Synoptic treatment of Dalechampia (Euphorbiaceae) from Espírito Santo, Brazil: distribution, morphology, illustration and new occurrences

Abstract

Euphorbiaceae is one of the largest and more complex families of angiosperms with 6,745 species and 218 genera. Dalechampia comprises approximately 130 species, with pantropical distribution, the genus presents pseudantial inflorescence with bilateral symmetry, and this characteristic differs from the others taxons in the family. Were registered 15 Dalechampia species for Espiríto Santo, of which D. margarethiae until then, it was endemic of state recording here a new occurrence for the state of Minas Gerais. Dalechampia leandrii, D. micromeria, and D. stipulacea constitute new records for the state. After expeditions in the field to observe and collect samples, bibliographic revision, and examination of herbarium specimens, we present a synopsis of Dalechampia from Espirito Santo state, in which we provide morphological illustration, an identification key, distribution maps, and comments about each taxon.

Key words Dalechampiinae; flora; taxonomy; twining vines

Resumo

Euphorbiaceae é uma das maiores e mais complexas famílias de angiospermas com 6.745 espécies e 218 gêneros. Dalechampia compreende aproximadamente 130 espécies, com distribuição pantropical. Dalechampia apresenta inflorescência pseudantial com simetria bilateral, característica esta que difere o gênero dos demais da família. Foram registradas 15 espécies de Dalechampia para o Espírito Santo, das quais D. margarethiae até então, era endêmica do estado, e aqui registramos uma nova ocorrência para o estado de Minas Gerais. Dalechampia leandrii, D. micromeria e D. stipulacea constituem novos registros para o estado. Após expedições em campo para observação e coleta de amostras, revisão bibliográfica e análise de espécimes de herbário, nós apresentamos uma sinopse de Dalechampia do Espírito Santo, na qual fornecemos ilustração morfológica, chave de identificação, mapas de distribuição e comentários sobre cada táxon.

Palavras-chave Dalechampiinae; flora; taxonomia; trepadeiras

Introduction

Euphorbiaceae Juss. is one of the largest and most complex families of Angiosperms (Webster 1994; Wurdack et al. 2005) with about 6,745 species and 218 genera (APG IV 2016). It presents greater diversity in tropical and subtropical regions, especially in the American and African continents (Lucena et al. 2009). Based on molecular studies (Chase et al. 2002; Wurdack et al. 2005; Davis et al. 2007; Wurdack & Davis 2009), Euphorbiaceae s.s. was classified into four subfamilies: Acalyphoideae, Cheilosoideae, Crotonoideae and Euphorbioideae.

Acalyphoideae comprises 20 tribes, 99 genera, and approximately 1,865 species (Webster 1975, 1994; APG IV 2016). The genera with the highest species richness in the subfamily are: Acalypha (430 species), Macaranga (260), Tragia (170), Dalechampia (ca.130), Mallotus (115), Claoxylon (80), Bernardia (50) and Ditaxis (45) (APG IV 2016). Among the tribes of Acalyphoideae, Plukenetieae deserves to be highlighted because it comprises 17 genera and more than 350 species widely distributed in tropical regions (Gillespie 1994; Webster 1994; Govaerts et al. 2000; Radcliffe-Smith 2001).

According to Webster (1994, 2014), Plukenetieae comprises the subtribes Dalechampiinae, Plukenetiinae and Tragiinae. Dalechampiinae contains only Dalechampia, classified into six sections and approximately 130 species with Pantropical distribution (Webster 1994; Pereira-Silva et al. in prep.). In Brazil, ca. 72 species are registered, of which 48 are endemic (Pereira-Silva et al. 2020a). According to Pereira-Silva et al. (2020a), in Espírito Santo state, 10 species of the genus are registered, however information on the distribution of taxa in this state is scarce. Dalechampia is the unique genus of Euphorbiaceae that presents pseudantial inflorescence with bilateral symmetry, thus it is easy to identify the genus, although identification at a specific level is difficult (Pax & Hoffmann 1919; Webster & Armbruster 1991; Webster 1994; Souza et al. 2010).

Many studies have been conducted by Pereira-Silva in Madagascar and Neotropical region, as well as by Mendes et al. (2021) in Amazon beyond the discovery of new species (Pereira-Silva et al. 2016, 2019, 2020b, 2020c, in prep.; Athiê-Souza et al. 2019; Pereira-Silva 2019; Mendes et al. 2019, 2020, 2021). Thus, as part of the studies in Neotropical Dalechampia (Pereira-Silva et al. in prep.), here we present a synopsis of the species occurring in the Espírito Santo state, as well as an identification key, character illustration, distribution maps, and comments about each taxon.

Materials and Methods

Study area

The Espírito Santo state is located in the southeastern region of Brazil and comprises an area of 97,123 km² (IBGE 2018). It presents quite rugged relief and altitudes that range from sea level in the eastern portion of the state to 2,897 meters at Pico da Bandeira, one of the highest points in Brazil. The entire state is covered by the phytogeographic domain Mata Atlântica, and due to the tremendous altitudinal variation, geological formation, and climatic variables, the state has a high diversity of vegetation formations (IBGE 2004; Garbin et al. 2017). Here we will follow the classification proposed by Fraga et al. 2019 (with one modification, we used the regional term Campos Nativos instead of Campinarana, like Garbin et al. 2017), where the state’s vegetation is classified in Seasonal Semideciduous Forest (Fig. 1a), Ombrophilous Dense Forest (Fig. 1b), Ecological Refuges (including Hight Grassland) (Fig. 1c, e), Pioneer Formations (Fig. 1d), Campos Nativos (Fig. 1f), and transition areas.

Figure 1
a-f. Different types of vegetation found in the state of Espírito Santo – a. seasonal semideciduous forest in the municipality of Marilândia; b. ombrophilous dense forest in Parque Nacional do Caparaó; c. ecological refuge (High Grassland) in Parque Nacional do Caparaó; d. pioneer formations in the municipality of Linhares; e. aspect of a stretch of ecological refuge in Parque Nacional do Caparaó; f. Campos Nativos in Natural Reserva Vale (Photos: a. Narcísio Bigio; b-c. Guilherme Peres Coelho; d. Josimar Külkamp; e. Lucas Daneu; f. Karinne Valdemarin).

The climate in the state has two well-defined areas, the low altitude region predominates high temperatures and a pronounced seasonality in winter, while in the region of altitudes above 1,000 meters, the temperatures are milder, and there is not defined seasonality (Alvares et al. 2014). The Espírito Santo state has ten Conservation Units (UCs) in the Integral Protection category, with six state Parks, two natural monuments, a National Park, a Biological Reserve, and a Private Reserve of National Heritage (IEMA 2021).

Synopsis Treatment

The preparation of this synopsis was based on field expeditions, bibliographic consultations, review of collections of national and international herbariums, mainly the state herbariums CVRD, MBML, and VIES (acronyms according to Thiers, continuously updated) in physical and virtual form, resulting in the analysis about of 100 specimens. The spelling of the taxon authors follows the International Index of Plant Names - IPNI (<https://www.ipni.org/>), while the systematic arrangement and morphology are based on Webster & Armbruster (1991) and Pereira-Silva et al. (2020d).

The identification of the specimens and the identification key was carried out with the aid of specific bibliography, information collected in the field, and herbarium specimens. Specimen analyses were performed with a digital caliper and stereomicroscope. The distribution map was generated in QGis v. 2.18.2 (QGIS Development Team 2017).

Results and Discussion

In Espírito Santo, Dalechampia is represented by 15 species, classified into three sections and three subsections (Tab. 1). Dalechampia margarethiae Pereira-Silva & Armbr. which until then was endemic to Espírito Santo, was recorded for Minas Gerais state, while D. leandrii Baill., D. micromeria Baill. and D. stipulacea Müll.Arg. constitute new records for the state. Pereira-Silva et al. (2020a), mention the occurrence of D. sylvestris S. Moore erroneously for Espirito Santo and Webster & Armbruster (1991), they mention D. armbrusteri Webster, since none of the specimens were found, these species were excluded from this synopsis.

Table 1
Dalechampia species with occurrence in Espírito Santo state, Brazil.

Táxon
Sect. Dalechampia
	Subsect. Convolvuloides G.L.Webster & Armbr.
		Dalechampia convolvuloides Lam.
		Dalechampia leandrii Baill.
	Subsect. Dalechampia
		Dalechampia brasiliensis Lam.
		Dalechampia ficifolia Lam.
		Dalechampia stipulacea Müll.Arg.
		Dalechampia viridissima Webster
	Subsect. Triphyllae (Pax & K.Hoffm.) G.L.Webster & Armbr.
		Dalechampia clausseniana Baill.
		Dalechampia micromeria Baill.
		Dalechampia triphylla Lam.
Sect. Dioscoreifoliae Pax & K.Hoffm.
		Dalechampia alata Müll.Arg.
		Dalechampia margarethiae Pereira-Silva & Armbr.
		Dalechampia peckoltiana Müll.Arg.
		Dalechampia pentaphylla Lam.
		Dalechampia sp.
Sect. Tiliifoliae G.L.Webster & Armbr.
		Dalechampia ilheotica Wawra

Previously some specimens (e.g., B.S. Mendes et al. 177 & 186; B.N. Melo et al. 78; H.Q.B. Fernandes et al. 3328; A. Alves-Araújo et al. 1638) were identified as D. scandens L., but here we recognized the specimens of the collector number [177, 186, 78] as D. peckoltiana Müll.Arg., the number [3328] as D. brasiliensis Lam. and [1638] as D. ficifolia Lam., thus excluding the occurrence of D. scandens for the state. Dalechampia ficifolia (29 specimens), D. peckoltiana (20), D. brasiliensis (13), D. margarethiae (12) and D. pentaphylla Lam. (9), in this order, they are the most representative species.

Dalechampia species are distributed throughout Espirito Santo and in almost all vegetations. Ombrophilous Dense Forest has the most significant number of Dalechampia species registered, 13 species (D. alata, D. brasiliensis, D. clausseniana, D. convolvuloides, D. ficifolia, D. ilheotica, D. leandrii, D. margarethiae, D. peckoltiana, D. pentaphylla, D. stipulacea, D. triphylla and D. viridissima), following by Pioneer Formations with ten species (D. brasiliensis, D. clausseniana, D. convolvuloides, D. ficifolia, D. ilheotica, D. leandrii, D. margarethiae, D. micromeria, D. peckoltiana and D. stipulacea); the Seasonal Semideciduous Forest six species (D. brasiliensis, D. clausseniana, D. ficifolia, D. peckoltiana, D. triphylla and Dalechampia sp.); the transition areas with four species (D. brasiliensis, D. ficifolia, D. peckoltiana and D. pentaphylla); while the Ecological Refuges and Campos Nativos there is no records of collections (Fig. 2).

Figure 2
a-c. Geographic distribution of Dalechampia species in Espírito Santo state – a. Dalechampia micromeria, D. ficifolia, D. sp, D. leandrii, D. clausseniana, D. alata; b. D. stipulacea, D. convolvuloides, D. pentaphylla, D. viridissima, D. peckoltiana; c. D. ilheotica, D. brasiliensis, D. triphylla, D. margarethiae.

We found four species collected in six different UCs (Tab. 2), the most frequent is D. ficifolia. We point out that in Espírito Santo there are no endangered Dalechampia species (Fraga et al. 2019).

Table 2
Species that occur in protected áreas.

Conservation unit	Species
Biological Reserve Augusto Ruschi	Dalechampia ficifolia
Biological Reserve of Córrego Grande	Dalechampia ficifolia
Biological Reserve Duas Bocas	Dalechampia margarethiae
National Park of Caparaó	Dalechampia pentaphylla
Natural Reserve Vale	Dalechampia ficifolia, Dalechampia peckoltiana
State Park of Itaúnas	Dalechampia ficifolia, Dalechampia peckoltiana

Relevant morphological aspects in the identification of the taxa Vegetative characters

The species registered for the Espírito Santo are twining vines or lianas (Fig. 3a), although there is a notable variation in habit, such as erect or decumbent subshrubs, these are not found in the state, however they are quite common in the region Central-West of Brazil (Webster & Armbruster 1991; Pereira-Silva in prep.; Pereira-Silva et al. 2020c). The branches are generally striated, angular, cylindrical, and are glabrescent, pubescent, villous, or hirsute (Fig. 3b), sometimes ferruginous as in D. ficifolia (Fig. 3c). The stipules are linear, lanceolate or oblong to rounded shape (Fig. 3d), and D. stipulacea (Fig. 3e) present glandular trichomes on the margins and commonly parastipules.

Figure 3
a-i. Vegetative characters of Dalechampia species found in Espírito Santo state – a. habit of D. micromeria; b. branches of D. clausseniana; c. branches of D. ficifolia; d. bracteal stipule of D. ficifolia; e. bracteal stipule of D. stipulacea; f. leaf unilobed of D. ilheotica with details the stipels on the base; g. leaf 3-lobed of D. brasiliensis; h. leaf 3-foliolate of D. clausseniana; i. leaf 5-foliolate of D. pentaphylla with details the stipels on the base. (Photos: a. Alexandre Medeiros; b,e. Otávio Marques; c,d,g,h,i. Josimar Külkamp; f. Alex Popovkin).

The leaves are simple, unilobed (Fig. 3f) to 3-lobed (Fig. 3g), as well as they can vary from unilobed to (2) 3-lobed in the same branch and compound 3–5-foliolate (Fig. 3h-i). Leaflets present acute, rounded, or caudate apex and attenuated, corded or oblique base. Margins are entire to serrated and sometimes with glandular trichomes as in D. stipulacea. On the base of leaves there is a pair of stipels, with a linear shape (see detail of Fig. 3f), oblong or lanceolate (see detail of Fig. 3i), most are pubescent, with glands on margins or bases, sometimes deciduous and are present in all species of the genus (Pereira-Silva 2019).

The species present simple trichomes, unicellular, stinging or glandular (Webster & Armbruster 1991). Most of the species show stinging trichomes; the glandular trichomes are less common and easily visible, thus presenting great taxonomic importance for D. stipulacea.

Reproductive characters

In Dalechampia the pseudantial inflorescence are usually colored, composed of a pleiochasium and pistillate cymule, as well as a resin gland (Fig. 4a,d) (Armbruster 1996; Pereira-Silva et al. 2020c). The species registered in this study present greenish, whitish, creamy, or pink to purplish involucral bracts; entire, 3-spit, 3-lobed, 3-toothed or deeply 3–5-lobed (see Figs. 4-6). Each bract has a pair of stipules clearly homologous to the leaves, with different shapes (Fig. 3b).

Figure 4
a-g. Reproductive characters of Dalechampia stipulacea found in Espírito Santo state – a. inflorescence (ib = involucral bract; mb = button staminate); b. details of the bracteal stipules (bs); c. staminate pleiochasium (se = sepals; st = stamens; tb = staminal tube); d. staminate pleiochasium with details (pd = peduncle; sb = staminate bracteoles; gl = resiniferous glands); e. pistillate cymule (se = sepals; sc = stylar column; sg = apex); f. fruit; g. fruit with details the presence of bracts, staminate sepals, and the stylar column (Photos: a. Otávio Marques; b,c,d,e,f,g. Josimar Külkamp).

The staminate pleiochasium is more complex than pistillate (Webster & Armbruster 1991). The taxa studied here present staminate bracteole free, connates to bilabiate or fused at the base and contain 7–15 staminate flowers, plus an adjacent resin gland (Fig. 4c,d). In the Convolvuloides and Dalechampia sections, the resin gland is laminar with entire apex, while in the Dioscoreifoliae section it is fimbriated, and in the Tiliifoliae section the gland is laminar with fimbriated or lacerated apex (Webster 1989; Pereira-Silva in prep.).

The pistillate cimules, typically in a contracted 3-flowered (Fig. 4e) with 1–3 bracteoles, 1 more external and two internal, with different shapes, which protect the three pistillate flowers. Each pistillate flower possesses 6–12 lanceolate sepals, often pinnatifid, glandular trichomes on the margins or rarely entire margins. The apex of the stylar column most common are lobed, discoid, dilated, peltate, and terete, in addition variations of these shapes are found in D. hassleriana which is unilaterally dilated.

The fruits (Fig. 4f) are capsules with explosive dehiscence (Gillespie & Armbruster 1997), with stylar column and sepals persistent, the involucral bract is rarely persistent (Fig. 4g). Finally, the seeds of the Brazilian Dalechampia are often globose to subglobose (Pereira-Silva et al. 2020a), rarely apiculate as in D. macrobractea R.A. Pereira-Silva & Armbr. an African species (Pereira-Siva et al. 2020d).

Key to Dalechampia species from Espírito Santo state

• 1. Leaves simple...................2

  • 2. Leaves unlobed...................3

    • 3. Involucral bracts deeply 3–5-lobed; 6 pistillate sepals, entire.........................................................8. Dalechampia margarethiae

    • 3’. Involucral bracts unlobed to moderately 3-lobed or 3-toothed; 12 pistillate sepals, pinnatifid or laciniate...................4

      • 4. Involucral bracts velutinous; resiniferous gland lacerate...................6. Dalechampia ilheotica

      • 4’. Involucral bracts hirsute or sparsely pubescent; resiniferous gland laminar...................5

        • 5. Leaves cordiform; bracteal stipule ovate; apex of the stylar column discoid.........................................................4. Dalechampia convolvuloides

        • 5’. Leaves ovate; bracteal stipule lanceolate; apex of stylar column slightly lobed.........................................................7. Dalechampia leandrii

  • 2’. Leaves lobed...................6

    • 6. Leaves 3-lobed or varying between unlobed to 3-lobed...................7

      • 7. Involucral bracts unlobed (rarely 2–3-lobed); resiniferous gland lacerate.........................................................6. Dalechampia ilheotica

      • 7’. Involucral bracts exclusively 3-lobed; resiniferous gland laminar...................8

        • 8. Pistillate sepals sub entire; apex of stylar column unlobed to slightly lobed.........................................................14. Dalechampia viridissima

        • 8’. Pistillate sepals pinnatifid; apex of stylar column discoid or lobed...................9

          • 9. Parastipules present on the petiolar stipule; stipitate glandular trichomes present in the margin of petiolar stipules, leaf and, involucral bracts.........................................................12. Dalechampia stipulacea

          • 9’. Parastipules absent on the petiolar stipule; stipitate glandular trichomes absent in the margin of petiolar stipules, leaf and, involucral bracts...................10

            • 10. Villous branches; membranaceous leaves; oblong to ovate leaves; lanceolate stipules; stylar column 4–5 mm long, apex lobed.........................................................2. Dalechampia brasiliensis

            • 10’. Pubescent branches; chartaceous or coriaceous leaves; rounded to oblong stipules; stylar column 7–9 mm long, apex discoid to 3-lobed......................................5. Dalechampia ficifolia

    • 6’. Leaves deeply 5-lobed...................11

      • 11. Involucral bracts pink to purplish; stigma crateriform...................15. Dalechampia sp.

      • 11’. Involucral bracts greenish; stigma clavate...................1. Dalechampia alata

• 1’. Leaves compound...................12.

  • 12. Leaves 3-foliolate...................13

    • 13. Pistillate flowers with 6 sepals...................14

      • 14. Involucral bracts more than 4 cm long; pistillate sepals, lanceolate.........................................................10. Dalechampia peckoltiana

      • 14’. Involucral bracts 2−2.4 cm long; pistillate sepals pinnatifid.........................................................13. Dalechampia triphylla

    • 13’. Pistillate flowers with 7–12 sepals...................15

      • 15. Leaflet 0.5–0.7 cm wide; involucral bracts moderately 3-toothed; apex of the stylar column cylindrical...................9. Dalechampia micromeria

      • 15’. Leaflet 2–3.5 cm wide; involucral bracts moderately 3-lobed; apex of stylar column unilaterally dilated...................3. Dalechampia clausseniana

  • 12’. Leaves 5-foliolate...................11. Dalechampia pentaphylla

Dalechampia L., Species Plantarum, 2: 1054. 1753. Type: Dalechampia scandens L.

1. Dalechampia alata Müll.Arg. Linnaea 34: 220. 1865. Fig. 5a

Figure 5
a-f. Inflorescences of Dalechampia species found in Espírito Santo state – a. D. alata; b. D. brasiliensis; c. D. clausseniana; d. D. convolvuloides; e. D. ficifolia; f. D. ilheotica (Photos: a. João Zorzanelli; b,c,e. Josimar Külkamp; d. Rafaela Pereira; f. Jone Mendes).

Dalechampia alata is easily recognized by its pistillate sepals laciniate, and clavate stigma. However, it is very close to D. pentaphylla (Pereira-Silva et al. 2020c). Dalechampia pentaphylla and D. alata have similar shaped leaves. However, D. alata has deeply 5-lobed leaves (vs. 5-foliolate), involucral bracts 3-lobed (vs. 3–5 deeply lobed), pistillate sepals laciniate (vs. pinnatifid), and apex of stigma clavate (vs. terete).

Selected specimens: Santa Teresa, 19.VII.2000, fl. and fr., A.P. Fontana et al. 21 (MBML).

Dalechampia alata are endemic of Brazil, registered in the Northeast (Bahia, Pernambuco), and Southeast (Espírito Santo, Rio de Janeiro, São Paulo (Webster & Armbruster 1991; Pereira-Silva et al. 2020a). In Espírito Santo has one record in the northern region, occurring in the Ombrophilous Dense Forest vegetation (Fig. 2a), growing on the forest edges.

2. Dalechampia brasiliensis Lam., Méthodique, Botanique 2: 258. 1786. Fig. 5b

Dalechampia brasiliensis is characterized by villous branches and linear bracteal stipules. In state, D. brasiliensis is morphologically similar to D. ficifolia, both present simple leaves, 3-lobed and involucral bracts 3-lobed, pale greenish. Dalechampia brasiliensis has villous branches (vs. pubescent), lanceolate stipules (vs. rounded to oblong), membranaceous leaves (vs. chartaceous or leathery), oblong to ovate leaves (vs. linear), and apex of the lobed stigma (vs. discoid to 3-lobed). Dalechampia brasiliensis is popularly known as “cipó de fogo” in Espírito Santo state.

Selected specimens: Santa Leopoldina, 11.IV.2009, fl. and fr., A.P. Fontana et al. 5869 (MBML).

Dalechampia brasiliensis is endemic from Brazil, registered in the Northeast (Paraíba, Pernambuco) and Southeast (Espírito Santo, Minas Gerais, Rio de Janeiro, São Paulo) regions (Webster & Armbruster 1991; Pereira-Silva et al. 2020a). In Espírito Santo, it is distributed in the Ombrophilous Dense Forest, Pioneer Formations, Seasonal Semideciduous Forest, and Transitions Areas (Fig. 2c). This species is widely distributed in the state, growing preferably on the forests edges.

3. Dalechampia clausseniana Baill. Adansonia, 5: 310. 1865. Fig. 5c

Dalechampia clausseniana is characterized by compound leaves, 3-foliolate, involucral bracts moderately 3-lobed, and apex of stylar column unilaterally dilated. In Espírito Santo this species is similar to D. triphylla, both have 3-foliolate leaves. Dalechampia clausseniana is distinguished by 7–12 pistillate sepals pinnatifid (vs. widely pinnatifid), the apex of the stylar column unilaterally dilated (vs. apex moderately lobed).

Selected specimens: Domingos Martins, 8.II.1973, fl. and fr., G. Hatschbach et al. 31379 (MBM, US, NY, MO). Santa Teresa, São Lourenço, Mata Fria, 7.IV.1999, fl., L. Kolmmann et al. 2442 (MBML).

Dalechampiaclausseniana are endemic from Brazil, registered in the Central-West (Goiás), and Southeast (Espírito Santo, Rio de Janeiro, and São Paulo) regions (Webster & Armbruster 1991). In Espírito Santo, the species is found in Ombrophilous Dense Forest, Pioneer Formations, Seasonal Semideciduous Forest (Fig. 2a), growing on the forest edges.

4. Dalechampia convolvuloides Lam. Encycl. Methodique, Botanique, 2: 256, 1786. Fig. 5d

In Espírito Santo, D. convolvuloides is morphologically similar to D. leandrii due to unlobed leaves. However, D. convolvuloides can be differentiated by cordiform leaves (vs. ovate), bracteal stipule ovate (vs. lanceolate), and apex of stylar column discoid (vs. slightly lobed).

Selected specimens: Santa Teresa, 8.V.1984, fl. and fr., R.M. Piziolo 52 (MBML).

Dalechampia convolvuloides are endemic from Brazil, registered in Northeast (Bahia) and Southeast (Espírito Santo and Rio de Janeiro) (Webster & Armbruster 1991; Pereira-Silva et al. 2020a). In Espírito Santo, the species grows in Pioneer Formation (Guarapari) and in Ombrophilous Dense Forest (Santa Teresa) (Fig. 2b), growing on the forest edges.

5. Dalechampia ficifolia Lam., Encyclopédie Méthodique, Botanique 2: 258. 1786. Fig. 5e

Dalechampia ficifolia is characterized by presenting leaves 3-lobed, similar to D. brasiliensis. These species can be differentiated by present pubescent branches (vs. villous), rounded to oblong stipules (vs. lanceolate), chartaceous or leathery leaves (vs. membranaceous), linear leaves (vs. oblong to ovate), and the apex of the stigma discoid to 3-lobed (vs. lobed). This species is popularly known as “cipó urtiga” in Espírito Santo.

Selected specimen: Conceição da Barra, 17.X.2019, fl., A.F.A. Scheidegger et al. 117 (VIES).

Dalechampia ficifolia is endemic from Brazil and widely distributed. Registered in the regions Central-West (Goiás, Mato Grosso), Northeast (Bahia, Pernambuco), Southeast (Espírito Santo, Minas Gerais, Rio de Janeiro, São Paulo), and Southern (Paraná, Santa Catarina) (Webster & Armbruster 1991; Pereira-Silva et al. 2020a). In Espírito Santo is the most widely distributed species, occurs in the Ombrophilous Dense Forest, Pioneer Formation, Seasonal Semideciduous Forest, and Transitions Areas (Fig. 2a). This species grows on the forest edges and rocky outcrops.

6. Dalechampia ilheotica Wawra, Oesterr. Bot. Z., 13: 222. 1863. Fig. 5f

Dalechampia ilheotica differs from the other species in the state by presenting coriaceous to membranaceous leaves, which can be simple, unlobed to 2–3-lobed in the same individual, prominent veins, besides having velutine involucral bracts, usually with entire apex and apex of the stigma crateriform. This species is known in Espírito Santo as “urtiga branca”.

Selected specimen: Vila Velha, 7.II.1975, fl., M. Sazima & I. Sazima 170 (UEC).

Dalechampia ilheotica are endemic from Brazil, being registered for the Northeast (Bahia, Pernambuco) and Southeast (Espírito Santo) regions (Webster & Armbruster 1991; Pereira-Silva et al. 2020a). In Espírito Santo D. ilheotica is restricted in Ombrophilous Dense Forest and Pioneer Formation (Fig. 2c), growing mainly at the forest edges.

7. Dalechampia leandrii Baill., Adansonia 5: 315. 1865. Fig. 6a

Figure 6
a-h. Inflorescences of Dalechampia species found in Espírito Santo state – a. D. leandrii; b. D. margarethiae; c. D. micromeria; d. D. peckoltiana; e. D. pentaphylla; f. D. stipulacea; g. D. triphylla; h. D. sp. (Photos: a. Juliano R. Fabricante; b. Otávio Marques; c. Alexandre Medeiros; d,e. Antônio Farias; f,g. Josimar Külkamp; h. André S. Pellanda).

Dalechampia leandrii is characterized by presenting unilobed leaves with undulate margins and involucral bracts entire to 3-lobed. It is similar to D. convolvuloides by ovate leaves (vs. cordiform), bracteal stipule lanceolate (vs. ovate), and apex of stylar column slightly lobed (vs. discoid).

Selected specimen: Conceição da Barra, 20.II.2019, fl. and fr., R. Nichio-Amaral et al. 590 (VIES).

Dalechampia leandrii are endemic from Brazil, registered for the Northeast (Paraíba), Southeast (Espírito Santo, São Paulo, Rio de Janeiro), and Southern (Paraná) regions (Webster & Armbruster 1991; Pereira-Silva et al. 2020a). Here we present the first records of D. leandrii for Espírito Santo (Fig. 2a). In the state, it is found in Ombrophilous Dense Forest (Conceição da Barra) and in Pioneer Formation (Gururi and Viana) (Fig. 5a), growing on the forest edges.

8. Dalechampia margarethiae Pereira-Silva & Armbr., Systematic Botany 44(4): 832-837. 2019. Fig. 6b

Dalechampia margarethiae is recognized by its leaves unlobed, cordiform, involucral bracts deeply 3–5-lobed usually in the same individual, staminate column not elongated and staminate sepals slightly open after anthesis. Dalechampia margarethiae is very similar to D. peckoltiana due to the shapes of the stylar column, resiniferous gland, and pistillate sepals. Dalechampia margarethiae differ by present entire leaves (vs. 3-foliolate), involucral bracts deeply 3–5-lobed (vs. involucral bracts 3-lobed), and slightly open sepals in the staminate flowers at anthesis (vs. widely open).

Selected specimen: Serra, 22.I.2013, fl., P.H.D. Barros et al. 129 (VIES).

Additional specimen: BRAZIL. Minas Gerais: Marliéria, Parque Estadual do Rio Doce, trilha do Vinhático, 29.III.1996, fl., J.A. Lombardi et al.1163 (BHCB).

Dalechampia margarethiae were endemic from Espírito Santo state (Pereira-Silva et al. 2019), here we present a new record of the species for Minas Gerais state. In Espírito Santo, Dalechampia margarethiae occurs in Ombrophilous Dense Forest (Fig. 2c), growing on the forest edges.

9. Dalechampia micromeria Baill., Adansonia 5: 310. 1865. Fig. 6c

Dalechampia micromeria is easily identified by a set of morphological characters that differentiate from other species with 3-foliolate from Espírito Santo, and these are: leaves with 3.5–4 cm long (vs. 5–10 cm long in the others species); involucral bracts moderately 3-toothed (vs. moderately 3-lobed or 3-lobed); stylar column in flower 3 mm long (vs. 0.4–1.8 cm long). The stylar column can variate in size when these are in the fruits.

Selected specimen: Vila Velha, 5.III.2001, fl., P. Fiaschi et al. 652 (SPF).

Dalechampia micromeria occurs in Brazil, registered for the Southeast (Espírito Santo, Minas Gerais, Rio de Janeiro and São Paulo), Southern (Paraná, Rio Grande do Sul, Santa Catarina), and in Paraguay (Cordillera de Altos) (Webster & Armbruster 1991; Pereira-Silva et al. 2020d). Here we present the first record of D. micromeria for Espírito Santo (Fig. 2a). It is found in Pioneer Formation (Vila Velha) (Fig. 5a), growing in a dense shrubby sandbank, with an abundance of Allagoptera arenaria (Gomes) Kuntze and Bromelia balansae Mez.

10. Dalechampia peckoltiana Müll.Arg., Fl. bras. 11(2): 647. 1874. Fig. 6d

Dalechampia peckoltina can be recognized by the presence of involucral bracts monomorphic, always 3-lobed, and staminate sepals widely open. It is similar to D. margarethiae, and differs from this by the presence of 3-foliolate leaves (vs. entire), involucral bracts 3-lobed (vs. deeply 3–5-lobed), and widely open sepals in the staminate flowers at anthesis (vs. slightly open). The species is known as “urtiga mirim” in Espírito Santo.

Selected specimen: Conceição da Barra, 18.VII.2019, fl. and fr., B.N. Mello et al. 204 (VIES).

Endemic species from Brazil, registered in the Northeast (Alagoas, Bahia, Pernambuco and Sergipe), and Southeast (Espírito Santo, Minas Gerais, Rio de Janeiro) (Webster & Armbruster 1991; Pereira-Silva et al. 2020a). In the Espírito Santo, this species occurs in all vegetation types in Espirito Santo, except in Ecological Reguge (Fig. 2b), growing on the forest edges.

11. Dalechampia pentaphylla Lam., Encycl. 2: 258. 1786. Fig. 6e

Dalechampia pentaphylla is recognized by leaves 5-foliolate, involucral bracts deeply 3‒5-lobed. It is similar to D. alata, and can be differentiated by 5-foliolate leaves (vs. 5-lobed), involucral bracts 3–5 deeply lobed (vs. 3-lobed), pistillate sepals pinnatifid (vs. laciniate), and apex of stigma terete (vs. clavate).

Selected specimen: Iúna, 7.I.2013, fl., J.P.F. Zorzanelli & G. Graciliano 614 (VIES).

Dalechampia pentaphylla occurs in Brazil and Paraguay. In Brazil is registered in the Central-West (Goiás, Mato Grosso do Sul), Northeast (Bahia), Southeast (Espírito Santo, Minas Gerais, Rio de Janeiro and São Paulo), and Southern (Paraná) regions (Webster & Armbruster 1991; Pereira-Silva et al. 2020a). In Espírito Santo it is found in the Ombrophilous Dense Forest and Transition Areas (Fig. 2b), mainly in the Serra do Valentim (Iúna), as well as in the municipalities of Conceição do Castelo, Domingos Martins, Marechal Floriano, Santa Teresa and Vargem Alta, growing on the forest edges, with altitude up to 1,900 meters.

12. Dalechampia stipulacea Müll.Arg., Linnaea, 34: 221. 1865. Fig. 6f

Dalechampia stipulacea is a very peculiar species due to present glandular trichomes in margins of leaves, petiolar stipule, bracteal stipule, and involucral bracts. This kind of trichome is very apparent in this taxon, making it different from other Dalechampia with 3-foliolate leaves. The species is known as “micuim” in Espírito Santo.

Selected specimen: Vila Velha, 21.X.1987, fl., O.J. Pereira et al. 1186 (VIES).

Dalechampia stipulacea is distributed in South America, registered in Argentina, Brazil, Colombia, Peru, Venezuela and Paraguay (Webster & Armbruster 1991). In Brazil it is registered in the Central-West (Mato Grosso do Sul), Northeast (Bahia, Maranhão, Pernambuco, Piauí), Southeast (Espírito Santo, Minas Gerais, Rio de Janeiro, São Paulo), and Southern (Paraná, Rio Grande do Sul, Santa Catarina) regions (Webster & Armbruster 1991; Pereira-Silva et al. 2020a). Here we presented the first record of D. stipulacea for Espírito Santo, where it is found in the Pioneer Areas and Ombrophilous Dense Forest (Fig. 2b), growing on the forest edges.

13. Dalechampia triphylla Lam., Encycl. 2: 258. 1786. Fig. 6g

Dalechampia triphylla is recognized by its branches, glabrescent, elongated leaflets, margins serreate, and pistillate sepals widely pinnatifid. The species is compared and differentiated in the comments of D. clausseniana.

Selected specimen: Barra de São Francisco, 21.XI.2000, fl. and fr., L. Kollmann et al. 3292 (MBML, PEUFR).

Dalechampia triphylla is distributed in Brazil, French Guiana, Mexico, and Suriname. In Brazil it is occurs in the Northeast (Bahia, Pernambuco), North (Amazonas, Roraima), Southeast (Espírito Santo, Minas Gerais, Rio de Janeiro, São Paulo), and Southern (Paraná, Santa Catarina) regions (Webster & Armbruster 1991; Funk et al. 2007; Pereira-Silva et al. 2020a). In Espírito Santo state, D. triphylla is found in Ombrophilous Dense Forest and Seasonal Semideciduous Forest (Fig. 2c). Occurs in the Municipal Park Sombra da Tarde (Barra de São Francisco), as well as in the Environmental Protection Area of ​​Pedra do Elefante (Nova Venécia), growing on the forest edges.

14. Dalechampia viridissima Webster, Brittonia 41: 6. 1989.

In all species with 3-lobed leaves, Dalechampia viridissima is easily recognized due to involucral bracts deep green, pistillate sepals subentire, and apex of stylar column unlobed to slightly lobed.

Selected specimen: Vitória, 2.II.1969, fl. and fr., D. Sucre & P.I.S. Braga 4587 (RB).

Dalechampia viridissima is endemic to Brazil, occurring in the Northeast (Bahia) and Southeast (Espírito Santo) (Webster & Ambruster 1991). In the Espírito Santo, D. viridissima is found in Ombrophilous Dense Forest (Fig. 2b). Occurs in the Municipal Park Gruta da Onça (Vitória), specifically in Morro do Vigia, growing in secondary forest, in a place with rocky outcrop.

15. Dalechampia sp. Fig. 6h

Dalechampia sp. differs from the other species registered in the state by the pink to purplish, 3–5-lobed involucral bracts, and the stigma’s apex crateriform. The deeply 5-lobed leaves are similar to Dalechampia alata, while in D. pentaphylla the leaves are 5-foliolate, but Dalechampia sp. differs from these by the pink color of the involucral bracts (vs. greenish in D. alata and D. pentaphylla). We still need to see more specimens to concluded that can be a new species. Due to its morphology, the taxon might be classified in the Dioscoreifoliae section, which presents deeply laciniate resiniferous bractlets, larger distal involucral bract and staminate involucral of free decussate bracts (Cordeiro 1998), with D. violacea Pax & K.Hoffm, from Central Brazil and D. purpurata Cordeiro endemic from Bahia.

Selected Specimen: Alegre, 21.XI.2020, fl., J.C.R. Mendes et al. 790 (PEUFR, MBML).

Dalechampia sp. occur in the Seasonal Semideciduous Forest (Fig. 2a). This taxon was registered inside a Conservation Unit (Parque Estadual Cachoeira da Fumaça) in the municipality of Alegre. The specimen was collected at the forest edges.

Acknowledgements

We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), for a doctoral grant to Jone Clebson Ribeiro Mendes (process 142316/2018-0), Josimar Külkamp (process 141707/2020-8) and Narcísio Costa Bígio (process 141313/2018-8). We also like to thank everyone that shared field images, and Amélia Tuler and Claudio Nicoletti de Fraga who gave maps shapes.

References

• Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM & Sparovek G (2014) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728.
• Armbruster WS (1996) Cladistic analysis and revision of Dalechampia sections Rhopalostylis and Brevicolumnae (Euphorbiaceae). Systematic Botany 21: 209-235. <https://doi.org/10.2307/2419748>.
• APG IV - Angiosperm Phylogeny Group (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1-20.
• Athiê-Souza SM, Pereira-Silva RA, Sales MF & Armbruster WS (2019) Nomenclatural update of Dalechampia sect. Dioscoreifoliae (Euphorbiaceae). Kew Bulletin 74: 44.
• Chase MW, Zmarzty S, Lledó MD, Wurdack KJ, Swensen SM & Fay MF (2002) When in doubt, put it Flacourtiaceae: a molecular phylogenetic analysis based on plastid rbcL DNA sequences. Kew Bulletin 57: 141-181.
• Davis CC, Latvis M, Nickrent DL, Wurdack KJ & Baum DA (2007) Floral gigantism in Rafflesiaceae. Science 315: 1812.
• Fraga CN, Peixoto AL, Leite YLR, Santos ND, Oliveira JRPM, Sylvestre LS, Schwartsburd PB, Tuler AC, Freitas J, Lírio EJ, Couto DR, Dutra VF, Waichert C, SobrinhoTG, Hostim-Silva M, Ferreira RB, Bérnils RS, Costa LP, Chaves FG, Formigoni, MG, Silva JP, Ribeiro RS, Reis JCL, Capellão RT, Lima RO & Saiter FZ (2019) Lista da fauna e flora ameaçadas de extinção no estado do Espírito Santo. In: Fraga CN, Formigoni MH & Chaves FG (2019) Fauna e flora ameaçadas de extinção no estado do Espírito Santo. Instituto Nacional da Mata Atlântica, Santa Teresa. Pp. 343-397.
• Garbin ML, Saiter FZ, Carrijo TT & Peixoto AL (2017) Breve histórico e classificação da vegetação capixaba. Rodriguésia 68: 1883-1894. <https://doi.org/10.1590/2175-7860201768521>.
• Gillespie LJ & Ambruster WS (1997) A contribution to the Guianan Flora: Dalechampia, Haematostemon, Omphalea, Pera, Plukenetia and Tragia (Euphorbiaceae) with notes on subfamily Acalyphoideae. Smithsonian Contributions to Botany 86: 1-48. DOI: https://doi.org/10.5962/bhl.title.103726
  » https://doi.org/https://doi.org/10.5962/bhl.title.103726
• Gillespie LJ (1994) Pollen morphology and phylogeny of the tribe Plukenetieae (Euphorbiaceae). Annals of the Missouri Botanícal Garden 81: 317-348.
• Govaerts R, Frodin DG & Radcliffe-Smith A (2000) World checklist and bibliography of Euphorbiaceae (and Pandaceae). Vol. 2. Royal Botanical Gardens, Kew. 420p.
• IBGE - Instituto Brasileiro de Geografia e Estatística (2004) Mapa de vegetação do Brasil. 3ª ed. Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro. Available at <ftp://ftp.ibge.gov.br/ Cartas_e_Mapas/Mapas_Murais/>. Access on 24 January 2021.
  » ftp://ftp.ibge.gov.br/ Cartas_e_Mapas/Mapas_Murais/
• IBGE - Instituto Brasileiro de Geografia e Estatística (2018) Área territorial brasileira. Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro. Available at <https://www.ibge.gov.br/cidades-e-estados.html?view=municipio>. Access on 24 January 2021.
  » https://www.ibge.gov.br/cidades-e-estados.html?view=municipio
• IEMA - Instituto Estadual de Meio Ambiente (2021) Unidades de conservação no estado do Espírito Santo. Available at <https://iema.es.gov.br/unidades-de-conservacao>. Access on 24 January 2021.
  » https://iema.es.gov.br/unidades-de-conservacao
• Lucena MFA, Amorim BS & Alves M (2009) Sinopse das espécies de Euphorbiaceae s.l do Parque Nacional Serra de Itabaiana, Sergipe, Brasil. Revista Caatinga 22: 214-224.
• Mendes JCR, Secco RS, Bigio NC & Rosario AS (2019) Lectotypifications, new synonyms and new occurrences of Dalechampia L. (Euphorbiaceae) in Brazil. Phytotaxa 415: 189-198.
• Mendes JCR, Pereira-Silva RA, Athiê-Souza SM, Bigio NC, Armbruster WS, Secco RS & Sales MF (2020) The genus Dalechampia L. (Euphorbiaceae) from Brazil. Catalogue Field Museum, version 1, 6/2020, Chicago. 1122p.
• Mendes JCR, Rosario AS, Bigio NC, Pereira-Silva RA & Secco RS (2021) Dalechampia L. (Euphorbiaceae) in the Brazilian Amazon. Biota Neotropica 21: e20201010.
• Pax F & Hoffmann K (1919) Euphorbiaceae - Dalechampia. In: Engler A (ed.) Das Pflanzenreich IV - 147. XII (Heft 68): 1-59.
• Pereira-Silva RA, Athiê-Souza SM, Secco RS, Melo AL & Sales MF (2016) Dalechampia erythrostyla (Euphorbiaceae), a New Species from Northeastern Brazil. Systematic Botany 41: 989-995.
• Pereira-Silva RA, Mendes JCR, Athiê-Souza SM, Melo AL, Sales MF, Souza LGR & Armbruster WS (in preparation) Taxonomic revision of Neotropical species of Dalechampia sect. Dalechampia (Euphorbiaceae).
• Pereira-Silva RA, Athiê-Souza SM, Secco RS, Melo AL, Sales MF & Armbruster WS (2019) Dalechampia margarethiae (Euphorbiaceae), a new species from Southeastern Brazil. Systematic Botany 44: 832-837.
• Pereira-Silva RA, Oliveira JCP, Mendes JCR, Bigio NC, Secco RS, Gama BRA, Silva DF, Leal BA, Melo AL, Athiê-Souza SM, Sales MF & Cordeiro WPFS (2020a) Dalechampia In: Flora do Brasil 2020. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. Available at <http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB17551>. Access on 3 March 2021.
  » http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB17551
• Pereira-Silva RA, Athiê-Souza SM, Secco RS, Melo AL & Sales MF (2020b) Dalechampia (Acalyphoideae, Euphorbiaceae) em Pernambuco (Brasil). Rodriguésia 71: 1-22.
• Pereira-Silva RA, Gama BRA, Athiê-Souza SM, Melo AL & Sales MF (2020c) Dalechampia (Euphorbiaceae, Acalyphoideae): synopsis of species from Northeast Brazil. Biota Neotropica 20: 1-16.
• Pereira-Silva RA, Athiê-Souza SM, Fabriani F, Melo AL, Sales MF & Armbruster WS (2020d) Taxonomic revision of Dalechampia (Euphorbiaceae) in Madagascar. Systematic Botany 45: 254-267.
• QGIS Development Team (2017) QGIS Geographic Information System. V. 2.18.2. Open Source Geospatial Foundation. Available at <http://qgis.osgeo.org>. Access on 1 March 2021.
  » http://qgis.osgeo.org
• Radcliffe-Smith A (2001) Genera Euphorbiacearum. Royal Botanic Gardens, Kew. 464p.
• Souza LA, Silva AC & Moscheta IS (2010) Morphology and anatomy of flowers of Dalechampia stipulacea Müll.arg. (Euphorbiaceae). Acta Botanica Venezuelica 33: 103-117.
• Thiers B [continuously updated] Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at <http://sweetgum.nybg.org/science/ih/>. Access on 4 March 2021.
  » http://sweetgum.nybg.org/science/ih/
• Webster GL & Ambruster WS (1991) A synopsis of the neotropical species of Dalechampia (Euphorbiaceae). Botanical Journal of the Linnean Society 94: 3-46.
• Webster GL (1975) Conspectus of a new classification of the Euphorbiaceae. Taxon 24: 593-601.
• Webster GL (1994) Synopsis of the genera and suprageneric taxa of Euphorbiaceae. Annals of the Missouri Botanical Garden 81: 33-144.
• Webster GL (2014) Euphorbiaceae. In: Kubitzki K (ed.) The families and genera of vascular plants. Flowering plants. Eudicots. Malpighiales. Vol. 11. Springer-Verlag, Berlin, Heidelberg. Pp. 51-216.
• Wurdack KJ, Hoffman P & Chase MW (2005) Molecular phylogenetic analysis of uniovulate Euphorbiaceae (Euphorbiaceae sensu stricto) using plastid rbcL and trnL-F DNA sequences. American Journal of Botany 92: 1397-1420.
• Wurdack KJ & Davis CC (2009) Malpighiales phylogenetics: gaining ground on one of the most recalcitrant clades in the angiosperm tree of life. American Journal of Botany 96: 1551-1570.

List of specimens

Alves-Araújo A 1638 (5), 1699 (5). Amorim AMA 7149 (8). Arbo MM 5592 (2). Assis AM 1608 (10). Barros PHD 129 (8). Boone W 859 (5). Damaceno IV 160 (5). Demuner V 448 (5), 4394 (5), 208 (12). Devecchi MF 107.0 (10). Dutra SC 42 (10). Fabris LC 18 (11). Farias GL 534 (10). Fernandes HQB 3328 (2). Fiaschi P 671 (8), 652 (9). Firmino AD 1634 (7), 991 (7). Fontana AP 21 (1), 769 (2), 5869 (2), 3378 (11). Folli DA 571 (5), 4039 (6), 4420 (10). Forzza RC 7863 (5), 5098 (2). Gomes JML 498 (5), 3245 (5), 469 (5), 110 (7), VIES32885 (10), 32 (2). Gurtler J 181 (5), 541 (6). Hashimoto G 10192 (11). Hatschbach G 51415 (5), 50689 (5), 49940 (5), 436973 (5), 51415 (5), 31379 (3), 48655 (11), CESJ74994 (11), 59744 (11). Hoehne W 5509 (2). Hoffmann WA 223 (5). Kollmann L 2376 (1), 13220 (2), 3292 (3), 1516 (5), 10176 (5), 7729 (8), 10381 (8), 3292 (13), 9036 (11). Külkamp J 1003 (2), 980 (3). Lombardi JA 9644 (5). Luber J 183 (8), 32 (13). Lucas, EJ 807 (8). Machado JO 224 (10). Magnago LFS 897 (5), 655 (10). Mansano VF 502 (6). Martinelli G 2038 (10). Martins MLL 135 (11). Martins RFA 173 (7). Mello BN 204 (10), 78 (10), 196 (10). Mendes BS 186 (10), 177 (10). Mendes JCR 790 (15). Milaneze-Gutierre MA 806 (12). Moraes PN 1 (10), 5 (10). Nichio-Amaral R 590 (7). Oliveira RM 33 (10). Pena NTL 169 (2). Pereira OJ 227 (2), 337 (2), 2257 (5), 3901 (5), 1186 (12). Pirani JR 2404 (4), 212 (5), 3030 (5), 6165 (8), 184 (8). Piziolo RM 52 (8). Queiroz LP 2482 (5), 2465 (10). Romão GO 1273 (10). Rosa LV 163 (4). São-Mateus 11 (2). Sarnaglia-Júnior VB 314 (5). Sazima M 170 (6). Saiter FZ 585 (8). Silva JM 2572 (12). Simonelli M 1308 (5). Siqueira GS 353 (6). Sobral M 4743 (10). Souza VC 23673 (11). Sucre D 4587 (14). Vervloet RR 2388 (5). Vimercat JM 322 (8). Weiler-Júnior I 190 (5). Zorzanelli JPF 614 (11).

Edited by

• Area Editor: Dra. Tatiana Carrijo

Publication Dates

• Publication in this collection
  07 Mar 2022
• Date of issue
  2022

History

• Received
  14 Mar 2021
• Accepted
  27 Aug 2021