the abaxial surface and margin of a leaf; b. detail of an inflorescence; c. immature fruits; d-e. O. castaneifolia – d. branch with flowers, detail of a flower (frontal view); e. leaves (adaxial view); f-g. O. cearensis – f. branch with flower buds and flowers, detail of a flower (frontal view); g. leaf (adaxial view). Photos: a-b. André Scatigna; c-g. Lucas Marinho.

Shrub, up to 2 m tall, canopy paucifoliate, irregular. Stipules early caducous. Leaves petiolate; petiole 0.8–12 mm long, thicker in the basal portion, slightly rugous; leaf blades 5.6–10.5 × 2.5–5 cm, subcoriaceous, oblong, base decurrent, apex obtuse, margin entire to repand, adaxial surface dark green, abaxial surface light green in vivo, discolor; secondary veins in 8–10 pairs, forming 50°–60° angle with the midvein. Inflorescence a terminal raceme, lax, central axis 4.6–6 cm long, pendulous; bracts and bracteoles early caducous; pedicel 1–2 cm long, white to reddish; flower buds 5–6 × 2–3 mm, ovoid, apex cuneate, white; sepals 5, 5–6 × 2–3 mm, oblong, white, base rounded, apex cuneate; petals 5, 5–8 × 3–4.5 mm, slightly unguiculate, white, reflexed to the sepals, base slightly attenuate, apex rounded; stamens 10, 3–4 mm long, anthers sessile, yellow, poricidal, slightly rugous; gynoecium 4–6 × 1–2 mm, ovary 5-carpellate, 1–1.5 × 1–2 mm, white, styles 3–5 mm long, white, stigma inconspicuous. Fruits 5.5–8 × 4–6 mm, carpophore subglobose, 2.2–3 × 2–4 mm, light green, mericarps up to 5, usually with 3 aborted, 3.3–5 × 2.4–4 mm, ellipsoid, light green when immature. Seeds not seen.

Specimens examined: São Luís, Ponta do Guaxinim, 3.XI.1986, fr., M.C.F. V. Santos 400 (MAR); Alumar, 13.XI.1995, fl. and fr., K.B. Ferreira et al. 17 (MAR); Sítio do Físico, 02°34’23”S, 44°16’56”W, 3.IX.2022, fl., L.C. Marinho et al. 1833 (MAR).

Additional specimens examined: BRAZIL. MARANHÃO: Icatú, área de campinarana próximo à lagoa, 02°49’03.5”S, 43°55’11”W, 63 m alt., 16.VII.2022, fl., L.C. Marinho et al. 1813 (MAR).

This species has been recorded with flowers in July, September, and December and with fruits in November and December.

Ouratea cassinifolia is the most distinct species of Ouratea on the island. It can be easily recognized by the non-serrate leaf margin (Fig. 1a), inflorescence that is a raceme, and white flowers (Fig. 1b). Photographs of O. cassinifolia from other localities generally show smaller, oval leaves that are often grouped at the end of branches. However, the specimen Marinho 1833 has considerably larger leaves that are oblong and spaced out along the branch.

Ouratea cassinifolia is endemic to Brazil and occurs in the North and Northeast regions, only in the states of Pará and Maranhão (Flora e Funga do Brasil 2022, continuously updated). This is a new record for São Luís Island; there are only three specimens, which are all from shady areas far from the coast.

1.2. Ouratea castaneifolia (DC.) Engl., Fl. bras. 12(2): 309. 1876. Fig. 1d-e

Shrub, up to 2.5 m tall, canopy with numerous leaves, irregular. Stipules caducous. Leaves petiolate; petiole ca. 1 cm long, slightly rugous; leaf blades 4.7–23 × 1.6–8 cm, coriaceous, oblong, base rounded, apex acuminate, margin entirely serrate, adaxial surface light green, glossy, abaxial surface light green in vivo, discolor; secondary veins in 8–10 pairs, forming 60°–70° angle with the midvein. Inflorescence a terminal panicle, congested, central axis 4–10 cm long, lateral axis 1–6 cm long; bracts ≥ 10, 5–9 × 2.5–3.5 mm, narrowly triangular, striated longitudinally, reddish-brown in vivo, erect, apex acute; bracteoles ≥ 10, 2–3 × 1–2 mm, lanceolate, striated longitudinally, reddish-brown in vivo, apex acute; pedicel 1–9 mm long, green; flower buds 4–5.5 × 2.5–5 mm, ovoid, yellowish-green in vivo, apex acute; sepals 5, 4–6 × 1.5–3 mm, ovate, yellowish green, adpressed to the petal, base rounded, apex acute to cuneate; petals 5, 6–8 × 5–8 mm, slightly unguiculate, yellow, base slightly attenuate, apex rounded; stamens 10, 4–5 mm long, anthers sessile, yellow, poricidal, rugous; gynoecium 4–6 × 1–2 mm, ovary 5-carpellate, 1–1.5 × 1–1.5 mm, yellow, styles 3–6 mm long, yellow, stigma inconspicuous. Fruits 18–20 × 7–8 mm, carpophore subglobose, 6.5–9 × 7–11 mm, brown in sicco, mericarps up to 5, usually with 3 aborted, 11–13 × 7–8 mm, ellipsoid, brown in sicco. Seeds not seen.

Specimens examined: São Luís, II-III.1939, fr., R.L. Fróes 11570 (NY); Mata da CAEMA, 4.X.1988, fl., J. Ferreira et al. (MAR 3031); Alumar, 13.XI.1995, fl., K.B. Ferreira et al. (MAR 5314); Parque Estadual do Bacanga, 02°37’16,53”S, 44°17’04,36”W, 24.I.2013, fr., M.S. Rodrigues 582 (SLUI); 03°23’35,40”S, 44°19’22,61”W, 20.III.2013, fr., M.S. Rodrigues 588 (SLUI); Bacanga, campus da Universidade Federal do Maranhão (UFMA), 02°32’20,7”S, 44°16’58,4”W, 22.I.2018, fr., J.S. Anjos 569 (MAR); Parque Estadual do Sítio do Rangedor, vegetação ao lado da ciclovia, 02°29’55”S, 44°15’54”W, 1.IX.2022, fl., L.C. Marinho et al. 1826 (MAR); 7.IX.2022, fl., M.D. Caldas et al. 14 (MAR).

Ouratea castaneifolia has been recorded with flowers and flower buds between September and November and with fruits between January and March.

This species is easily recognized in the field by the leaves with strongly serrate margins (Fig. 1e), woody stems, and robust flowers compared to the other Ouratea species on the island, in addition to having numerous bracts and bracteoles. While analyzing the herbarium material and works previously conducted on island, we verified that specimens of O. castaneifolia have frequently been identified as O. fieldingiana or Ouratea nitida (Swartz 1788: 67) Engler (1876: 310). The latter is the most similar to O. castaneifolia but does have records from Maranhão (Flora e Funga do Brasil 2022, continuously updated). Ouratea castaneifolia can be differentiated from O. fieldingiana by its leaves, which have a completely serrate margin, and paniculate inflorescence, while in O. fieldingiana only 2/3 of the leaf margin is serrate and the inflorescence is pseudoracemose (Flora e Funga do Brasil 2022, continuously updated). Ouratea nitida differs by the partially serrate, elliptic leaves and less than 10 bracts, while O. castaneifolia has oblong leaves with a completely serrate margin and greater than 10 bracts.

Ouratea castaneifolia has been recorded in four of the five regions in Brazil (North, Northeast, Central-West, and Southeast). In the Northeast region, this species occurs in the states of Bahia, Ceará, Maranhão, and Piauí (Flora e Funga do Brasil 2022, continuously updated). On São Luís Island, this species was recorded in vegetation typical of the Cerrado and some transition areas. Previously, it had not been cited in any work about the island; however, the Rosa Mochel Herbarium (SLUI) already had two specimens and NY already had one specimen.

1.3. Ouratea cearensis (Tiegh.) Sastre & Offroy, Adansonia 38(1): 86. 2016. Fig. 1f-g

Shrub, up to 2 m tall, canopy paucifoliate, irregular. Stipules 1–2 per node, 1–2 × 1 mm, smooth to slightly striated longitudinally, triangular, apex acute. Leaves petiolate; petiole 2–6 mm long, thicker in the basal portion, slightly rugous; leaf blades 2.3–13.6 × 1.1–5.8 cm, coriaceous, elliptic, base decurrent, green in vivo, slightly discolor, apex acuminate, margin slightly serrate on the distal half; secondary veins in 8–11 pairs, forming 60°–70° angle with the midvein. Inflorescence a terminal or lateral panicle, congested, central axis 3.5–12 cm long, lateral axis 0.9–5.5 cm long, erect; bracts 2, 6–7 × 1–1.5 mm, narrowly triangular, striated longitudinally, brown in vivo, apex acute; bracteoles numerous, 1–1.5 × 0.5 mm, narrowly triangular, striated longitudinally, brown in vivo, apex acute; pedicel 2–9 mm long, green; flower buds 2–5 × 1–3.5 mm, ovoid, yellowish-green in vivo, apex acute; sepals 5, 3.5–6 × 2–3 mm, ovate, yellowish green, patent, base rounded, apex cuneate; petals 5, 3.5–6.5 × 2.5–6 mm, slightly unguiculate, yellow, base attenuate, apex rounded; stamens 10, 2.5–5 mm long, anthers sessile, yellow, poricidal, slightly rugous; gynoecium 3–5 × 1–2 mm, ovary 5-carpellate, 1 × 1–2 mm, yellowish green, styles 2–4 mm long, yellow, stigma inconspicuous. Fruits 5–10 × 5–12 mm, carpophore subglobose, 1.5–3.2 × 3–6 mm, brown in sicco, mericarps up to 5, usually with 3 or 4 aborted, 2.5–7.5 × 2–5 mm, ellipsoid, brown in sicco. Seeds not seen.

Specimens examined: São José de Ribamar, Praia de Panaquatira, 02°28’23”S, 44°03’13,8”W, 23.I.2014, fr., J.P. Lima 105 (MAR). São Luís, II-III.1939, fr., R.L. Fróes 11567 (NY); campus da Universidade Estadual do Maranhão (UEMA), 26.XI.1991, fl., J. Azevedo 04 (SLUI); Parque Estadual do Sítio do Rangedor, 27.XI.2010, fl., S.M. Santos (MAR 5452); Bacanga, Campus da Universidade Federal do Maranhão (UFMA), 02°33’06,8”S, 44°17’21,6”W, 4.IX.2018, fl., J.J.F. Sousa 109 (MAR); 02°32’20,7”S, 44°16’58,4”W, 29.I.2019, fr., J.S. Anjos 450 (MAR); Sítio Santa Eulália, 02°30’38”S, 44°16’37”W, 8.X.2019, fl. and fr., E.C.G. Silva (MAR 12224); Área de Proteção Ambiental do Itapiracó, área de floresta estacional semidecidual, 9.XII.2019, fl., L.C. Marinho et al. 1554 (MAR). São Luís, Sítio do Físico, 20.XI.2021, fl., M.D. Caldas et al. 09 (MAR); 20.XI.2021, fl., M.D. Caldas et al. 10 (MAR); Parque Estadual do Sítio do Rangedor, 7.IX.2022, fl., M.D. Caldas et al. 12 (MAR); dunas da praia de São Marcos, 7.IX.2022, fl., M.D. Caldas et al. 16 (MAR).

This species has been recorded with flowers and flower buds from September to December and with fruits in January and October.

Ouratea cearensis is easily confused with O. racemiformis; however, some characters differ between the species. For example, in O. cearensis the central inflorescence axis is reddish and shorter, with lateral axes approximately the same size as the central axis. The sepals are patent, and the flower buds are slightly smaller compared to those of O. racemiformis.

Ouratea cearensis is endemic to Brazil and occurs the North and Northeast region in the States of Bahia, Ceará, Maranhão, Paraíba, Piauí (Flora e Funga do Brasil 2022, continuously updated), and Pará. On São Luís Island, this was the only species collected in an area of restinga and, like O. castaneifolia, it has been misidentified as O. fieldingiana. Unlike the other species, the specimens of O. cearensis often had galls.

1.4. Ouratea hexasperma (A. St.-Hil.) Baill., Hist. Pl 4: 366. 1873. Fig. 2

Figure 2
a-e. Ouratea hexasperma – a. habit; b. detail of an inflorescence; c. detail of dichasial arrangement showing the red pedicel of the central flower; d. individual of Tyrannus savana consuming the fruits of O. hexasperma; e. fruit with metallic blue mericarps. Photos: Lucas Marinho.

Shrub, up to 1 m tall, canopy paucifoliate, irregular. Stipules present, 1–2 per node, 9–10 × 3 mm, coriaceous, striated longitudinally, triangular, apex acute. Leaves petiolate; petiole ca. 5 mm long, slightly rugous; leaf blades 4.6–7.1 × 2.6–3.9 cm, coriaceous, ovate, base rounded, light green in vivo, slightly discolor, apex acuminate, margin slightly serrate on the distal half; secondary veins in 9–12 pairs, forming 60°–70° angle with the midvein. Inflorescence terminal or subterminal, thyrsoid, congested, central axis 11.5–14.5 cm long, lateral axis 3–10 cm long; bracts 1, 2–4.5 × 1–2.5 mm, lanceolate, striated longitudinally, greenish-yellow in vivo, erect, apex acute; bracteoles 2, 3–4 × 1.5–2.5 mm, lanceolate, striated longitudinally, greenish-yellow in vivo, apex acute; pedicel 4–9 mm long, green on the lateral flower, reddish on the central flower of dichasium; flower buds 4–7 × 3–4.5 mm, ovoid, yellowish-green in vivo, apex acute; sepals 5, 4.5–6.5 × 2–3 mm, lanceolate to ovate, yellowish green, adpressed to the petals, base rounded, apex acute, persistent; petals 5, 6–8.6 × 5–6.5 mm, unguiculate, yellow, base attenuate, apex rounded; stamens 10, 4.5–5.5 mm long, anthers sessile, yellow, poricidal, slightly rugous; gynoecium 6–8 × 1–2 mm, ovary 5–6-carpellate, 1–2 × 1–2 mm, yellow, styles 4–7 mm long, yellow, stigma inconspicuous. Fruits 4–11 × 5–11 mm, carpophore subglobose, 2–3.5 × 3–5 mm, red in vivo, mericarps up to 5(–6), usually with 3 aborted, 2–8.5 × 2–5 mm, ellipsoid, green to metallic blue in vivo. Seeds 3.5–5.5 mm long.

Specimens examined: Raposa, restinga da Ilha de Curupu, 02°24’09”S, 44°01’19”W, 1.XI.2014, fl., M.A. Machado 96 (MAR); 1.XI.2014, fl., M.A. Machado 130 (MAR); 6.III.2015, fl., M.A. Machado (MAR 013067). São José de Ribamar, Praia de Ponta Verde, 14.XI.1986, fl., C.C. Marques 03 (MAR); Praia de Panaquatira, 02°28’23’’S, 44°03’13,8’’W, 29.III.2014, fl., G.P. Lima 205 (MAR). São Luís, Sítio Santa Eulália, 02°30’38”S, 44°16’37”W, 8.X.2018, fl., E.C.G. Silva (MAR 012222); Parque Estadual do Sítio do Rangedor, vegetação ao lado da ciclovia, 02°29’55”S, 44°15’54”W, 11.IX.2021, fl. and fr., M.D. Caldas et al. 06 (MAR); 11.IX.2021, fl., M.D. Caldas et al. 07 (MAR); 1.IX.2022, fl., L.C. Marinho et al. 1825 (MAR); 7.IX.2022, fl., M.D. Caldas et al. 13 (MAR); 7.IX.2022, fl., M.D. Caldas et al. 15 (MAR); 15.XI.2022, fr., M.D. Caldas et al. 17 (MAR); 15.XI.2022, fl., M.D. Caldas et al. 18 (MAR); 15.XI.2022, fr., M.D. Caldas et al. 19 (MAR).

This species has been recorded with buds, flowers, and fruits from September to November. The rest of the year, the inflorescences are sterile, and the sepals are dry but persistent on the inflorescence. During fieldwork, we observed birds, Tyrannus savana Daudin, 1802, eating the mature fruits (Fig. 2d).

Ouratea hexasperma is easily recognized in the field by the congested inflorescences that look like “brooms” when senescent due to the persistent sepals. Although it is characterized by the presence of 6 carpels, few specimens have this character state. Observations in the field provided information about the colors of live O. hexasperma: the mericarps can be metallic blue (Fig. 2e), which is a little unusual; and the inflorescence dichasia (Fig. 2c), which are here called thyrsoid, have central flowers with a red pedicel.

This species is typical of Cerrado and has been recorded in all regions of Brazil except the South (Flora e Funga do Brasil 2022, continuously updated). On São Luís Island, this species has been recorded on Panaquatira Beach (Lima et al. 2018) and in Sítio do Rangedor State Park (Almeida Jr. et al. 2021) and Sítio Santa Eulália (Silva et al. 2022). It was the most common species encountered during the fieldwork.

1.5. Ouratea racemiformis Ule, Notizbl. Bot. Gart. Berlin-Dahlem 6: 335. 1915. Fig. 3a-c

Figure 3
a-e. Ochnaceae on São Luís Island – a-c. Ouratea racemiformis – a-b. branches with flowers, detail of a flower (frontal view) in b; c. immature fruits; d-e. Sauvagesia erecta – d. habit, detail of a flower (lateral-frontal view); e. habit with flowers. Photos: a-d. Lucas Marinho; e. Mayara Caldas.

Tree, up to 2.5 m tall, canopy with numerous leaves, globose. Stipules present, 2–3 per node, 0.5–1.5 × 0.3–0.7 mm, smooth, slightly striated longitudinally, triangular, apex acute. Leaves petiolate; petiole 4–10 mm long, rugous; leaf blades 3.5–12.5 × 1.9–5.2 cm, subcoriaceous, oblong, base rounded, apex acuminate, margin slightly serrate on the distal third, discolor, adaxial surface dark green, abaxial surface light green in vivo; secondary veins in 9–11 pairs, forming 50°–60° angle with the midvein. Inflorescence a terminal panicle, congested, central axis 4.6–19 cm long, lateral axis 0.3–3.5 cm long, pendulous with an upward curve; bracts 2, 4–6 × 1–3 mm, cymbiform, slightly striated longitudinally, brown in vivo, apex acute; bracteoles 2, 2.5–5 × 1–2 mm, narrowly triangular, slightly striated longitudinally, yellowish-green, apex acute; pedicel 0.1–1.1 cm long, green; flower buds 3–7 × 1.5–4.5 mm, ovoid, yellowish-green in vivo, apex acute; sepals 5, 3.2–7.5 × 1.1–3.5 mm, ovate, yellowish-green, adpressed to the petals, base rounded, apex acute; petals 5, 3–9 × 2.1–7 mm, unguiculate, yellow, base attenuate, apex rounded; stamens 10, 1–6.2 mm long, anthers sessile, yellow, poricidal, rugous; gynoecium 0.5-7 × 0.3-1.5 mm, ovary 5-carpellate, 0.2-1.2 × 0.2-1.2 mm, yellow, styles 0.3-5.8 mm long, yellow, stigma inconspicuous. Fruits 3-12 × 2-13 mm, carpophore subglobose, 1.5-4 × 0.7-7.5 mm, green in vivo, mericarps up to 5, usually with 3 aborted, 1.2-9 × 1.3-5.5 mm, ellipsoid, green in vivo. Seeds 1.5-6.5 mm long.

Specimens examined: São José de Ribamar, Praia de Panaquatira, 02°28’23”S, 44°03’13,8W, 9.XI.2013, fl., G.P. Lima 14 (MAR); 16.XI.2014, fl., G.P. Lima 502 (MAR). São Luís, Calhau 02°30’S, 44°15’W, 30.X.1982, fl., I. & G. Gottsberger 21 (MAR); 30X.1982, fr., I. & G Gottsberger 22 (MAR); Reserva Botânica Rosa Mochel, 25.XI.1987, fl., A. Fernandes 01 (SLUI); campus da Universidade Estadual do Maranhão (UEMA), 28.I.1992, fl. and fr., J. Azevedo 18 (SLUI); Alumar, 29.XI.1994, fr., N. Figueiredo 08 (MAR); Parque Estadual do Sítio do Rangedor, 30.X.2010, fl., S.M. Santos (MAR 5454); Parque Estadual do Bacanga, 02°35’41,15”S, 44°16’14,18”W, 1.XI.2012, fl., M.S. Rodrigues 554 (SLUI); 02°35’41,09”S, 44°16’13,94”W, 1.XI.2012, fl., M.S. Rodrigues 555 (SLUI); Av. Litorânea, dunas da Praia de São Marcos, 02°29’7”S, 44°15’59”W, 21.XI.2015, fl., A.N.F. Silva 702 (MAR); Área de Proteção Ambiental do Itapiracó, área de floresta estacional semidecidual, 9.XII.2019, fl., L.C. Marinho et al. 1549 (MAR); 9.XII.2019, fl., L.C. Marinho et al. 1560 (MAR); Parque Estadual do Sítio do Rangedor, 11.IX.2021, fl., M.D. Caldas et al. 08 (MAR).

Ouratea racemiformis has been recorded with flowers from September to January and with fruits in October, November, and January.

When alive, Ouratea racemiformis is easily confused with O. cearensis. Some of the main characters that can differentiate them are the inflorescence of O. racemiformis has a longer central axis, short lateral axes, and is always curved upward (see Fig. 3a-b). Among the species described, the double, cymbiform bracts are exclusive to this species (Fig. 3b).

In Brazil, it occurs in the North and Northeast regions, its distribution is restricted to the states of Amazonas, Amapá, Pará, and Maranhão (Flora e Funga do Brasil 2022, continuously updated). For São Luís Island, this species had been collected for years but it was never correctly identified. Thus, we report Ouratea racemiformis for the first time for the area.

1.6. Sauvagesia erecta L., Sp. Pl. 1: 203. 1753. Fig. 3d-e

Herb, up to 40 cm tall, paucifoliate. Stipules present, numerous, 4–8.5 mm long, striated, margin fimbriate, apex fimbriate. Leaves sessile; leaf blades 5.3 × 2.2–7.2 mm, membranaceous, oblanceolate, green in vivo, slightly discolor, base attenuate, apex acute, margin serrate; secondary veins in 8–10 pairs, forming 20°–30° angle with the midvein. Solitary flowers, terminal or axillary; bracts foliaceous; bracteoles absent; pedicel 2–11 mm long, pale pink; flower buds 6–7 × 2–5 mm, ovoid, green in vivo, apex acute; sepals 5, 6–7 × 1.2–2.2 mm, lanceolate, green, patent, base rounded and fimbriate on the margin, apex acute and fimbriate on the margin; petals 5, 4–5.5 × 2.5–4 mm, unguiculate, white, base attenuate, apex cuneate; staminodes present, numerous, 0.5–1.5 mm long, pinkish to purple in vivo; stamens 5, 1–2 mm long, anthers 1–1.8 mm long, subsessile, yellow, rimose, smooth; gynoecium 1.1–2.5 × 0.5–1 mm, ovary 3-carpellate, 0.5–1 × 0.5–1 mm, brown in sicco, styles 1.5–3 mm long, white, stigma inconspicuous. Fruits capsules septicidal, 5–6 × 2–3.5 mm, ovoid, sepals, stamens and staminodes persistent. Seeds numerous, 0.5–0.7 × 0.1–0.5 mm, ovoid to globose, rugous to porous. Specimens examined: São José de Ribamar, Sítio Aguahy, 02°38’47,85”S, 44°09’05,76”W, 28.VIII.2012, fl. and fr., F.C.V. Serra 80 (MAR); Área de Proteção Ambiental do Itapiracó, acesso pela Av. Joaquim Mochel, 19.VI.2021, fl., L.C. Marinho et al. 1706 (MAR). São Luís, Sítio Santa Eulália, 11.II.2022, fl. and fr., M.D. Caldas et al. 11 (MAR).

This species has been collected with flowers in February, June, and August and with fruits in February and August.

Sauvagesia erecta is the only species of Sauvagesia that occurs on the island. It can be recognized in the field by the herbaceous habit, white flowers with five stamens (Fig. 3d-e), and stipules and sepals with a fimbriate margin. Its fruit is a capsule with numerous seeds. It has solitary flowers instead of inflorescences. The flowers have staminodes and only 5 stamens, which is half the number of stamens of all the other species described here.

Sauvagesia erecta is widely distributed and has been collected in every Brazilian state (Flora e Funga do Brasil 2022, continuously updated). It occurs in various domains and vegetations. On São Luís Island, S. erecta has been recorded by Cabral Freire & Monteiro (1993) and Serra et al. (2016), and it is frequently associated with swampy areas.

Data availability statement

In accordance with Open Science communication practices, the authors inform that all data are available within the manuscript.

Acknowledgements

We thank the following: the Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA), for the Scientific Initiation grant awarded to the first author (BIC-03710/21); the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), for financing this research through an Edital Universal (402943/2021-0); and the curators of the MAR and SLUI herbaria, for granting us access to the archives.

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Edited by

Area Editor: Dr. Pedro Viana

Publication Dates

• Publication in this collection
  30 Oct 2023
• Date of issue
  2023

History

• Received
  07 Mar 2023
• Accepted
  25 Aug 2023