Research Article |
Corresponding author: Emerson R. Pansarin ( epansarin@ffclrp.usp.br ) Academic editor: Brecht Verstraete
© 2024 Emerson R. Pansarin.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Pansarin ER (2024) Rediscovery and revalidation of the Brazilian endemic Vanilla schwackeana Hoehne (Orchidaceae): its distribution and phylogenetic position. Plant Ecology and Evolution 157(1): 32-41. https://doi.org/10.5091/plecevo.110331
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Background and aims – With 40 species, Brazil is the centre of diversity for Vanilla. Frederico Carlos Hoehne described eight Vanilla species for the Brazilian flora, including Vanilla schwackeana, an obscure taxon currently assumed to be a synonym of V. planifolia. While studying Neotropical Vanilla, plants were found in gallery forests of the Vale do Rio Doce region, Minas Gerais, south-eastern Brazil. Based on the examination of the protologues of the Brazilian species, in addition to the study of herbarium specimens, it was verified that the plants correspond to the rare V. schwackeana.
Material and methods – A redescription of V. schwackeana is provided, and a morphological comparison with other Neotropical taxa is presented. An illustration of V. schwackeana based on living specimens is provided, and its geographic distribution is presented based on recent findings. The position of V. schwackeana within Vanilla is discussed based on both morphological data and a molecular phylogeny.
Key results – Vanilla schwackeana is distinguishable by its pseudopetiolate leaves, by its largely elliptic to obelliptic leaf blades with attenuate base and acuminate apex, by its apical racemes with small flowers, by its yellow labellum with white undulate-crenulate margins, and by its papillous appendages on the apical portion of the labellar crest. Both morphological and molecular data suggest a close relationship of V. schwackeana with V. appendiculata, V. hartii, and the Brazilian endemic V. rupicola. Based on current data, V. schwackeana is assessed as Critically Endangered.
Conclusion – Integrative taxonomy was crucial to understand the identity and species boundaries of V. schwackeana. The V. appendiculata/V. schwackeana/(V. hartii/V. rupicola) clade comprises an unrecognized infrageneric Vanilla group. It seems plausible that the formation of a new infrageneric group will be necessary. As the habitat of V. schwackeana has been devastated by iron ore extraction, conservation strategies for this Brazilian endemic species will be necessary.
Atlantic Forest, Cerrado, phylogeny, systematics, taxonomy, Vanilleae, Vanilloideae
Frederico Carlos Hoehne (1882–1959), a Brazilian botanist who devoted his life to the study of the Brazilian flora, was the first director of the Botanical Garden and Botanical Institute of São Paulo. During his fieldworks in Brazil, Hoehne collected more than 10,000 plant specimens, leading to the description of at least 200 species new to science. He wrote more than 200 scientific papers, mostly regarding the plants he collected on his field trips (
The description of V. schwackeana was based on a single specimen collected in Minas Gerais, south-eastern Brazil, by Carl August Wilhelm Schwacke (Schwacke 11106, RB), who, however, did not specify the locality.
With more than 100 species distributed throughout tropical regions of Americas, Africa, and Asia, Vanilla is the most species-rich genus among the Vanilloideae (
In the course of studies on Neotropical Vanilla, an unidentified species was found in gallery forests of the Vale do Rio Doce region, Minas Gerais, south-eastern Brazil. Based on the examination of the protologues of the Brazilian species, in addition to a study of herbarium specimens, it was verified that the plants correspond to the rare V. schwackeana. A redescription of this Vanilla is presented, and a morphological comparison with other Neotropical taxa is provided. An illustration of V. schwackeana based on living specimens is presented, and the geographic distribution of this rare taxon is provided based on recent findings. The position of V. schwackeana within Vanilla is discussed based on both morphological data and a molecular phylogeny for Vanilla.
The fieldwork was performed along the Vale do Rio Doce, in the state of Minas Gerais, south-eastern Brazil. The climate of the region is classified as “Aw”, namely semi-humid warm tropical (
Fresh and herbarium material of flowering and fruiting plants was used for the study. Photographs were based on specimens collected in the field. Measurements were made directly on the floral structures using a Vernier caliper. The vegetative structures, inflorescence, and flowers were photographed with a Nikon D-SLR D800 camera and a Micro Nikkor 105 mm f2.8 lens. Floral details were analysed with a Stereozoom Leica S8 APO stereomicroscope with an integrated photo output. Digitized images were used for diagramming a template over a black background, following the model presented by
The terminology for describing shapes followed
The map with the geographic distribution of V. schwackeana was produced with QGIS v.3.32.2 (
The preliminary conservation status of V. schwackeana was defined according to the IUCN Red List categories and criteria, and guidelines (
A total of 57 Vanilla accessions (41 species) were analysed and are referred to here as the ingroup. Lecanorchis multiflora J.J.Sm. was selected as an outgroup according to previous phylogenetic studies on Vanilloideae (e.g.
DNA of Vanilla schwackeana was extracted from fresh material according to a modified CTAB method (
A data matrix of ITS containing 58 accessions was used for phylogenetic analyses. Maximum parsimony analysis (MP) was run with PAUP* v.4.0b5 (
BRAZIL – Minas Gerais • s.loc.; s.d.; Schwacke 11106; holotype: RB [RB00542725, accession n° 37015].
Nomadic vines, up to 8 m in length. Roots axillary, 1.8–2.2 mm diam., whitish to brownish, one per node. Stem climbing, sinuous, cylindrical, glabrous, fleshy, and green; internodes 42–80 × 3–4 mm. Leaves 5.5–11 × 3–5.5 cm, alternate, distichous, elliptic to obelliptic, symmetric to asymmetric, slightly fleshy, glabrous, green, pseudopetiolate, margin entire, base attenuate, apex acuminate; pseudopetiole 5.5–8 mm. Inflorescence 3.5–6 cm long, apical or axillary, racemose, with up to 10 flowers opening in succession; 1–2 flowers opening each morning; bracts 4–8.5 × 3.5–7 mm, progressively smaller toward the apex, alternate, triangular to ovate, coriaceous, concave, patent. Flowers resupinate, pedicellate, abscission layer between perianth and ovary present; pedicel with ovary 3–3.5 × 0.35–0.42 cm, green, straight to incurved, dilated at the apex, subcylindrical in transverse section. Sepals 4.2–4.6 × 0.8–1.1 cm, free, oblanceolate, fleshy, slightly concave, pale green, margin entire, slightly incurved, apex acute to obtuse; dorsal sepal symmetric; lateral sepals asymmetric. Petals 4–4.4 × 0.7–0.9 cm, free, slightly spatulate, asymmetric, membranous, pale green, apex acute, adaxial surface with a central and longitudinally disposed keel. Labellum 1-lobed to slightly 3-lobed, 4.2–4.7 × 2.5–2.7 cm, yellowish, white in distal portion, inner surface with longitudinal yellow stripes, with a central crest near the apex, and with a penicillate callus just below the anther; central crest ca 4 mm wide, with yellow protrusions arranged in 3–5 longitudinal lines near the apex; penicillate callus 4.5–5 × 3.7–4.2 mm, yellow; margins fused from the base to ca ¾ of the column length forming a tubular nectar chamber; nectar chamber 1–1.2 cm long; lateral lobes rounded, margins undulate to crenulate; apical lobe rounded to emarginated, reflexed, margin undulate to slightly crenulate. Column 3.2–3.5 × 0.3–0.32 cm, semicylindrical, slender, sinuous, white, attenuate base, dilated to the apex, with white-hyaline hairs close to the stigma, apex ending in a membranous ochrea; anther 2.9–3 × 2.1–2.5 mm, ovate, white, versatile; rostellum 3.8–4.1 × 2.3–2.6 mm, trapezoidal, membranous, white. Fruits 11–15 × 2.8–3.2 cm, linear, incurved, slightly triangular in transverse section, fleshy.
Vanilla schwackeana. A. Part of a plant showing the sinuous stem and distichous leaves. B. Leaf. Note the elliptical shape of the leaf blade. C. Detail of a leaf showing the acuminate apex. D. Apical inflorescence. E. Flower in diagonal view. F. Flower in lateral view. G. Longitudinal section of a flower. The detail (dashed area) shows the labellum base. H. Longitudinal section of part of the labellum. Note the penicillate callus (arrow), the anther (a), and the rostellum (arrowhead). I. Detail of the labellum and column. Note the central crest of the labellum, the penicillate callus, and the anther. J. Dissected perianth. The detail (dashed area) shows the penicillate callus and the central labellar crest. K. Labellum in lateral view. L. Column in lateral view. M. Apex of the column: in lateral view with an articulated anther (above), in lateral view with a disarticulated anther (mid), and in abaxial view (below). Based on E.R. Pansarin 1568 (LBMBP).
Vanilla schwackeana occurs in both gallery forests and mesophytic semideciduous forests from the south of Vale do Rio Doce, eastern Minas Gerais, south-eastern Brazil (Fig.
Vanilla schwackeana blooms from September to October.
Critically Endangered: CR B2ab(i,ii,iii). Vanilla schwackeana is a rare species growing in mesophytic forests in the municipalities of Timóteo and Antônio Dias, southern region of Vale do Rio Doce. The populations only contain a few specimens. The species is known from only three herbarium collections, the holotype without any locality information and two more recent specimens. Since only two specimens have locality data, the EOO (extent of occurrence) cannot be calculated. The area of occupancy (AOO) is estimated to be 8 km2 (cell width 2 km), which falls within the limits for Critically Endangered (CR) under criterion B2 (area of occupancy). The two recent specimens are found in one location, which also falls within the limits of Critically Endangered under subcriterion a. The region where individuals of V. schwackeana are found is being studied for the extraction of iron ore by a mining company. The Vale do Rio Doce has known a long history of deforestation. The region comprises 81 municipalities, 24 of which comprise the “Vale do Aço” (Steel Valley), including Timóteo and Antônio Dias, where exploitation of iron ore has drastically reduced the native flora of the region to sparse forest fragments. I therefore project a continuing decline in (i) extent of occurrence, (ii) area of occupancy, and (iii) extent and/or quality of habitat. Considering these threats and the fact that the species is distributed in one location, V. schwackeana is assessed as Critically Endangered (CR).
BRAZIL – Minas Gerais • Antônio Dias, Comunidade Japao, semi-deciduous forest; 19°61’15”S, 42°77’26”W; 850 m; 6 Oct. 2022; E.R. Pansarin 1567; SPFR • Timóteo, semi-deciduous forest; 19°54’59”S, 42°69’56”W; 840 m; 7 Oct. 2022; E.R. Pansarin 1568; LBMBP.
Based on Hoehne’s hypothesis that the holotype of V. schwackeana is a mixture of elements from distinct Vanilla species and due to the size of the similar floral parts, a dissected flower from the material Schwacke 11106, deposited in the RB herbarium, was designated as the lectotype of V. schwackeana and synonymized under V. planifolia (
Vanilla schwackeana is easily recognized by its pseudopetiolate leaves, by its largely elliptic to obelliptic leaf blades with attenuate base and acuminate apex, by its apical inflorescence with small flowers, by its yellow labellum with white undulate-crenulate margins, and by its papillous appendages on the apical portion of the labellar crest. These characteristics suggest a close relationship of V. schwackeana with V. rupicola Pansarin & E.L.F.Menezes and with some species currently recognized in the V. planifolia group and V. trigonocarpa group, i.e. V. appendiculata Rolfe and V. hartii Rolfe, respectively (Table
Comparison of the morphological features of Vanilla schwackeana and related species. Vanilla rupicola data were obtained from
V. schwackeana | V. rupicola | V. appendiculata | V. hartii | |
Habit | hemiepiphytic | rupicolous | hemiepiphytica,b | hemiepiphytic |
Stem | scandent | reptant | scandenta,b | scandent |
Leaves (cm) | 5.5–11 × 3–5.5 | 3.2–9 × 2.8–5.2 | 13–19 × 3.9–5.7a | 6.5–8 × 2.5–3.5 |
14–17.7 × 4.2–4.9b | ||||
Leaves | pseudopetiolate | sessile | petiolatea,b | petiolate |
Leaf blade | elliptic to obelliptic | ovate to rounded | obovoida | elliptic |
spatulateb | ||||
Inflorescence | apical/lateral | apical/lateral | apicala,b | apical/lateral |
Sepals (cm) | 4.2–4.6 × 0.8–1.1 | 5.8–6.3 × 1–1.3 | 6.6 × 0.7a | 4.9–5.3 × 0.8–1.1 |
7.5–7.8 × 0.8–1.1b | ||||
Petals (cm) | 4–4.4 × 0.7–0.9 | 5.7–6.2 × 0.7–1.2 | 6.5 × 0.6a | 4.9–5.1 × 0.7–0.9 |
7.6–7.7 × 0.7–0.8b | ||||
Labellum (cm) | 4.2–4.7 × 2.5–2.7 | 5.6–6.3 × 3.2–3.5 | 6.8 × 1.6a | 4.4–4.7 × 2.3–2.4 |
3.8 × 2.9b | ||||
Labellar protrusions | papillous | papillous | finger-likeb | verrucose |
Column (cm) | 3.2–3.5 × 0.3–0.32 | 4.2–4.8 × 0.3–0.4 | 5.4 × 0.2a; 6.1 × 0.3b | 3.8–4 × 0.2–0.3 |
Phylogenetic analysis of the ITS region resulted in strongly congruent MP and BI trees (Fig.
Bayesian inference (right) and Maximum parsimony (left) analyses of Vanilla (Orchidaceae) based on ITS (nrDNA) showing the phylogenetic relationships among V. schwackeana (bold) and Neotropical congeners. Bootstrap values > 50% (MP) and posterior probability values > 0.5 (BI) are given above the branches. Acronyms after species names are Brazilian states: AM = Amazonas, AP = Amapá, GO = Goiás, MT = Mato Grosso, PA = Pará, PE = Pernambuco, SP = São Paulo. Vertical bars refer to the main Vanilla lineages: white bar = Neotropical Vanilla with membranaceous leaves, dashed bar = Old World/Caribbean clade, black bar = Neotropical Vanilla with non-membranaceous leaves.
My results reveal that V. schwackeana is easily distinguishable by its pseudopetiolate leaves, by its largely elliptic to obelliptic leaf blades with an attenuated base and acuminate apex, by its apical inflorescences with small flowers, by its yellow labellum with white undulate-crenulate margins, and by its papillous appendages on the apical portion of the labellar crest. Such characteristics suggest a close relationships of V. schwackeana with V. appendiculata, V. hartii, and the Brazilian endemic V. rupicola (
Integrative taxonomy was crucial to understand the identity and species boundaries of V. schwackeana. The V. appendiculata/ V. schwackeana/(V. hartii/V. rupicola) clade comprises an unrecognized infrageneric Vanilla group. The formation of a new infrageneric group comprising species from this clade will be necessary.
The author thanks ICMBIO for permission to collect (Protocol SISBIO number 35178-1), Elettra Greene for English revision, and Cristina Lourenço for help with fieldwork. Research supported by the São Paulo Research Foundation – FAPESP (Grant 2018/07357-5) and by CNPq (Productivity Research Grant 301773/2019-0).
Species of Vanilla included in the molecular study, their locations, vouchers and GenBank accession numbers. VAN = Vanilla germplasm bank, LBMBP Orchid House, Department of Biology, FFCLRP-USP, University of Sao Paulo, Brazil, available at https://www.lbmbplab.net/vanillacollection.