First record of Aristolochia wankeana (Aristolochiaceae, Piperales) from Brazil with a key to the species of Aristolochia subser. Anthocaulicae from the Brazilian Amazon

Primeiro registro de Aristolochia wankeana (Aristolochiaceae, Piperales) no Brasil, com uma chave para as espécies de Aristolochia subser. Anthocaulicae da Amazônia brasileira

ABSTRACT

Aristolochia comprises about 450 species, occurring mainly in tropical regions. Here, we record for the first time Aristolochia wankeana in Brazil, specifically in two municipalities in the state of Amazonas (Presidente Figueiredo and Rio Preto da Eva). Previously, this species had only been recorded in Guyana and French Guiana. We provide the species description based on the new records, a preliminary extinction risk assessment, photographic plates, an updated geographic distribution map, ecological comments, and an updated key for species identification of Aristolochia subser. Anthocaulicae from the Brazilian Amazon.

KEYWORDS:
cauliflory; flora of South America; Guiana Shield; lianas; Neotropical region

RESUMO

Aristolochia possui cerca de 450 espécies, ocorrendo principalmente em regiões tropicais. Aqui registramos pela primeira vez Aristolochia wankeana no Brasil, especificamente em dois municípios do estado do Amazonas (Presidente Figueiredo e Rio Preto da Eva). A espécie havia sido anteriormente registrada apenas na Guiana e Guiana Francesa. Neste estudo, fornecemos a descrição da espécie com base nos novos registros, a avaliação preliminar do risco de extinção, pranchas fotográficas, um mapa de distribuição geográfica atualizado, comentários ecológicos, e uma chave atualizada de identificação das espécies de Aristolochia subser. Anthocaulicae da Amazônia brasileira.

PALAVRAS-CHAVE:
caulifloria; Escudo das Guianas; flora da América do Sul; lianas; região Neotropical

Aristolochia L. is the largest genus of the family Aristolochiaceae (Piperales), with about 450 species distributed mainly in tropical regions (POWO 2023). In Brazil, the genus is represented by 85 species distributed across all phytogeographic domains, except the Pantanal (BFG 2024; Freitas et al. 2022). In the Brazilian Amazon, 37 species are known (BFG 2024).

The genus Aristolochia includes plants with climbing habit, herbs or shrubs, corky stems, alternate simple, petiolate or sessile leaves (with pseudostipules present or absent), leaf blades with 3-7 primary veins, axillary cauliflorous and racemose inflorescences (pauciflorum or not), monochlamydeous gamosepalous flowers presenting utricle, tube and limb, capsular, usually cylindrical or fusiform fruits with numerous concave-convex or flat seeds (alates or not) (Freitas and Alves-Araújo 2017; Freitas et al. 2022).

Within the taxonomic groups of Aristolochia that occur in South America, 25 species are part of Aristolochia subseries Anthocaulicae F. González, which present inflorescences in ramiflorous or cauliflorous racemes, with internodes between the flowers reduced 5 mm, and flowers subtended by small bracts (González 1990; 1991). This subseries is distributed in the Amazon and Atlantic Forest, as well as in some countries of Central America (BFG 2024; POWO 2023). Aristolochia wankeana J. Freitas, F. González & Poncy is a representative of this subseries and was described in 2020, with known occurrences at that time in Guyana and French Guiana. It forms a species complex with A. cornuta Mast. and A. iquitensis O.C.Schmidt, both being distinguished by perianth analysis using geometric morphometry (Freitas et al. 2020). Recent collections in Amazonas state, Brazil, expanded the distribution of A. wankeana and here we present the first record of this species for Brazil, with a morphological description, taxonomic comments, an updated distribution map, high-resolution photographs and an updated identification key for the species that occur in the Brazilian Amazon.

Specimens of A. wankeana were collected in August 2019 and August 2023 in the municipalities of Rio Preto da Eva and Presidente Figueiredo, Amazonas state, Brazil, respectively. The climate in the region is tropical humid with no dry season (Sombroek 2001), of the type Af according to the Köppen-Geiger climate classification (Beck et al. 2018). The material was deposited in the INPA herbarium [acronym according to Thiers (2024, continuously updated)]. The species determination was based on Freitas et al. (2020). We used characters collected in the field and observed the material available in the herbarium. We also dissected the flowers stored in 70% alcohol. We obtained the measurements presented here through image analysis using the ImageJ software (Schneider et al. 2012).

We created a geographic distribution map of the known records of A. wankeana in the R environment, version 4.3.3 (R Core Team 2024), with the R packages grid (R Core Team 2024), sf (Pebesma 2018; Pebesma and Bivand 2023) and tmap (Tennekes 2018). We obtained the shapes of South American countries and Brazilian states by R packages rnaturalearth (Massicotte 2023) and geobr (Pereira and Gonçalves 2024), respectively. Based on the available records, we estimated the extension of occurrence (EOO) and the area of occupation (AOO) of the species using the GeoCAT platform (Bachman et al. 2011) to determine the preliminary conservation status of A. wankeana using the criteria of IUCN (2012).

Aristolochia wankeana J. Freitas, F. González & Poncy

(Figures 1 and 2)

Figure 1
Aristolochia wankeana. A - habit; B - flower bud; C - flower; D - side view of flower with floral visitor; E - fimbriae; F - trichomes at the entrance to the flower tube; G - gynostemium and floral visitor Megaselia scalaris; H - floral visitor Megaselia scalaris. Credits: A-C, E by A.M. Araújo; D, F-H by C.A.S. Batista.

Figure 2
Aristolochia wankeana. A - leaves; B - abaxial leaf; C - abaxial leaf showing the base and primary veins; D - fruit; E - inflorescence showing the fimbriae. Specimens: A-B = Araújo A. M. 211; E = Araújo A. M. 191; C = Batista C.A.S. 19; D-F = Batista, C.A.S. 18). Credits: Adriane Maciel.

Type - FRENCH GUIANA. Village de Saint-Elie, 4°50’0’’N, 53°18’0’’W, 120 m, 16 November 1998 (fl.), Poncy et al. 1160 (Holotype: P00187008!; isotypes: CAY014365!, NY!).

Description - Woody climbers with stems 0.5-0.8 cm in diameter, twigs with internodes 9-9.9 cm long. Pseudostipules absent. Petiole 4.2-5.3 cm long, pubescent; leaves obovate, 9.1-15.5 × 3-7.2 cm, chartaceous, adaxial surface glabrous, abaxial surface pubescent, lobed base, lobes with 1.3-1.7 cm of invagination, acuminate apex, basal primary veins 5. Inflorescences cauliflorous 13.6-14 cm long, ca. 20 cm above the ground, ca. 8 to 10 flowers. Peduncle 3-6.7 cm long, cream to yellowish perianth with vinaceous lines externally; utricle obovoid, 1.9-2 cm long; syrinx 0.5-0.6 cm long, tube tapering, 1-1.2 cm long and 0.5-0.6 cm in diameter proximally, 0.6-0.7 cm in diameter distally; limb falcate, two oblong lateral lobes, 3.6-5.1 × 1-1.2 cm, stripes yellow with purple, adaxially fimbriated at the apex of the lobes, yellow fimbriae with purple apex, base of the limb emarginate, yellow with red trichomes at the entrance of the tube, apex obtuse. Gynostemium 6-lobed, 0.3-0.4 cm long; anthers ca. 0.2 cm long. Capsule mature dehiscent, 6-carpellate, ca. 9 × 2.7 cm. Seeds not seen.

Material examined - BRAZIL. Amazonas: Presidente Figueiredo, Balbina, Trilha da Sussuarana, 1°54’50’’S, 59°24’36’’W, 176 m, 27 August 2023 (fl.), Araújo, A.M. et al. 191 (INPA![298855]); ibid., 1°54’54’’S, 59°24’32’’W, 178 m, 28 August 2023 (fl.), Araújo, A.M. et al. 211 (INPA![298875]); Amazonas: Rio Preto da Eva, BR-174, Parcelas do PDBFF, acampamento Porto Alegre, 2°22’11’’S, 59°58’2’’W, 121 m,14 August 2019 (fl.; fr.), Batista, C.A.S. 18 (INPA![284468]); ibid., 2°22’11’’S, 59°58’2’’W, 106 m, 20 August 2019 (ste.), Batista, C.A.S. 19 (INPA![298894]).

Preliminary conservation status - Aristolochia wankeana occurs in Guyana, French Guiana, and Brazil, with EOO of 362,257.561 km², and AOO of 56,000 km². The estimated number of populations was >10 (“condition a”) with no observed decrease in the populations (“condition b”), therefore the species was categorized as of Least Concern - LC (B1a, B2biii) according to IUCN criteria.

Distribution, habitat, and phenology - Aristolochia wankeana is found in French Guiana, Guyana (Freitas et al. 2020) and the state of Amazonas in Brazil (this study) occurring in both primary and secondary tropical rainforests (Figure 3). In Brazil, individuals were found in terra firme forests, at elevation ranging from 106 to 178 m.a.s.l. In Rio Preto da Eva, the species was found within the conservation area of the Biological Dynamics of Forest Fragments Project (BDFFP; https://pdbff.org.br/), and in Presidente Figueiredo near the Uatumã Biological Reserve (Uatumã Rebio; https://www.gov.br/icmbio/pt-br/assuntos/biodiversidade/unidade-de-conservacao/unidades-de-biomas/amazonia/lista-de-ucs/rebio-do-uatuma). In both areas the species occurred in primary tropical rainforest with canopy up to 30 m and clayey soil. The new collections, observed bearing flowers and fruits in August, represent a novelty in the phenological knowledge of the species. According to Freitas et al. (2020), specimens bearing flowers were collected in April, July, and between October and December, while specimens bearing both flowers and fruits were collected in April and between October and December.

Figure 3
Geographical distribution of the known locality records of Aristolochia wankeana. Grey circles = previous records; black triangles = new records.

Remarks - While collecting specimen Batista C.A.S. 19 (INPA 298894), a visiting fly of the superfamily Muscoidea (Diptera: Calyptratae) was observed landing on a flower (Figure 1d), although it was not possible to capture it for identification to specific level. Specimens of the fly Megaselia scalaris (Loew, 1866) (Diptera: Phoridae) (Figure 1h) were found inside the flowers of specimen Araújo, A.M. et al. 191 (INPA 298855). The presence of M. scalaris may indicate a potential pollinator of A. wankeana, as this genus is commonly found in Aristolochia flowers (Hipólito et al. 2012). However, studies of pollination biology are recommended. Flies are typically attracted to Aristolochia flowers due to their unpleasant odor, where they oviposit (Hipólito et al. 2012). The presence of trichomes on the flower tube precludes the exit of flower visitors until pollen grains are released, allowing them to be transported to another flower (Freitas and Alves-Araújo 2017).

Key to the species of Aristolochia subseries Anthocaulicae F. González in the Brazilian Amazon forest

1. Limb of the perianth unilobed 2

1’. Limb of the perianth bilobed (side lobes) or bilabiate (upper and lower lips) 8

2. Limb of the perianth peltate at its base 3

2’. Limb of the perianth not peltate at its base 6

3. Leaf lamina peltate or slightly peltate at its base 4

3’. Leaf lamina not peltate at its baseA. lagesiana Ule

4. Leaf base deeply cordate. Capsule 2-3 cm longA. goudotii Duch.

4. Leaf base truncate, slightly cordate or rounded. Capsule 6-12.5 cm long 5

5. Tube 1.6-3 cm long; syrinx present, inequilateralA. ruiziana Duch.

5’. Tube 1-1.3 cm long; syrinx absentA. guentheri O.C.Schmidt

6. Limb of the perianth with caudated apexA. lanceolatolorata S.Moore

6’. Limb of the perianth not caudated 7

7. Limb ovate, 0.4-0.9 cm wideA. disticha Mast.

7’. Limb very widely ovate, 2.8-3 cm wideA. lorenae J.Freitas & F.González

8. Limb bilobed 9

8’. Limb bilabiate 11

9. Lobes of the perianth limb oblong, slightly curved downwards, with fimbriae on the distal portion of their inner surfacesA. wankeana J.Freitas, F.González & Poncy

9. Lobes of the perianth limb linear or strongly curved downwards, efimbriate 10

10. Lobes of the perianth limb upright, lineariform, 1.0-3.0 × 0.1-0.2 cmA. cornuta Mast.

10. Lobes of the perianth limb curved downwards, oblong, hypocrepiform, 1-2 × 0.5-1.2 cmA. iquitensis O.C.Schmidt

11’. Leaf lamina not peltate at its base; inflorescences ca. 15 cm longA. klugii O.C. Schmidt

11. Leaf lamina peltate at its base; inflorescences ca. 2 cm longA. cremersii Poncy

ACKNOWLEDGMENTS

This study was financed in part by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil - Finance Code 001. AMA thanks the Graduate Program in Botany (INPA), INPA herbarium, CAPES for a doctoral fellowship, and Francisco Farroñay for assistance with Photoshop. CASB thanks CAPES for a doctoral fellowship, the Graduate Program in Ecology (INPA) and the Biological Dynamics of Forest Fragment Project (BDFFP) for technical and financial support. ROP thanks CAPES for a postdoctoral fellowship with the Graduate Program in Natural Resources (PRONAT) at Universidade Federal de Roraima. AMA, ROP and ATM thank Instituto Chico Mendes de Conservação da Biodiversidade - ICMBIO for field support in Vila de Balbina. MMMS thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a postdoctoral fellowship (PROTAX-PDJ 151271/2023-2). JF thanks CNPq and the Brazilian Ministry of Science, Technology and Innovation (MCTI) (within the scope of the Programa de Capacitação Institucional - PCI) at Instituto Nacional da Mata Atlântica (INMA) for the fellowship granted (grant # 301430/2024-1). This is study 873 of the BDFFP Technical Series (BDFFP INPA/STRI). We thank an anonymous reviewer, the associate editor and the editor-in-chief for their suggestions.

REFERENCES

• Bachman, S.; Moat, J.; Hill, A.W.; de la Torre, J.; Scott, B. 2011. Supporting Red List threat assessments with GeoCAT: geospatial conservation assessment tool. ZooKeys 150: 117-126.
• Beck, H.E.; Zimmermann, N.E.; McVicar, T.R.; Vergopolan, N.; Berg, A.; Wood, E.F. 2018. Present and future Köppen-Geiger climate classification maps at 1-km resolution. Scientific Data 5: 180214.
• Brazil Flora Group. 2024. Brazilian Flora 2020 project. Checklist dataset. Version 393.398. Instituto de Pesquisas Jardim Botanico do Rio de Janeiro. ( (https://doi.org/10.15468/1mtkaw ). Accessed on 09 Feb 2024.
  » https://doi.org/10.15468/1mtkaw
• Freitas, J.; Alves-Araújo, A. 2017. Flora do Espírito Santo: Aristolochiaceae. Rodriguésia 68: 1505-1539.
• Freitas, J.; de Lírio, E.J.; dos Santos-Moraes, Q.; Santos-Miranda, V.; Nichio-Amaral, R.; et al. 2022. New records of Aristolochia (Aristolochiaceae) from Brazil: the importance of citizen science as a tool to study geographic distribution, conservation and insect-plant interactions. Revista Mexicana de Biodiversidad 93: e934971.
• Freitas, J.; González, F.; Poncy, O.; Feuillet, C.; Alves-Araújo, A. 2020. Floral geometric morphometrics unveils a new cauliflorous species of Aristolochia (Aristolochiaceae) from the Guiana Shield. Phytotaxa 474: 1-14. doi: 10.11646/phytotaxa.474.1.1
  » https://doi.org/10.11646/phytotaxa.474.1.1
• González, F.A. 1990. Flora de Colombia 12 Aristolochiaceae Universidad Nacional de Colombia, Bogotá, 184 p.
• González, F. 1991. Notes on the systematics of Aristolochia subsect. Hexandrae Annals of the Missouri Botanical Garden 78: 497-503.
• Hipólito, J.; Viana, B.F.; Selbach-Schnadelbach, A.; Galetto, L.; Kevan, P.G. 2012. Pollination biology and genetic variability of a giant perfumed flower (Aristolochia gigantea Mart and Zucc., Aristolochiaceae) visited mainly by small Diptera. Botany 90: 815-829.
• IUCN. 2012. International Union for the Conservation of Nature. IUCN Red List Categories and Criteria Version 3.1. 2nd ed. ( (https://portals.iucn.org/library/sites/library/files/documents/RL-2001-001-2nd.pdf ). Accessed on 10 Jun 2024.
  » https://portals.iucn.org/library/sites/library/files/documents/RL-2001-001-2nd.pdf
• Massicotte, P.; South, A. 2023. rnaturalearth: World Map Data from Natural Earth. R package version 1.0.1. ( (https://CRAN.R-project.org/package=rnaturalearth ). Accessed on 01 Feb 2024.
  » https://CRAN.R-project.org/package=rnaturalearth
• Pebesma, E. 2018. Simple features for R: standardized support for spatial vector Data. The R Journal 10: 439-446.
• Pebesma, E.; Bivand, R. 2023. Spatial Data Science: With Applications in R 1st ed. Chapman and Hall/CRC, New York, 314p.
• Pereira, R.; Goncalves, C. 2024. geobr: Download of official spatial data sets of Brazil. R package version 1.8.2. ( (https://github.com/ipeaGIT/geobr ). Accessed on 01 Feb 2024.
  » https://github.com/ipeaGIT/geobr
• POWO. 2023. Plants of the World Online. Royal Botanic Gardens, Kew. ( (http://www.plantsoftheworldonline.org/ ). Accessed on 01 Dec 2023.
  » http://www.plantsoftheworldonline.org/
• R Core Team. 2024. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ( (https://www.R-project.org/ ). Accessed on 01 Feb 2024.
  » https://www.R-project.org/
• Sombroek, W. 2001. Spatial and temporal patterns of Amazon rainfall: consequences for the planning of agricultural occupation and the protection of primary forests. Ambio 30: 388-396.
• Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671-675.
• Tennekes, M. 2018. tmap: Thematic Maps in R. Journal of Statistical Software 84: 1-39. doi.org/10.18637/jss.v084.i06
  » https://doi.org/10.18637/jss.v084.i06
• Thiers, B. 2024 [continuously updated]. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. ( (http://sweetgum.nybg.org/science/ih/ ). Accessed on 25 Aug 2024.
  » http://sweetgum.nybg.org/science/ih/

• CITE AS:

  Araújo, A.M. de; Batista, C.A. dos S.; Perdiz, R. de O.; Mello, A.T.; Soares, M.M.M.; Freitas, J. 2024. First record of Aristolochia wankeana (Aristolochiaceae, Piperales) from Brazil with a key to the species of Aristolochia subser. Anthocaulicae from the Brazilian Amazon. Acta Amazonica 54: e54bc24128.

Data availability

The data that support the findings of this study are available, upon reasonable request, from the corresponding author, Adriane Maciel de Araújo.

Edited by

ASSOCIATE EDITOR:

Ricarda Riina

Publication Dates

• Publication in this collection
  11 Oct 2024
• Date of issue
  Jul-Sep 2024

History

• Received
  03 Apr 2024
• Accepted
  22 Aug 2024