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Duguetia rolimii (Annonaceae), a new large tree species from the Atlantic Forest of Espírito Santo, Brazil

Abstract

A new species of Duguetia from Reserva Natural Vale, in the Atlantic Forest of the Brazilian state of Espírito Santo, is described and illustrated, and an updated key to the Duguetia species from this state is presented. Duguetia rolimii is known only from two large trees, restricted to the municipality of Linhares. It resembles D. sooretamae in having young twigs densely covered with stellate scales, narrow and shiny leaves with similar dimensions, and fruits with more than 200 fertile monocarps. Nevertheless, these two species can be distinguished from each other mainly by the type of vegetation where they occur, plant size, the density of stellate scales at the lower side of the leaves, the angle between the primary and secondary leaf veins, the shape of the flower buds, length of the upper bract, the shape of the fertile monocarps and indument of the areoles. Comments on distribution, conservation status and field photos of the new species, and comparisons with other related species are provided.

Keywords:
Annonoideae; Duguetieae; Espírito Santo; Neotropical flora; Tabuleiro forest; taxonomy.

Introduction

Neotropical forests are particularly rich in plant species and endemism (Antonelli & Sanmartín 2011Antonelli A, Sanmartín I. 2011. Why Are There So Many Plant Species in the Neotropics? Taxon 60: 403-414. doi: 10.1002/tax.602010
https://doi.org/10.1002/tax.602010...
), and much of this diversity is in the Atlantic Forest, which is the second-largest rainforest in South America (Sobral-Souza & Lima-Ribeiro 2017Sobral-Souza T, Lima-Ribeiro MS. 2017. De volta ao passado: revisitando a história biogeográfica das florestas neotropicais úmidas. Oecologia Australis 21: 93-107. doi: 10.4257/oeco.2017.2102.01.
https://doi.org/10.4257/oeco.2017.2102.0...
). This domain is a biodiversity hotspot, as only 12.4% of the original forest remains (Myers et al. 2000Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J. 2000. Biodiversity Hotspot for Conservation Priorities. Nature 403: 853-858. doi: 10.1038/35002501
https://doi.org/10.1038/35002501...
; Fundação SOS Mata Atlântica & INPE 2023Fundação SOS Mata Atlântica, INPE. 2023. Atlas dos remanescentes florestais da Mata Atlântica: período 2021-2022, relatório técnico. São Paulo, Fundação S.O.S Mata Atlântica, Instituto Nacional de Pesquisas Espaciais. https://cms.sosma.org.br/wp-content/uploads/2023/05/SOSMAAtlas-da-Mata-Atlantica_2021-2022-1.pdf. 18 Nov. 2022.
https://cms.sosma.org.br/wp-content/uplo...
) and comprises a mosaic of different vegetation types mainly along the Brazilian coast (Ribeiro et al. 2009Ribeiro MC, Metzger JP, Martensen AC, Ponzoni F, Hirota MM. 2009. Brazilian Atlantic Forest: How Much Is Left and How Is the Remaining Forest Distributed? Implications for Conservation. Biological Conservation 142: 1141-1153. doi: 10.1016/j.biocon.2009.02.021
https://doi.org/10.1016/j.biocon.2009.02...
). More than 15,600 species of angiosperms are recorded in the Atlantic Forest, of which 7,580 (48.5%) are endemic (Flora e Funga do Brasil 2023Flora e Funga do Brasil. 2023. Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/. 18 Nov. 2023.
https://floradobrasil.jbrj.gov.br/...
).

The plant family Annonaceae comprises ca. 110 genera and over 2400 species of trees, shrubs and lianas, with a pantropical distribution and great diversity in Neotropical forests (Chatrou et al. 2012Chatrou LW, Pirie MD, Erkens RHJ et al. 2012. A New Subfamilial and Tribal Classification of the Pantropical Flowering Plant Family Annonaceae Informed by Molecular Phylogenetics. Botanical Journal of the Linnean Society 169: 5-40. doi: 10.1111/j.1095-8339.2012.01235.x
https://doi.org/10.1111/j.1095-8339.2012...
; 2018Chatrou LW, Turner IM, Klitgaard BB, Maas PJ, Utteridge TMA. 2018. A Linear Sequence to Facilitate Curation of Herbarium Specimens of Annonaceae. Kew bulletin 73: 1-10. doi: 10.1007/s12225-018-9764-3
https://doi.org/10.1007/s12225-018-9764-...
; Guo et al. 2017Guo X, Tang CC, Thomas DC, Couvreur TLP, Saunders RMK. 2017. A Mega-Phylogeny of the Annonaceae: Taxonomic Placement of Five Enigmatic Genera and Recognition of A New Tribe, Phoenicantheae. Scientific Reports 7: 7323. doi: 10.1038/s41598-017-07252-2
https://doi.org/10.1038/s41598-017-07252...
). In Brazil, the Atlantic Forest is the second center of diversity for this family (Lobão et al. 2020Lobão AQ, Lopes JC, Erkens RHJ, et al. 2020. Annonaceae. In: Flora e Funga do Brasil. Rio de Janeiro, Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB110219/. 13 Nov. 2023.
https://floradobrasil.jbrj.gov.br/reflor...
), as well as for Duguetia A.St.-Hil. ( Lobão & Bazante 2023Lobão AQ, Bazante ML. 2023. Duguetia. In: Flora e Funga do Brasil. Rio de Janeiro, Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/FB110296/. 13 Nov. 2023.
https://floradobrasil.jbrj.gov.br/FB1102...
), a monophyletic genus within the family (Guo et al. 2017Guo X, Tang CC, Thomas DC, Couvreur TLP, Saunders RMK. 2017. A Mega-Phylogeny of the Annonaceae: Taxonomic Placement of Five Enigmatic Genera and Recognition of A New Tribe, Phoenicantheae. Scientific Reports 7: 7323. doi: 10.1038/s41598-017-07252-2
https://doi.org/10.1038/s41598-017-07252...
; Xue et al. 2020Xue B, Guo X, Landis JB, et al. 2020. Accelerated Diversification Correlated with Functional Traits Shapes Extant Diversity of the Early Divergent Angiosperm Family Annonaceae. Molecular Phylogenetics and Evolution 142: 106659. doi: 10.1016/j.ympev.2019.106659
https://doi.org/10.1016/j.ympev.2019.106...
).

Duguetia belongs to the subfamily Annonoideae, tribe Duguetieae (Chatrou et al. 2012Chatrou LW, Pirie MD, Erkens RHJ et al. 2012. A New Subfamilial and Tribal Classification of the Pantropical Flowering Plant Family Annonaceae Informed by Molecular Phylogenetics. Botanical Journal of the Linnean Society 169: 5-40. doi: 10.1111/j.1095-8339.2012.01235.x
https://doi.org/10.1111/j.1095-8339.2012...
), and can be distinguished from other Annonaceae genera by the indument of scaly and/or stellate hairs, and by the fruit usually formed by numerous, tightly-appressed sessile monocarps, with sterile monocarps connate at the base into a collar (Maas et al. 2003Maas PJM, Westra LYTH, Chatrou LW. 2003. Duguetia (Annonaceae). New York, New York Botanical Garden Press. Vol. LXXXVIII.). Species of Duguetia are distributed throughout the Neotropics and tropical West Africa, occurring predominantly in non-flooded lowland rainforests. Few species occur in drier and nutrient-poor soils such as Duguetia dicholepidota Mart. (1841Martius CFP von. 1841. Annonaceae. In: Martius CFP von, Eichler AG, Urban I. (eds.). Flora Brasiliensis. Vol. XIII. https://florabrasiliensis.cria.org.br/search?taxon_id=523. 13 Nov. 2023.
https://florabrasiliensis.cria.org.br/se...
: 22) and D. furfuracea (A.St.-Hil.) Saff. (1914Safford WE. 1914. Classification of the genus Annona with Descriptions of New and Imperfectly Known Species. Contributions from the United States National Herbarium 18: 1-68.: 61) (Maas et al. 2003Maas PJM, Westra LYTH, Chatrou LW. 2003. Duguetia (Annonaceae). New York, New York Botanical Garden Press. Vol. LXXXVIII.). Ninety-five species are recognized in this genus (Maas et al. 2003Maas PJM, Westra LYTH, Chatrou LW. 2003. Duguetia (Annonaceae). New York, New York Botanical Garden Press. Vol. LXXXVIII.; Maas & Westra 2010Maas PJM, Westra LYT. 2010. New Species of Annonaceae from the Neotropics and Miscellaneous Notes. Blumea 55: 259-275.; Bazante & Alves 2017Bazante ML, Alves M. 2017. A New Species of Duguetia (Annonaceae) From the Atlantic Forest of Northeastern Brazil. Phytotaxa 314: 266-272. doi: 10.11646/phytotaxa.314.2.8
https://doi.org/10.11646/phytotaxa.314.2...
; Bazante et al. 2023Bazante ML, Maas PJM, Barbosa MRV. 2023. Duguetia leucotricha (Annonaceae), A New Species From the Atlantic Coastal Forest of Brazil. Acta Botanica Brasilica 37: e20220203. doi: 10.1590/1677-941X-ABB-2022-0203
https://doi.org/10.1590/1677-941X-ABB-20...
), and 18 have been reported to occur in the Atlantic Forest domain, including the recently described D. leucotricha M. L. Bazante & Maas (2023Bazante ML, Maas PJM, Barbosa MRV. 2023. Duguetia leucotricha (Annonaceae), A New Species From the Atlantic Coastal Forest of Brazil. Acta Botanica Brasilica 37: e20220203. doi: 10.1590/1677-941X-ABB-2022-0203
https://doi.org/10.1590/1677-941X-ABB-20...
: 2), endemic to Bahia (Lobão & Bazante 2023Lobão AQ, Bazante ML. 2023. Duguetia. In: Flora e Funga do Brasil. Rio de Janeiro, Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/FB110296/. 13 Nov. 2023.
https://floradobrasil.jbrj.gov.br/FB1102...
).

The states of Bahia and Espírito Santo have the greatest richness of tree species in the Brazilian Atlantic Forest, including the Annonaceae family with 62 and 55 species, respectively (Rolim et al. 2016Rolim SG, Peixoto AL, Pereira OJ, et al. 2016. Angiospermas da Reserva Natural Vale, na floresta atlântica do norte do Espírito Santo. In: Rolim SG, Menezes LFT, Srbek-Araujo AC. (eds.). Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale. Belo Horizonte, Rona Editora . p. 167-230.; Lobão et al. 2020Lobão AQ, Lopes JC, Erkens RHJ, et al. 2020. Annonaceae. In: Flora e Funga do Brasil. Rio de Janeiro, Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB110219/. 13 Nov. 2023.
https://floradobrasil.jbrj.gov.br/reflor...
). Furthermore, the portion along southern Bahia and northern Espírito Santo represents a center of endemism in the Atlantic Forest (Silva & Casteleti 2003Silva JMC, Casteleti CH. 2003. Estado da biodiversidade da Mata Atlântica brasileira. In: Galindo-Leal C, Gusmão-Câmara I (eds.). Mata Atlântica, Biodiversidade, Ameaças e Perspectivas. Belo Horizonte, Fundação SOS Mata Atlântica, Conservação Internacional. p. 43-59.; Thomas et al. 2003Thomas WW, Jardim JG, Fiaschi P, Amorim AM. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In: Prado PI, Landau EC, Moura RT, Pinto LPS, Fonseca GAB, Alger K (eds.). Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia. Ilhéus, IESB/CI/CABS/UFMG/UNICAMP. (CD-ROM.)) and one of the richest spots for tree species in the world (Martini et al. 2007Martini AMZ, Fiaschi P, Amorim AMA, Paixão JL. 2007. A Hot-Point Within A Hot-Spot: A High Diversity Site in Brazil’s Atlantic Forest. Biodiversity and Conservation 16: 3111-3128.; Ostroski et al. 2018Ostroski P, Saiter FZ, Amorim AM, Fiaschi P. 2018. Endemic Angiosperms in Bahia Coastal Forests, Brazil: An Update Using A Newly Delimited Area. Biota Neotropica 18: e20180544. doi: 10.1590/1676-0611-BN-2018-0544
https://doi.org/10.1590/1676-0611-BN-201...
). Despite intense forest suppression in the northern portion of Espírito Santo, this region contains the largest remnant of Tabuleiro forest in southeastern Brazil (Germano Filho et al. 2000Germano Filho P, Peixoto AL, Jesus RM. 2000. Espécies vegetais descritas a partir de espécimes coletados na Reserva Florestal de Linhares, Espírito Santo, Brasil. Boletim do Museu de Biologia Mello Leitão 11/12: 35-48.) and harbors high floristic diversity, especially among woody plants with ca. 930 species (Saiter et al. 2016Saiter FZ, Rolim SG, Oliveira Filho AT. 2016. A floresta de Linhares no contexto fitogeográfico do leste do Brasil. In: Rolim SG, Menezes LFT, Srbek-Araujo AC (eds.). Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale. Belo Horizonte, Rona Editora . p. 61-69.). A particular remnant in this region is the Reserva Natural Vale (RNV, “Vale Natural Reserve”), which records half of the Annonaceae species for Espírito Santo, including three species of Duguetia (Fig. 4, 5), D. chrysocarpaMaas (1999Maas PJM. 1999. Studies in Annonaceae XXXVII. Monograph of Duguetia: Preliminary Notes II. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 121: 465-489.: 471), D. sessilis (Vell.) Maas (1993Maas PJM, Westra LYTH, Meijdam NAJ, van Tol IAV. 1993. Studies in Annonaceae XV. A taxonomic revision of Duguetia A. F. C. P. de Saint-Hilaire Sect. Geanthemum (R. E. Fries) R. E. Fries (Annonaceae). Boletim do Museu Paraense Emilio Goeldi (Série Botânica) 9: 31-58.: 38) and D. sooretamaeMaas (1999Maas PJM. 1999. Studies in Annonaceae XXXVII. Monograph of Duguetia: Preliminary Notes II. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 121: 465-489.: 486) (Lobão et al. 2010Lobão AQ, Siqueira GS, Maas PJM, Neto LM. 2010. Reserva Natural da Vale, Linhares - Espírito Santo, Brasil. Annonaceae da Vale. Rapid Color Guide, 278, version 1. Environmental & Conservation Programs, The Field Museum, Chicago. https://fieldguides.fieldmuseum.org/pt-br/guias/guia/278
https://fieldguides.fieldmuseum.org/pt-b...
; Lopes & Mello-Silva 2014Lopes JC, Mello-Silva R. 2014. Annonaceae da Reserva Natural Vale, Linhares, Espírito Santo. Rodriguésia 65: 599-635. doi: 10.1590/2175-7860201465304
https://doi.org/10.1590/2175-78602014653...
). The RNV is an important center of angiosperm diversity in the Neotropics, with a high richness of endemic and threatened species (Rolim et al. 2016Rolim SG, Peixoto AL, Pereira OJ, et al. 2016. Angiospermas da Reserva Natural Vale, na floresta atlântica do norte do Espírito Santo. In: Rolim SG, Menezes LFT, Srbek-Araujo AC. (eds.). Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale. Belo Horizonte, Rona Editora . p. 167-230.). From there several novelties in different plant families have been newly reported (Lopes et al. 2013Lopes JC, Junikka L, Mello-Silva R. 2013. Oxandra unibracteata (Annonaceae), A New Species from the Atlantic Forest and A New Synonym of O. nitida. Phytotaxa 84: 25-30. doi: 10.11646/phytotaxa.84.1.2
https://doi.org/10.11646/phytotaxa.84.1....
; 2014Lopes JC, Mello-Silva R. 2014. Annonaceae da Reserva Natural Vale, Linhares, Espírito Santo. Rodriguésia 65: 599-635. doi: 10.1590/2175-7860201465304
https://doi.org/10.1590/2175-78602014653...
; Lewis et al. 2017Lewis G, Siqueira GS, Banks H, Bruneau A. 2017. The Majestic Canopy-Emergent Genus Dinizia (Leguminosae: Caesalpinioideae), Including A New Species Endemic to the Brazilian State of Espírito Santo. Kew Bulletin 72: 48. doi: 10.1007/s12225-017-9720-7
https://doi.org/10.1007/s12225-017-9720-...
; Rossetto & Ferraz 2020Rossetto EFS, Ferraz JR. 2020. Guapira siqueirae (Nyctaginaceae, Pisonieae), A New Species from Espírito Santo State, Brazil. Phytotaxa 460: 143-148. doi: 10.11646/phytotaxa.460.2.4
https://doi.org/10.11646/phytotaxa.460.2...
; Gaem et al. 2021Gaem PH, Fernandes T, Valdemarin KS, Lucas E, Mazine FF. 2021. Myrcia excelsa (Myrtaceae), A New Species from Espírito Santo, Brazil. Phytotaxa 501: 293-296. doi: 10.11646/phytotaxa.501.2.4
https://doi.org/10.11646/phytotaxa.501.2...
).

Recently revising the collections made after the last treatment of Annonaceae for the RNV (Lopes & Mello-Silva 2014Lopes JC, Mello-Silva R. 2014. Annonaceae da Reserva Natural Vale, Linhares, Espírito Santo. Rodriguésia 65: 599-635. doi: 10.1590/2175-7860201465304
https://doi.org/10.1590/2175-78602014653...
), we found an undescribed species of Duguetia, here described. We also provide illustrations and the preliminary conservation status of the new species, as well as comparisons with closely related species, a distribution map and an identification key to all Duguetia species in the state of Espírito Santo.

Material and methods

Morphological studies and distribution data were based on specimens deposited at CVRD, HASSI, RB, SPF and WAG (acronyms according to Thiers 2023Thiers B. 2023. Index Herbariorum: A global directory of public herbaria and associated staff. https://sweetgum.nybg.org/science/ih/. 12 Nov. 2023.
https://sweetgum.nybg.org/science/ih/...
, continually updated), digital images respectively available through REFLORA - Herbário Virtual (2023REFLORA. 2023. Herbário Virtual. https://reflora.jbrj.gov.br/reflora/herbarioVirtual. 05 Sept. 2023.
https://reflora.jbrj.gov.br/reflora/herb...
) and SpeciesLink (2023SpeciesLink. 2023. Sistema de informação distribuído para recuperação de dados de acervos de coleções biológicas e de observação em campo. https://splink.cria.org.br/. 15 Sept. 2023.
https://splink.cria.org.br/...
) platforms, and field observations by the authors. The barcode numbers of the examined specimens are cited within square brackets when presented. External structures were analyzed with a stereomicroscope LEICA EZ4. Bark morphology follows Junikka (1994Junikka L. 1994. Survey of English Macroscopic Bark Terminology. IAWA Journal 15: 3-45. doi: 10.1163/22941932-90001338
https://doi.org/10.1163/22941932-9000133...
). Hair types, density of the indument and the description of flowers and fruits follow Maas et al. (2003Maas PJM, Westra LYTH, Chatrou LW. 2003. Duguetia (Annonaceae). New York, New York Botanical Garden Press. Vol. LXXXVIII.). Plant height, phenology and colors of reproductive parts were derived from specimen labels and photographs of live plants. Vegetative parts were measured from dried specimens, rehydrated flowers and fleshy fruits preserved in spirit (Folli 7004, CVRD014298). General morphology follows the Systematics Association Committee for Descriptive Biological Terminology (1962Systematics Association Committee for Descriptive Biological Terminology. 1962. II. Terminology of simple symmetrical plain shapes (Chart 1). Taxon 11: 145-156. doi: 10.2307/1216718.
https://doi.org/10.2307/1216718....
) and Beentje (2010Beentje HJ. 2010. Plant Glossary. Surrey, Kew Publishing.). Preliminary conservation status follows IUCN Red List Categories and Criteria (2012IUCN. 2012. Red List Categories and Criteria. Version 3.1. 2nd. edn. Cambridge, IUCN. https://www.iucnredlist.org/resources/categories-and-criteria. 10 Sept. 2023.
https://www.iucnredlist.org/resources/ca...
; 2022IUCN. 2022. Guidelines for using the IUCN red list categories and criteria. Version 15.1 Prepared by the Standards and Petitions Subcommittee. https://www.iucnredlist.org/resources/redlistguidelines. 10 Sept. 2023.
https://www.iucnredlist.org/resources/re...
). The distribution map was prepared using ArcGIS Desktop v.10.8 (ESRI 2020ESRI. 2020. ArcGIS Desktop Help 10.8 Geostatistical Analyst. https://desktop.arcgis.com/en/. 10 Sept. 2023.
https://desktop.arcgis.com/en/...
) and based on geospatial data present on specimen labels.

Results

Taxonomic treatment

Duguetia rolimii M.L.Bazante, G.S.Siqueira & Maas, sp. nov. (Figs. 1, 2, 3A-E, 4; Table 1)

Type: BRAZIL. Espírito Santo: Linhares, Reserva Natural Vale, 70 m, 2 January 2013 (fr), D.A. Folli 7004 (Holotype: CVRD [CVRD014298]; Isotypes: HASSI, SPF [SPF00228241], WAG [WAG1973530]).

Duguetia rolimii is most similar to D. sooretamae, but D. sooretamae has leaves totally to densely covered with stellate scales 0.3-0.5 mm in diam. below, secondary veins at an angle more than 70° with the primary vein and indistinct at the lower side of the leaves, cauliflory present, upper bract ca. 1 mm long, flower buds broadly to very broadly ovoid with three slightly to absent ridges and an obtuse and not apiculate apex, petals broadly ovate with more than 12 mm wide, stamens 3-4 mm long with apex of connective not umbonate, fruit with fertile monocarps ovoid and with areoles narrowly pyramidal, totally covered with persistent stellate scales, whereas D. rolimii has leaves rather densely to sparsely covered with stellate scales 0.1-0.2 mm in diam. below, secondary veins at an angle up to 65° with the primary vein and distinct at the lower side of the leaves, cauliflory absent, upper bract 6-8 mm long, flower buds triangular-ovoid with three prominent ridges and an acute and apiculate apex, petals narrowly panduriform-elliptic to narrowly elliptic up to 12 mm wide, stamens up to 1.5 mm long with apex of connective umbonate, fruit with fertile monocarps obtrulloid to oblongoid and with areoles shallowly ovoid-pyramidal, glabrous or sparsely covered with stellate hairs towards the apicule (Fig. 3).

Figure 1.
Duguetia rolimii. A. Branch with flower buds. B. Leaf, lower side. C. Detail of the indument on the lower side of leaf. D. Flower bud, side view. E. Flower at anthesis, side view with one inner petal removed. F. Longitudinal section of androecium and gynoecium. G. Sepal, inner view. H. Outer petal, inner view. I. Inner petal, inner view. J. Stamen, outer view. K. Carpel, side view. L. Fruit, side view. M. Fertile monocarp, side view. N. Seed, side view. A-D from Folli 7567 b [CVRD15760]; E-K from Siqueira 1198 [CVRD15811]; L-N from Folli 7004 [CVRD014298, holotype]. Illustration by Klei Sousa.

Figure 2.
Duguetia rolimii. A. Tree canopy. B. Trunk, note the fissures and ridges of the outer bark. C. Leaves, lower and upper side view. D. Flower at anthesis, top view. E. Flowers after the petals fall. F. Fruit. Photos: A-C by Márcio L. Bazante; D-F by Geovane S. Siqueira.

Figure 3.
Comparison between Duguetia rolimii (A-F) and D. sooretamae (G-L). A. Leaf, upper side. B. Leaf, lower side. C. Detail of the indument on the lower side of the leaf. D. Flower bud. E. Fruit. F. Fertile monocarp. G. Leaf, upper side. H. Leaf, lower side. I. Detail of the indument on the lower side of the leaf. J. Flower bud. K. Fruit. L. Fertile monocarp. A-D from Siqueira 1172 [CVRD15753]; E-F from Folli 7004 [CVRD014298, holotype]; G-I from Maas et al. 8827 [CVRD006115]; J-L from Tressmann et al. 60 [SAMES08092].

Figure 4.
Distribution of Duguetia species in the state of Espírito Santo, Brazil.

Table 1.
Main characters distinguishing Duguetia rolimii and D. sooretamae.

Figure 5.
Species of Duguetia previously recorded in the Reserva Natural Vale, Espírito Santo, Brazil. A-C. Duguetia chrysocarpa. A. Leaf, lower side. B. Flower bud. C. Fruits. D-F. Duguetia sessilis. D. Leaf, upper side. E. Inflorescence flagelliflorous. F. Flower. G-I. Duguetia sooretamae. G. Inflorescence cauliflorous. H. Flower. I. Fruit. Photos: A, B, D, E by Diogo B. Kanouté; C, F, G-I by Geovane S. Siqueira.

Tree, 20-22 m tall, 120-130 cm in diam.; outer bark hard, rough, pale greenish brown; fissures parallel, deep, elongated; ridges rounded or V-shaped. Young twigs, leaf buds and petioles totally to densely covered with yellowish stellate scales 0.1-0.2 mm in diam. Petioles shallowly canaliculate, 2.5-5 mm long, 1-2 mm in diam. Leaves narrowly elliptic, 6-17 cm long, 1.5-5 cm wide, leaf index 2.2-4.6, coriaceous to chartaceous, smooth, dark green in vivo to yellowish brown in sicco above, paler green in vivo to yellowish brown in sicco below, distinctly shiny and glabrous above, slightly shiny and rather densely to sparsely covered with yellowish stellate scales 0.1-0.2 mm in diam. below, base acute, apex long-acute, margin slightly undulate; primary vein slightly impressed to flat above, secondary veins curved, 9-20 on either side of primary vein, raised and distinct on both sides, but strongly so below, angles with primary vein 55-65°, loops distinct, smallest distance between loops and margin 1-8 mm, tertiary veins reticulate, slightly raised and distinct on both sides. Inflorescences among leaves, axillary, leaf-opposed or terminal, sometimes terminal on short axillary shoots, a single rhipidium; rhipidia 1-2-flowered; indument: peduncles, pedicels, outer side of bracts and sepals totally covered with brownish yellow stellate scales 0.1-0.2 mm in diam., inner side of bracts and sepals and both sides of petals totally covered with pale yellow, furcate and stellate hairs to 1 mm long, almost glabrous towards the base. Peduncle 1-4 mm long, ca. 2 mm in diam. Pedicels 6-18 mm long, 2-3 mm in diam., fruiting pedicels to 25 mm long, 5-8 mm in diam. Upper bract at the basal third to just below the middle of the pedicel, ovate to broadly so, 6-8 mm long, 5-7 mm wide, recurved, soon falling off. Flower buds triangular-ovoid, 10-14 mm long, 8-10 mm in diam., apex acute, apiculate (apicule curved, 1-2 mm long), prominently 3-ridged by recurved edges of the sepals. Flowers pale green to yellowish in vivo. Sepals 10-15% connate at the base, 14-20 mm long, 9-15 mm wide, triangular-ovate, apex acute to acuminate (acumen ca. 2 mm long), soon falling off. Petals subequal, narrowly panduriform-elliptic to narrowly elliptic, 33-45 mm long, 9-12 mm wide, apex acuminate, inner base of inner petals concave, callose, distinctly grooved. Stamens numerous, 0.8-1.5 mm long, yellowish brown, apex of connective depressed ovoid, umbonate, ca. 0.4 mm long, 0.7-0.8 mm wide, papillate. Carpels numerous, 2-2.5 mm long, base of ovary glabrous, rest of ovary densely to totally covered with furcate and stellate hairs up to 0.3 mm long, stigma sparsely so to glabrous. Immature fruit pale green in vivo, globose to broadly ellipsoid, 3-10 cm long, 3-7 cm in diam., basal collar composed of 16-20 connate, sterile monocarps, 10-15 in diam., not protruding below the fruit, fertile monocarps > 200, obtrulloid to oblongoid, free, 8.5-20 mm long, 5.5-11 mm in diam., areoles shallowly ovoid-pyramidal, 3-5 mm high, obtuse, abruptly apiculate (apicule curved, 1-2 mm high), sharp-pointed, slightly verrucose, 4-7-ribbed, glabrous except for a few yellowish stellate hairs towards the apicule. Seeds obovoid to ellipsoid, 10-16 mm long, 6-9 mm in diam., apex acute to obtuse, slightly apiculate (apicule ≤ 1 mm long), brownish, shiny.

Distribution and habitat: Duguetia rolimii is known only from the type locality, the Reserva Natural Vale (RNV), a protected area in the municipality of Linhares, northern part of Espírito Santo, Brazil. Two adult individuals were found in this forest remnant, at an elevation less than 100 m (50 to 70 m, Fig. 4), known as Tabuleiro forest (Rizzini 1997Rizzini CT. 1997. Tratado de fitogeografia do Brasil: aspectos ecológicos, sociológicos e florísticos. 2nd. edn. Rio de Janeiro, Âmbito Cultural Edições.) or Lowland Tropical Ombrophilous Forest (IBGE 2012IBGE - Instituto Brasileiro de Geografia e Estatística. 2012. Manual Técnico da Vegetação Brasileira. 2nd. edn. Rio de Janeiro, IBGE. ). It is found in mata alta (“tall forest”) formation, a vegetation type that comprises about 70% of the RNV (Jesus 1987Jesus RM. 1987. Mata atlântica de Linhares: aspectos florestais. In: Anais do Seminário Desenvolvimento econômico e impacto ambiental em áreas do trópico úmido brasileiro - a experiência da CVRD. Rio de Janeiro, Companhia Vale do Rio Doce. p. 35-71.; Peixoto et al. 2008Peixoto AL, Silva IM, Pereira OJ, Simonelli M, Jesus RM, Rolim SG. 2008. Tabuleiro Forests North of the Rio Doce: their representation in the Vale do Rio Doce Natural Reserve, Espírito Santo, Brazil. In: Thomas WW (ed.). The Atlantic Coastal Forest of Northeastern Brazil. New York, Memoirs of The New York Botanical Garden. p. 313-344.). The mata alta has large trees up to 40 m tall, a dense canopy that shades the understory, clay or sandy-clay soils, and is dominated by species of Fabaceae and Myrtaceae (Peixoto et al. 2008Peixoto AL, Silva IM, Pereira OJ, Simonelli M, Jesus RM, Rolim SG. 2008. Tabuleiro Forests North of the Rio Doce: their representation in the Vale do Rio Doce Natural Reserve, Espírito Santo, Brazil. In: Thomas WW (ed.). The Atlantic Coastal Forest of Northeastern Brazil. New York, Memoirs of The New York Botanical Garden. p. 313-344.; Rolim et al. 2016Rolim SG, Peixoto AL, Pereira OJ, et al. 2016. Angiospermas da Reserva Natural Vale, na floresta atlântica do norte do Espírito Santo. In: Rolim SG, Menezes LFT, Srbek-Araujo AC. (eds.). Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale. Belo Horizonte, Rona Editora . p. 167-230.). Among the vegetation types of the RNV, mata alta presents the greatest diversity of species and is where most of the new species recently described come from (Rolim et al. 2016Rolim SG, Peixoto AL, Pereira OJ, et al. 2016. Angiospermas da Reserva Natural Vale, na floresta atlântica do norte do Espírito Santo. In: Rolim SG, Menezes LFT, Srbek-Araujo AC. (eds.). Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale. Belo Horizonte, Rona Editora . p. 167-230.).

Phenology: Specimens with flower buds were gathered in August, with flowers in November, and with fruits in January.

Vernacular name in the RNV: Ariticum-gigante.

Etymology: The specific epithet honors the Brazilian researcher Dr. Samir G. Rolim, in recognition of his significant contributions to the biological knowledge of the Atlantic Forest, particularly of the Reserva Natural Vale. In 2016, Rolim and collaborators coordinated the remarkable book “Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale”, which highlights the biodiversity and relevant research conducted in this protected area.

Preliminary IUCN conservation assessment: Although Duguetia rolimii was collected in a relatively well-known protected area (Reserva Natural Vale), where field expeditions have taken place since the 1950s (Peixoto & Jesus 2016Peixoto AL, Jesus RM. 2016. Reserva Natural Vale: memórias de 65 anos de conservação. In: Rolim SG, Menezes LFT, Srbek-Araujo AC (eds.). Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale. Belo Horizonte, Rona Editora. p. 21-29.), only two individuals were identified in the field, probably due to the difficulty in recognizing and collecting its large trees, up to 22 m tall. Owing to insufficient information on abundance and distribution for a reliable conservation assessment, we suggest that D. rolimii be considered Data Deficient (DD) according to IUCN criteria (IUCN 2012, 2022). The available evidence indicates that the area surrounding its known occurrence is destroyed by cattle farming, pasture, eucalyptus forestry and the cultivation of coffee, papaya and cacao, or remains in very small and isolated fragments, suggesting the continued decline of its habitat (Rolim et al. 2005Rolim SG, Jesus RM, Nascimento HEM, Couto HTZ, Chambers JQ. 2005. Biomass Change in an Atlantic Tropical Moist Forest: The ENSO Effect in Permanent Sample Plots Over 22-year Period. Oecologia 142: 238-246. doi: 10.1007/s00442-004-1717-x
https://doi.org/10.1007/s00442-004-1717-...
; Saiter et al. 2016Saiter FZ, Rolim SG, Oliveira Filho AT. 2016. A floresta de Linhares no contexto fitogeográfico do leste do Brasil. In: Rolim SG, Menezes LFT, Srbek-Araujo AC (eds.). Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale. Belo Horizonte, Rona Editora . p. 61-69.).

Additional specimens examined (Paratypes) - BRAZIL. Espírito Santo: Linhares, Reserva Natural Vale, Estrada Oiticica, 18 January 2018 (fr), G.S. Siqueira 1252 (CVRD [CVRD15869], HASSI); Estrada Louro, 28 November 2014 (fl), G.S. Siqueira 1039 (CVRD [CVRD15184], WAG [WAG1973537, WAG1973538]); ibidem, 7 August 2017 (fl), G.S. Siqueira 1172 (CVRD [CVRD15753], HASSI); ibidem, 7 August 2017 (fl), D.A. Folli 7567 b (CVRD [CVRD15760], HASSI); ibidem, 21 November 2017 (fl), D.A. Folli 7596 (CVRD [CVRD15809], HASSI, RB [RB01378923]); ibidem, 21 November 2017 (fl), G.S. Siqueira 1198 (CVRD [CVRD15811], HASSI, RB [RB01378928]).

Discussion

Duguetia rolimii, one of the largest trees in the genus Duguetia, is characterized by leaves that are rather densely to sparsely covered with stellate scales below, secondary veins at an angle of less than 70° with the primary vein, conspicuous on both leaf sides, large upper flower bract, triangular-ovoid flower buds with a curved apicule and three prominent ridges, stamens with an umbonate connective at the apex, fruit with more than 200 fertile monocarps and with areoles shallowly ovoid-pyramidal, glabrous or soon becoming glabrous (Figs. 1, 2, 3A-E).

The type collection of Duguetia rolimii was misidentified as D. sooretamae Maas or only identified to the genus level. Justifiably, D. rolimii and D. sooretamae are more closely allied morphologically because of similar trichomes, shape, size and shine of the leaves and their fruits with more than 200 fertile monocarps. Moreover, both species occur in the RNV and are restricted to Espírito Santo (Fig. 4) (Maas et al. 2003Maas PJM, Westra LYTH, Chatrou LW. 2003. Duguetia (Annonaceae). New York, New York Botanical Garden Press. Vol. LXXXVIII.; Lopes & Mello-Silva 2014Lopes JC, Chatrou LW, Mello-Silva R. 2014. Ephedranthus dimerus (Annonaceae), A New Species from the Atlantic Forest of Brazil and A Key to the Species of Ephedranthus. Brittonia 66: 70-74. doi: 10.1007/s12228-013-9311-3
https://doi.org/10.1007/s12228-013-9311-...
; Lobão & Bazante 2023Lobão AQ, Bazante ML. 2023. Duguetia. In: Flora e Funga do Brasil. Rio de Janeiro, Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/FB110296/. 13 Nov. 2023.
https://floradobrasil.jbrj.gov.br/FB1102...
). However, the height of the plants, outer bark pattern and diameter, angle and distinction of secondary veins and density of stellate scales at the lower side of the leaves, cauliflory, length of upper bract, shape of flower buds, width of petals, length of stamens, shape of apex of connective, shape of fertile monocarps and other features allow the distinction of these taxa (Fig. 3, 5G-I; Table 1). In addition to that, D. rolimii and D. sooretamae prefer different vegetation types within the RNV. The latter grows in the muçununga forest, whereas D. rolimii flourishes in the mata alta. The muçununga forest, which comprises about 8% of the RNV and forms enclaves within the mata alta, is a vegetation with lower trees up to 10 m tall, a more open canopy that allows sunlight to reach ground level, sandy soils and a greater abundance of xerophytic species, lianas and bromeliads (Garay 2003Garay I. 2003. Uma história recente. In: Garay I, Rizzini CM (eds.). A Floresta Atlântica de Tabuleiros: diversidade funcional da cobertura arbórea. Petrópolis, Vozes. p. 3-7.; Simonelli et al. 2008Simonelli M, Souza AL, Peixoto AL, Silva AF. 2008. Floristic composition and structure of the tree component of a Muçununga Forest in the Linhares Forest Reserve, Espírito Santo, Brazil. In: Thomas WW (ed.). The Atlantic Coastal Forest of Northeastern Brazil. New York, Memoirs of The New York Botanical Garden . p. 345-364.).

The other two Duguetia species recorded in the RNV, D. chrysocarpa Maas and D. sessilis (Vell.) Maas (Lopes & Mello-Silva 2014Lopes JC, Mello-Silva R. 2014. Annonaceae da Reserva Natural Vale, Linhares, Espírito Santo. Rodriguésia 65: 599-635. doi: 10.1590/2175-7860201465304
https://doi.org/10.1590/2175-78602014653...
), grow in the mata alta and flooded forests (Fig. 4, 5). These species have heights up to 10 m tall and fruits with around 50 fertile monocarps, totally to densely covered with persistent stellate hairs on the areoles, whereas D. rolimii has heights up to 22 m tall and fruits with more than 200 fertile monocarps, glabrous or with few stellate hairs at the apex of the areoles. Duguetia. chrysocarpa also occurs in the states of Bahia and Minas Gerais, and D. sessilis in the state of Rio de Janeiro (Maas et al. 2003Maas PJM, Westra LYTH, Chatrou LW. 2003. Duguetia (Annonaceae). New York, New York Botanical Garden Press. Vol. LXXXVIII.; Lobão & Bazante 2023Lobão AQ, Bazante ML. 2023. Duguetia. In: Flora e Funga do Brasil. Rio de Janeiro, Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/FB110296/. 13 Nov. 2023.
https://floradobrasil.jbrj.gov.br/FB1102...
).

Considering other Atlantic Forest species, D. rolimii resembles D. gardneriana Mart. (1841Martius CFP von. 1841. Annonaceae. In: Martius CFP von, Eichler AG, Urban I. (eds.). Flora Brasiliensis. Vol. XIII. https://florabrasiliensis.cria.org.br/search?taxon_id=523. 13 Nov. 2023.
https://florabrasiliensis.cria.org.br/se...
: 22) and D. reticulataMaas (1996Maas PJM. 1996. Studies in Annonaceae XXX. Monograph of Duguetia: Preliminary Notes. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 118: 187-227.: 212) because of its leaves sparsely covered with stellate scales below and fruits with more than 200 fertile monocarps (Maas et al. 2003Maas PJM, Westra LYTH, Chatrou LW. 2003. Duguetia (Annonaceae). New York, New York Botanical Garden Press. Vol. LXXXVIII.; Lobão & Bazante 2023Lobão AQ, Bazante ML. 2023. Duguetia. In: Flora e Funga do Brasil. Rio de Janeiro, Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/FB110296/. 13 Nov. 2023.
https://floradobrasil.jbrj.gov.br/FB1102...
). Nevertheless, D. gardneriana has flower buds very broadly ovoid, obtuse, not apiculate, not 3-ridged and petals ovate to very broadly ovate, while the new species has flower buds triangular-ovoid, acute, apiculate, prominently 3-ridged and petals narrowly panduriform-elliptic to narrowly elliptic. Duguetia reticulata has leaves 5-8 cm wide, upper bract ca. 1 mm long and flowers pinkish in vivo, while D. rolimii has leaves 1.5-5 cm wide, upper bract 6-8 mm long and flowers pale green to yellowish in vivo. Duguetia gardneriana occurs in northeastern Brazil, from Rio Grande do Norte to Bahia, and D. reticulata is restricted to Bahia (Maas et al. 2003Maas PJM, Westra LYTH, Chatrou LW. 2003. Duguetia (Annonaceae). New York, New York Botanical Garden Press. Vol. LXXXVIII., Lobão & Bazante 2023Lobão AQ, Bazante ML. 2023. Duguetia. In: Flora e Funga do Brasil. Rio de Janeiro, Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/FB110296/. 13 Nov. 2023.
https://floradobrasil.jbrj.gov.br/FB1102...
).

Key to identify the Duguetia species present in the Espírito Santo

1. Young twigs, petioles, lower side of leaves, pedicels, bracts and sepals covered with stellate hairs (Mata alta and flooded forests, Figs. 4, 5A-C) ………….… D. chrysocarpa

1’. Young twigs, petioles, lower side of leaves, pedicels, bracts and sepals covered with entire scales and/or stellate scales ….…………………………………………………… 2

2. Upper side of leaves sparsely to densely covered with stellate hairs and stellate scales; fertile monocarps connate for 70-80% of their length (Flooded forests, Fig. 4) ………… …………………………………………………………………………… D. furfuracea

2’. Upper side of leaves glabrous; fertile monocarps free ……………………………… 3

3. Inflorescences flagelliflorous, i.e., inflorescence 8-14.5 cm long arising at the base of the main trunk; fruit ≤ 2 cm in diam., fertile monocarps ca. 8 (Mata alta, Figs. 4, 5D-F) …………………………………………………………………………………. D. sessilis

3’. Inflorescences among leaves or cauliflorous, rarely flagelliflorous; fruit ≥ 3 cm in diam., fertile monocarps ≥ 60 ………………………………………………………… 4

4. Tree to 22 m tall; upper bract 6-8 mm long; flower buds prominently 3-ridged by recurved edges of the sepals, apex apiculate; fruiting areoles glabrous or soon becoming glabrous (Mata alta, Figs. 1, 2, 3A-F, 4) ……………………………………… D. rolimii

4’. Shrub or tree to 6 m tall; upper bract 1-2 mm long; flower buds slightly 3-ridged by recurved edges of the sepals to not 3-ridged, apex not apiculate; fruiting areoles totally covered with persistent indument ……………………………………………………… 5

5. Lower side of leaves sparsely covered with stellate scales; fertile monocarps ca. 90, areoles broadly pyramidal, totally covered with brownish indument of stellate to furcate hairs (Mata alta, Fig. 4) …………………………………………………… D. riedeliana

5’. Lower side of leaves totally to densely covered with stellate scales; fertile monocarps > 200, areoles narrowly pyramidal, totally covered with greyish indument of stellate scales (Muçununga forest, Figs. 3G-L, 4, 5G-I) ………………………… D. sooretamae

Acknowledgements

We thank the Reserva Natural Vale for providing support during the research; Renato A. Magri for supplying images of the isotype from the SPF; Mariana C. dos Santos Senna for preparing the distribution map; and Klei Sousa for the illustration. The first author thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a Doctoral scholarship (process 141056/2021-5), and the International Association for Plant Taxonomy ‘IAPT Research Grant 2023’. MRVB also thanks CNPq and Propesq/UFPB for research grants (PVA13403-2020).

References

  • Antonelli A, Sanmartín I. 2011. Why Are There So Many Plant Species in the Neotropics? Taxon 60: 403-414. doi: 10.1002/tax.602010
    » https://doi.org/10.1002/tax.602010
  • Bazante ML, Alves M. 2017. A New Species of Duguetia (Annonaceae) From the Atlantic Forest of Northeastern Brazil. Phytotaxa 314: 266-272. doi: 10.11646/phytotaxa.314.2.8
    » https://doi.org/10.11646/phytotaxa.314.2.8
  • Bazante ML, Maas PJM, Barbosa MRV. 2023. Duguetia leucotricha (Annonaceae), A New Species From the Atlantic Coastal Forest of Brazil. Acta Botanica Brasilica 37: e20220203. doi: 10.1590/1677-941X-ABB-2022-0203
    » https://doi.org/10.1590/1677-941X-ABB-2022-0203
  • Beentje HJ. 2010. Plant Glossary. Surrey, Kew Publishing.
  • Chatrou LW, Pirie MD, Erkens RHJ et al 2012. A New Subfamilial and Tribal Classification of the Pantropical Flowering Plant Family Annonaceae Informed by Molecular Phylogenetics. Botanical Journal of the Linnean Society 169: 5-40. doi: 10.1111/j.1095-8339.2012.01235.x
    » https://doi.org/10.1111/j.1095-8339.2012.01235.x
  • Chatrou LW, Turner IM, Klitgaard BB, Maas PJ, Utteridge TMA. 2018. A Linear Sequence to Facilitate Curation of Herbarium Specimens of Annonaceae. Kew bulletin 73: 1-10. doi: 10.1007/s12225-018-9764-3
    » https://doi.org/10.1007/s12225-018-9764-3
  • ESRI. 2020. ArcGIS Desktop Help 10.8 Geostatistical Analyst. https://desktop.arcgis.com/en/ 10 Sept. 2023.
    » https://desktop.arcgis.com/en/
  • Flora e Funga do Brasil. 2023. Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/ 18 Nov. 2023.
    » https://floradobrasil.jbrj.gov.br/
  • Fundação SOS Mata Atlântica, INPE. 2023. Atlas dos remanescentes florestais da Mata Atlântica: período 2021-2022, relatório técnico. São Paulo, Fundação S.O.S Mata Atlântica, Instituto Nacional de Pesquisas Espaciais. https://cms.sosma.org.br/wp-content/uploads/2023/05/SOSMAAtlas-da-Mata-Atlantica_2021-2022-1.pdf 18 Nov. 2022.
    » https://cms.sosma.org.br/wp-content/uploads/2023/05/SOSMAAtlas-da-Mata-Atlantica_2021-2022-1.pdf
  • Gaem PH, Fernandes T, Valdemarin KS, Lucas E, Mazine FF. 2021. Myrcia excelsa (Myrtaceae), A New Species from Espírito Santo, Brazil. Phytotaxa 501: 293-296. doi: 10.11646/phytotaxa.501.2.4
    » https://doi.org/10.11646/phytotaxa.501.2.4
  • Garay I. 2003. Uma história recente. In: Garay I, Rizzini CM (eds.). A Floresta Atlântica de Tabuleiros: diversidade funcional da cobertura arbórea. Petrópolis, Vozes. p. 3-7.
  • Germano Filho P, Peixoto AL, Jesus RM. 2000. Espécies vegetais descritas a partir de espécimes coletados na Reserva Florestal de Linhares, Espírito Santo, Brasil. Boletim do Museu de Biologia Mello Leitão 11/12: 35-48.
  • Guo X, Tang CC, Thomas DC, Couvreur TLP, Saunders RMK. 2017. A Mega-Phylogeny of the Annonaceae: Taxonomic Placement of Five Enigmatic Genera and Recognition of A New Tribe, Phoenicantheae. Scientific Reports 7: 7323. doi: 10.1038/s41598-017-07252-2
    » https://doi.org/10.1038/s41598-017-07252-2
  • IBGE - Instituto Brasileiro de Geografia e Estatística. 2012. Manual Técnico da Vegetação Brasileira. 2nd. edn. Rio de Janeiro, IBGE.
  • IUCN. 2012. Red List Categories and Criteria. Version 3.1. 2nd. edn. Cambridge, IUCN. https://www.iucnredlist.org/resources/categories-and-criteria 10 Sept. 2023.
    » https://www.iucnredlist.org/resources/categories-and-criteria
  • IUCN. 2022. Guidelines for using the IUCN red list categories and criteria. Version 15.1 Prepared by the Standards and Petitions Subcommittee. https://www.iucnredlist.org/resources/redlistguidelines 10 Sept. 2023.
    » https://www.iucnredlist.org/resources/redlistguidelines
  • Jesus RM. 1987. Mata atlântica de Linhares: aspectos florestais. In: Anais do Seminário Desenvolvimento econômico e impacto ambiental em áreas do trópico úmido brasileiro - a experiência da CVRD. Rio de Janeiro, Companhia Vale do Rio Doce. p. 35-71.
  • Junikka L. 1994. Survey of English Macroscopic Bark Terminology. IAWA Journal 15: 3-45. doi: 10.1163/22941932-90001338
    » https://doi.org/10.1163/22941932-90001338
  • Lewis G, Siqueira GS, Banks H, Bruneau A. 2017. The Majestic Canopy-Emergent Genus Dinizia (Leguminosae: Caesalpinioideae), Including A New Species Endemic to the Brazilian State of Espírito Santo. Kew Bulletin 72: 48. doi: 10.1007/s12225-017-9720-7
    » https://doi.org/10.1007/s12225-017-9720-7
  • Lobão AQ, Bazante ML. 2023. Duguetia In: Flora e Funga do Brasil. Rio de Janeiro, Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/FB110296/ 13 Nov. 2023.
    » https://floradobrasil.jbrj.gov.br/FB110296/
  • Lobão AQ, Lopes JC, Erkens RHJ, et al 2020. Annonaceae. In: Flora e Funga do Brasil. Rio de Janeiro, Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB110219/ 13 Nov. 2023.
    » https://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB110219/
  • Lobão AQ, Siqueira GS, Maas PJM, Neto LM. 2010. Reserva Natural da Vale, Linhares - Espírito Santo, Brasil. Annonaceae da Vale. Rapid Color Guide, 278, version 1. Environmental & Conservation Programs, The Field Museum, Chicago. https://fieldguides.fieldmuseum.org/pt-br/guias/guia/278
    » https://fieldguides.fieldmuseum.org/pt-br/guias/guia/278
  • Lopes JC, Chatrou LW, Mello-Silva R. 2014. Ephedranthus dimerus (Annonaceae), A New Species from the Atlantic Forest of Brazil and A Key to the Species of Ephedranthus Brittonia 66: 70-74. doi: 10.1007/s12228-013-9311-3
    » https://doi.org/10.1007/s12228-013-9311-3
  • Lopes JC, Junikka L, Mello-Silva R. 2013. Oxandra unibracteata (Annonaceae), A New Species from the Atlantic Forest and A New Synonym of O. nitida Phytotaxa 84: 25-30. doi: 10.11646/phytotaxa.84.1.2
    » https://doi.org/10.11646/phytotaxa.84.1.2
  • Lopes JC, Mello-Silva R. 2014. Annonaceae da Reserva Natural Vale, Linhares, Espírito Santo. Rodriguésia 65: 599-635. doi: 10.1590/2175-7860201465304
    » https://doi.org/10.1590/2175-7860201465304
  • Maas PJM, Westra LYT. 2010. New Species of Annonaceae from the Neotropics and Miscellaneous Notes. Blumea 55: 259-275.
  • Maas PJM, Westra LYTH, Chatrou LW. 2003. Duguetia (Annonaceae) New York, New York Botanical Garden Press. Vol. LXXXVIII.
  • Maas PJM, Westra LYTH, Meijdam NAJ, van Tol IAV. 1993. Studies in Annonaceae XV. A taxonomic revision of Duguetia A. F. C. P. de Saint-Hilaire Sect. Geanthemum (R. E. Fries) R. E. Fries (Annonaceae). Boletim do Museu Paraense Emilio Goeldi (Série Botânica) 9: 31-58.
  • Maas PJM. 1996. Studies in Annonaceae XXX. Monograph of Duguetia: Preliminary Notes. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 118: 187-227.
  • Maas PJM. 1999. Studies in Annonaceae XXXVII. Monograph of Duguetia: Preliminary Notes II. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 121: 465-489.
  • Martini AMZ, Fiaschi P, Amorim AMA, Paixão JL. 2007. A Hot-Point Within A Hot-Spot: A High Diversity Site in Brazil’s Atlantic Forest. Biodiversity and Conservation 16: 3111-3128.
  • Martius CFP von. 1841. Annonaceae. In: Martius CFP von, Eichler AG, Urban I. (eds.). Flora Brasiliensis. Vol. XIII. https://florabrasiliensis.cria.org.br/search?taxon_id=523 13 Nov. 2023.
    » https://florabrasiliensis.cria.org.br/search?taxon_id=523
  • Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J. 2000. Biodiversity Hotspot for Conservation Priorities. Nature 403: 853-858. doi: 10.1038/35002501
    » https://doi.org/10.1038/35002501
  • Ostroski P, Saiter FZ, Amorim AM, Fiaschi P. 2018. Endemic Angiosperms in Bahia Coastal Forests, Brazil: An Update Using A Newly Delimited Area. Biota Neotropica 18: e20180544. doi: 10.1590/1676-0611-BN-2018-0544
    » https://doi.org/10.1590/1676-0611-BN-2018-0544
  • Peixoto AL, Jesus RM. 2016. Reserva Natural Vale: memórias de 65 anos de conservação. In: Rolim SG, Menezes LFT, Srbek-Araujo AC (eds.). Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale. Belo Horizonte, Rona Editora. p. 21-29.
  • Peixoto AL, Silva IM, Pereira OJ, Simonelli M, Jesus RM, Rolim SG. 2008. Tabuleiro Forests North of the Rio Doce: their representation in the Vale do Rio Doce Natural Reserve, Espírito Santo, Brazil. In: Thomas WW (ed.). The Atlantic Coastal Forest of Northeastern Brazil. New York, Memoirs of The New York Botanical Garden. p. 313-344.
  • REFLORA. 2023. Herbário Virtual. https://reflora.jbrj.gov.br/reflora/herbarioVirtual 05 Sept. 2023.
    » https://reflora.jbrj.gov.br/reflora/herbarioVirtual
  • Ribeiro MC, Metzger JP, Martensen AC, Ponzoni F, Hirota MM. 2009. Brazilian Atlantic Forest: How Much Is Left and How Is the Remaining Forest Distributed? Implications for Conservation. Biological Conservation 142: 1141-1153. doi: 10.1016/j.biocon.2009.02.021
    » https://doi.org/10.1016/j.biocon.2009.02.021
  • Rizzini CT. 1997. Tratado de fitogeografia do Brasil: aspectos ecológicos, sociológicos e florísticos. 2nd. edn. Rio de Janeiro, Âmbito Cultural Edições.
  • Rolim SG, Jesus RM, Nascimento HEM, Couto HTZ, Chambers JQ. 2005. Biomass Change in an Atlantic Tropical Moist Forest: The ENSO Effect in Permanent Sample Plots Over 22-year Period. Oecologia 142: 238-246. doi: 10.1007/s00442-004-1717-x
    » https://doi.org/10.1007/s00442-004-1717-x
  • Rolim SG, Peixoto AL, Pereira OJ, et al 2016. Angiospermas da Reserva Natural Vale, na floresta atlântica do norte do Espírito Santo. In: Rolim SG, Menezes LFT, Srbek-Araujo AC. (eds.). Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale. Belo Horizonte, Rona Editora . p. 167-230.
  • Rossetto EFS, Ferraz JR. 2020. Guapira siqueirae (Nyctaginaceae, Pisonieae), A New Species from Espírito Santo State, Brazil. Phytotaxa 460: 143-148. doi: 10.11646/phytotaxa.460.2.4
    » https://doi.org/10.11646/phytotaxa.460.2.4
  • Safford WE. 1914. Classification of the genus Annona with Descriptions of New and Imperfectly Known Species. Contributions from the United States National Herbarium 18: 1-68.
  • Saiter FZ, Rolim SG, Oliveira Filho AT. 2016. A floresta de Linhares no contexto fitogeográfico do leste do Brasil. In: Rolim SG, Menezes LFT, Srbek-Araujo AC (eds.). Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale. Belo Horizonte, Rona Editora . p. 61-69.
  • Silva JMC, Casteleti CH. 2003. Estado da biodiversidade da Mata Atlântica brasileira. In: Galindo-Leal C, Gusmão-Câmara I (eds.). Mata Atlântica, Biodiversidade, Ameaças e Perspectivas. Belo Horizonte, Fundação SOS Mata Atlântica, Conservação Internacional. p. 43-59.
  • Simonelli M, Souza AL, Peixoto AL, Silva AF. 2008. Floristic composition and structure of the tree component of a Muçununga Forest in the Linhares Forest Reserve, Espírito Santo, Brazil. In: Thomas WW (ed.). The Atlantic Coastal Forest of Northeastern Brazil. New York, Memoirs of The New York Botanical Garden . p. 345-364.
  • Sobral-Souza T, Lima-Ribeiro MS. 2017. De volta ao passado: revisitando a história biogeográfica das florestas neotropicais úmidas. Oecologia Australis 21: 93-107. doi: 10.4257/oeco.2017.2102.01.
    » https://doi.org/10.4257/oeco.2017.2102.01.
  • SpeciesLink. 2023. Sistema de informação distribuído para recuperação de dados de acervos de coleções biológicas e de observação em campo. https://splink.cria.org.br/ 15 Sept. 2023.
    » https://splink.cria.org.br/
  • Systematics Association Committee for Descriptive Biological Terminology. 1962. II. Terminology of simple symmetrical plain shapes (Chart 1). Taxon 11: 145-156. doi: 10.2307/1216718.
    » https://doi.org/10.2307/1216718.
  • Thiers B. 2023. Index Herbariorum: A global directory of public herbaria and associated staff. https://sweetgum.nybg.org/science/ih/ 12 Nov. 2023.
    » https://sweetgum.nybg.org/science/ih/
  • Thomas WW, Jardim JG, Fiaschi P, Amorim AM. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In: Prado PI, Landau EC, Moura RT, Pinto LPS, Fonseca GAB, Alger K (eds.). Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia. Ilhéus, IESB/CI/CABS/UFMG/UNICAMP. (CD-ROM.)
  • Xue B, Guo X, Landis JB, et al 2020. Accelerated Diversification Correlated with Functional Traits Shapes Extant Diversity of the Early Divergent Angiosperm Family Annonaceae. Molecular Phylogenetics and Evolution 142: 106659. doi: 10.1016/j.ympev.2019.106659
    » https://doi.org/10.1016/j.ympev.2019.106659

Edited by

Editor-in-Chief:

Thaís Elias Almeida

Associate Editor:

Paulo Takeo Sano

Publication Dates

  • Publication in this collection
    05 July 2024
  • Date of issue
    2024

History

  • Received
    29 Sept 2023
  • Accepted
    20 Feb 2024
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