Ruehssia quirinopolensis (Apocynaceae), a new species from the Cerrado Domain, Brazil

Isa Lucia de Morais Fábio da Silva do Espírito Santo Alessandro Rapini Francisco Morales About the authors

Abstract

A new species of Apocynaceae, Ruehssia quirinopolensis, endemic to Serra da Confusão do Rio Preto and Serra da Igrejinha, Quirinópolis, state of Goiás, Brazil, is described and illustrated. It resembles R. rupestris, differing by the white corolla, adaxially villose and with a longer tube, and by its corona lobes with the upper portion lanceolate. Besides a distribution map for the new species, we provide a key to identify the nine species of Ruehssia that occur in Goiás. Ruehssia quirinopolensis is assessed here as Critically Endangered (CR).

Key words
Asclepiadoideae; Marsdenia; Neotropics; taxonomy

Resumo

Uma nova espécie de Apocynaceae, Ruehssia quirinopolensis, endêmica da Serra da Confusão do Rio Preto e Serra da Igrejinha, Quirinópolis, estado de Goiás, Brasil, é descrita e ilustrada. Ela se assemelha a R. rupestris, diferindo, pela corola branca, adaxialmente vilosa e com tubo mais longo, e pelos lobos da corona com a porção superior lanceolada. Além de um mapa de distribuição para a nova espécie, apresentamos uma chave para identificar as nove espécies de Ruehssia que ocorrem em Goiás. Ruehssia quirinopolensis é avaliada aqui como Criticamente em Perigo (CR).

Palavras-chave
Asclepiadoideae; Marsdenia; Região Netropical; taxonomia

Introduction

The Apocynaceae comprise around 5,350 species and more than 370 genera (Endress et al. 2018Endress ME, Meve U, Middleton DJ & Liede-Schumann S (2018). Apocynaceae. In: Kadereit JW & Bittrich V (eds.) Flowering plants. Eudicots. Apiales and Gentianales (except Rubiaceae), K. Kubitzki (ed.), Families and genera of vascular plants. Vol. 15. Springer, Cham. Pp. 207-411. ). They are represented by nearly 70 genera and approximately 780 species in Brazil; more than half of these species are endemic (Apocynaceae in Flora do Brasil 2020). In Gentianales, the family is easily recognized by the presence of latex, a gynoecium with two carpels free at the ovary level but fused towards the apex to form a style-head, and a remarkable gradual synorganization of floral structures, culminating with the gynostegium (absent in the basal rauvolfioid grade) and the pollinaria (absent in the basal ‘rauvolfioid-apocynoid’ grade): the gynostegium arises from the post-genital fusion of the androecium to the style-head and pollinaria are the pollen units of Periplocoideae, Secamonoideae and Asclepiadoideae (Rapini 2012Rapini A (2012). Taxonomy “under construction”: advances in the systematics of Apocynaceae, with emphasis on the Brazilian Asclepiadoideae. Rodriguésia 63: 75-88. ). Counterintuitively, the most specialized groups of Apocynaceae, in particular the Asclepiadoideae, show wider ranges of pollinators (Ollerton et al. 2019Ollerton J, Liede-Schumann S, Endress ME, Meve U, Rech AR, Shuttleworth A, Keller HA, Fishbein M, Alvarado-Cárdenas LO, Amorim FW, Bernhardt P, Celep F, Chirango Y, Chiriboga-Arroyo F, Civeyrel L, Cocucci A, Cranmer L, Silva- Batista IC, Jager L, Deprá MS, Domingos-Melo A, Dvorsky C, Agostini K, Freitas L, Gaglianone MC, Galetto L, Gilbert M, González-Ramírez I, Gorostiague P, Goyder D, Hachuy-Filho L, Heiduk A, Howard A, Ionta G, Islas-Hernández SC, Johnson SD, Joubert L, Kaiser-Bunbury CN, Kephart S, Kidyoo A, Koptur S, Koschnitzke C, Lamborn E, Livshultz T, Machado IC, Marino S, Mema L, Mochizuki K, Morellato LPC, Mrisha CK, Muiruri EW, Nakahama N, Nascimento VT, Nuttman C, Oliveira PE, Peter CI, Punekar S, Rafferty N, Rapini A, Ren Z-X, Rodríguez-Flores CI, Rosero L, Sakai S, Sazima M, Steenhuisen S- L, Tan C-W, Torres C, Trøjelsgaard K, Ushimaru A, Vieira MF, Wiemer AP, Yamashiro T, Nadia T, Queiroz J & Quirino Z (2019) The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study. Annals of Botany 123: 311-325.)

With about 3,375 species (Endress et al. 2018Endress ME, Meve U, Middleton DJ & Liede-Schumann S (2018). Apocynaceae. In: Kadereit JW & Bittrich V (eds.) Flowering plants. Eudicots. Apiales and Gentianales (except Rubiaceae), K. Kubitzki (ed.), Families and genera of vascular plants. Vol. 15. Springer, Cham. Pp. 207-411. ), Asclepiadoideae is the largest subfamily of Apocynaceae. The group is characterized by bisporangiate stamens and pollen in monads, gathered in pollinia coated by a pellicle from the tapetum cells; pollinia of adjacent stamens are then connected one another by a translator, secreted by the style-head before the anthesis and formed by a corpusculum and two caudicles (Rapini et al. 2001Rapini A, Mello-Silva R & Kawasaki ML (2001) Asclepiadoideae (Apocynaceae) da Cadeia do Espinhaço de Minas Gerais, Brasil. Boletim de Botânica da Universidade de São Paulo 19: 55-169.). Apart from Fockeeae, a nine-species tribe from the Old World in which pollinia are attached directly to the corpusculum (i.e., the translators lack caudicles), Asclepiadoideae is divided into two clades, one with pendent pollinia (Asclepiadeae) and other with erect pollinia (Ceropegieae-Marsdenieae) (e.g., Rapini et al. 2003Rapini A, Chase MW, Goyder DJ & Griffiths J (2003) Asclepiadeae classification: evaluating the phylogenetic relationships of New World Asclepiadoideae (Apocynaceae). Taxon 52: 33-50. , 2007Rapini A, Berg C & Liede-Schumann S (2007) Diversification of Asclepiadoideae (Apocynaceae) in the New World. Annals of the Missouri Botanical Garden 94: 407-422.; Fishbein et al. 2018Fishbein M, Livshultz T, Straub SCK, Simões AO, Boutte J, McDonnell A & Foote A (2018) Evolution on the backbone: Apocynaceae phylogenomics and new perspectives on growth forms, flowers, and fruits. American Journal of Botany 105: 495-513.). This latter clade comprises only one American lineage, treated until recently in a Pantropical genus, Marsdenia R. Br.

A phylogenetic study based on plastid and nuclear data (Espírito Santo et al. 2019Espírito Santo FS, Rapini A, Ribeiro PL, Liede-Schumann S, Goyder DJ & Fontella-Pereira J (2019) Phylogeny of the tribe Marsdenieae (Apocynaceae), reinstatement of the genus Ruehssia and the taxonomic treatment of the species from Brazil. Kew Bulletin 74: 1-79.) showed that Marsdenia s.l. is not monophyletic, with species scattered across the whole Marsdenieae. The American species of Marsdenia, however, form a clade, but not closely related to M. tinctoria R. Br., the type of Marsdenia. Thus, Ruehssia H. Karst., until then treated in the synonymy of Marsdenia, was reinstated to accommodate the neotropical species of Marsdenieae. The genus comprises ca. 110 species, with centers of diversity in southeastern Mexico, northwestern South America, and northeastern Brazil, each with approximately 20 species. It shows a large range of ecological tolerance, occurring in environments as distinct as wet forests, savannas and seasonally dry forests. Although morphologically heterogeneous, Ruehssia can be easily recognized among the neotropical Asclepiadoideae by the erect pollinia, as it represents the only American lineage of the clade Ceropegieae-Marsdenieae (Espírito Santo et al. 2019Espírito Santo FS, Rapini A, Ribeiro PL, Liede-Schumann S, Goyder DJ & Fontella-Pereira J (2019) Phylogeny of the tribe Marsdenieae (Apocynaceae), reinstatement of the genus Ruehssia and the taxonomic treatment of the species from Brazil. Kew Bulletin 74: 1-79.).

Espírito Santo et al. (2019)Espírito Santo FS, Rapini A, Ribeiro PL, Liede-Schumann S, Goyder DJ & Fontella-Pereira J (2019) Phylogeny of the tribe Marsdenieae (Apocynaceae), reinstatement of the genus Ruehssia and the taxonomic treatment of the species from Brazil. Kew Bulletin 74: 1-79. recognized 42 species of Marsdenieae in Brazil and formally transferred 41 from Marsdenia to Ruehssia (except R. macrophylla H. Karst., the type of Ruehssia); since then, species from the rest of South America, Puerto Rico and Cuba have also been transferred to or described in Ruehssia (Bárrios et al. 2020Bárrios S, Sustache JA, Goyder D & Hamilton MA (2020) New island record and conservation status of Puerto Rican Bank endemic plant species, Ruehssia woodburyana (Acev.-Rodr.) Goyder, comb. nov., formally transferred from Marsdenia. Biodiversity Data Journal 8: e47110. ; Keller & Liede-Schumann 2020Keller HA & Liede-Schumann S (2020) New combinations in Ruehssia for the South American species of Marsdenia (Apocynaceae-Asclepiadoideae). Phytotaxa 471: 283-289.; Keller et al. 2020Keller HA, Liede-Schumann S, Rapini A & Cáceres Moral S (2020). El género Ruehssia (Apocynaceae) en la Argentina, filogenia, nuevas combinaciones y nuevos registros. Darwiniana 8: 414-437.; Reuss et al. 2020Reuss SJ, Meve U, Mangelsdorff RD & Liede-Schumann S (2020) Transfer of Cuban Marsdenia to Ruehssia (Apocynaceae - Asclepiadoideae), and two new species in Ruehssia. Willdenowia 50: 29-37.). Roughly one fifth of the Brazilian species in the genus (9 species) was described in the last three years (Espírito Santo et al. 2018aEspírito Santo FS, Sousa DJL, Chagas DB, Morais IL, Ribeiro PL & Rapini A (2018a) Four new species of Marsdenia (Apocynaceae) from the Cerrado Domain. Systematic Botany 43: 571-578., bEspírito Santo FS, Santos APB, Ribeiro PL & Rapini A (2018b) Three new species of Marsdenia (Apocynaceae) from Brazil. Acta Botanica Brasilica 32: 247-253., cEspírito Santo FS, Bitencourt C, Ribeiro PL & Rapini A (2018c) Two new species of Marsdenia (Apocynaceae) from limestone outcrops in Brazil. Willdenowia 48: 109-116.) and most of them (6 species) are endemic to the Cerrado Domain. Among these findings, we had an equivocal plant with fruits from Quirinópolis, state of Goiás, vegetatively very similar to R. rupestris (F. Esp. Santo) F. Esp. Santo & Rapini, a species known only from an area of 100 m2 in the Diamantina Plateau, state of Minas Gerais (Espírito Santo et al. 2018aEspírito Santo FS, Sousa DJL, Chagas DB, Morais IL, Ribeiro PL & Rapini A (2018a) Four new species of Marsdenia (Apocynaceae) from the Cerrado Domain. Systematic Botany 43: 571-578.). In November 2018, we found plants of this population in Quirinópolis with flowers; this allowed as to recognize another undescribed specie from the Cerrado domain. Therefore, our aim here is to describe and illustrate this new species of Ruehssia.

The state of Goiás is nested in the Cerrado domain; it is dominated by savannas and shelters a high diversity of angiosperms (Santos et al. 2012Santos TR, Pinto JR, Lenza E & Mewa HA (2012) The tree-shrub vegetation in rocky outcrop cerrado areas in Goiás states, Brazil. Brazilian Journal of Botany 35: 281-294.; Soares et al. 2015Soares MP, Reys P, Pifano DS, Sá JL, Silva PO, Santos TM & Silva FG (2015) Relationships between edaphic factors and vegetation in savannas on the Brazilian Midwest region. Rodriguésia 62: 123-137.). Rocky outcrop cerrados cover around 7% of the state (Santos et al. 2012Santos TR, Pinto JR, Lenza E & Mewa HA (2012) The tree-shrub vegetation in rocky outcrop cerrado areas in Goiás states, Brazil. Brazilian Journal of Botany 35: 281-294.) and occur throughout the state, on small and large mountain ranges (Lima 2008Lima CP (2008) O cerrado rupestre no estado de Goiás com base em imagens Landsat ETM+. Dissertação de Mestrado. Universidade de Brasília, Brasília. 117p.). In southern Goiás, only ranges near Caldas Novas have been floristically investigated, whereas important formations around Cachoeira Alta, Itarumã, and Quirinópolis remains poorly explored. The few floristic studies in these regions focused mainly on trees and shrubs (e.g., Amaral et al. 2006Amaral AG, Pereira FF & Munhoz CB (2006) Fitossociologia de uma área de cerrado rupestre na Fazenda Sucupira, Brasília-DF. Cerne 12: 350-359.; Miranda et al. 2007Miranda SC, Silva-Júnior MC & Salles LA (2007) Comunidade lenhosa de cerrado rupestre na Serra Dourada, Goiás. Heringeriana 1: 43-53.; Lima et al. 2010Lima TA, Pinto JR, Lenza E & Pinto AS (2010) Florística e estrutura da vegetação arbustivo-arbórea em uma área de cerrado rupestre no Parque Estadual da Serra de Caldas Novas, Goiás. Biota Neotropica 10: 159-166.) and vegetation on cliffs and gallery forests around small creeks remains poorly known; besides, many of these areas have been destroyed, resting only small remnants of natural vegetation today. The present study resulted from a botanical survey of unexplored forests in Serra da Confusão do Rio Preto and Serra da Igrejinha, Quirinópolis, and an inventory of the Apocynaceae in these areas. The vascular flora of Quirinópolis has been surveyed since 2017 and focused mainly on the cliffs around the city. As a result, rare and endangered species as well as taxonomic novelties have been found (e.g., Bueno et al. 2019Bueno VR, Morais IL & Nakajima N (2019) Isostigma resupinatum (Coreopsideae, Asteraceae), a new species from Central Plateau, Goiás state, Brazil. Phytotaxa 408: 227-232.), and this distinctive erect species of Ruehssia described for the first time here.

Material and Methods

Samples were collected and processed following techniques described by Fidalgo & Bononi (1984)Fidalgo O & Bononi VLR (1984) Técnicas de coleta, preservação e herborização de material botânico. Manual 4. Instituto de Botânica, São Paulo. 62p. and Mori et al. (1989)Mori SA, Silva LAM, Lisboa G & Coradin L (1989) Manual de manejo do herbário fanerogâmico. Ed 2. Centro de Pesquisas do Cacau, Ilhéus. 104p.. Descriptions were made based on fresh material, herbarium specimens, and preserved flowers (alcohol 70%). The terminology for the morphological description follows Radford et al. (1974)Radford AE, Dickison WC, Massey JR & Bell CR (1974) Vascular plant systematics. Harper & Row Publishers, New York. 891p. and Stearn (2004)Stearn WT (2004) Botanical Latin. 4th ed. Timber Press, Portland. 560p.. Herbarium acronyms are cited according to Thiers (continuously updated). Data on distribution, habitat, and phenology were obtained from herbarium specimens and field notes. The conservation status was assessed by calculating the extent of occurrence (EOO) and the area of occupancy (AOO) with GeoCAT (Bachman et al. 2011Bachman S, Moat J, Hill AW, de la Torre J & Scott B (2011) Supporting red list threat assessments with GeoCAT: Geospatial conservation assessment tool. Zookeys 150: 117-126.) and applying the IUCN Red List Categories and Criteria (IUCN 2012IUCN (2012) IUCN red list categories and criteria version 3.1. 2nd ed. IUCN, Gland, Cambridge. 32p.). The AOO was calculated based on a user defined grid cell of 2 km.

Results and Discussion

Taxonomic treatment

Ruehssia quirinopolensis I. L. Morais & F. Esp. Santo, sp. nov.

Tipo: BRAZIL. GOIÁS: Quirinópolis, Serra da Confusão do Rio Preto, 18°30’48”S, 50°22’29”W, 680-700 m, 16.XI.2018, fl., I.L.Morais 5122 (holotype: JAR!, isotype: HUEFS!). Figs. 1-3

Figure 1
a-g. Ruehssia quirinopolensis – a. branch with inflorescence; b. flower, lateral view; c. flower, seen from above; d. flower, perianth removed to show the corona in front of gynostegium; e. corona lobe, frontal view; f. pollinarium. g. fruit. (a-f. Morais 5122; g. Morais & Morales 4818). Illustrated by Lucas Menezes Silva.
Figure 2
a-e. Ruehssia quirinopolensis – a-b. habit; c. inflorescence; d. flower, seen from above; e. fruit.

Ruehssia quirinopolensis is morphologically similar to R. rupestris (F. Esp. Santo) F. Esp. Santo & Rapini, differing by the white corolla (vs. greenish-vinaceous), adaxially villose, forming five rows of trichomes at the base of the tube (vs. adaxially pubescent only on the middle portion of the tube), with longer tube (> 9 mm vs. < 5.4 mm long) and lobes (> 5.8 mm vs. < 3.8 mm long), and corona lobes with the upper portion lanceolate (vs. ovate).

Erect shrubs, up to 1.7 m tall; stems cylindrical, glabrous. Leaves with petiole 0.3–1.0 cm long, glabrous; lamina 6–15 × 4.4–9(–11) cm, elliptic, base cordate or rounded, apex cuspidate, margins not revolute, with 2–4 colleters adaxially at the base of the midvein, fleshy and glabrous. Inflorescences umbelliform cymes, 7–32 flowers; peduncle 3–5.5 cm long, glabrous; bracts 1.12–1.82 × 0.81–1.1 mm, deltoid to ovate, scarious, margins ciliate; pedicels 1.2–1.6 cm long, glabrous; sepals 3–5 × 2.8–3.8 mm, ovate, greenish, apex acute, margins ciliate, abaxially glabrous, adaxially with five axilar alternisepalous colleters. Corolla tubular, basally swollen, white, with purple spots at the end of the anthesis, abaxially glabrous, adaxially villose, forming five rows of trichomes at the base of the tube; tube 9.1–10.1 × 4.6–6 mm; lobes 5.9–8.4 × 3.6–4.2 mm, ovate to ovate-oblong, apex rounded or irregularly emarginate, recurved, margins not ciliate, adaxially villose, glabrescent toward the apex. Corona lobes 4.2–5 × 1.8–2 mm, lower portion triangular, fused to the anther, the upper portion lanceolate, free, apex acute, incurved over the style-head. Gynostegium c. 7.8 mm long, stipitate (stipe c. 3.5 mm long), inserted within the corolla tube; style-head c. 1.6 × 1.7 mm, ovate; anthers c. 0.49 × 0.3 mm, the apical membranous appendix c. 1.65 × 1.3 mm, ovate-oblong; corpusculum 0.44–0.5 × 0.22–0.25 mm, ovoid, apex rounded, erect; caudicles c. 0.25–0.32 mm long; pollinia 0.48–0.65 × 0.25–0.31 mm, oblong. Fruits c. 10–12 × 2.9–3.2 cm, fusiform, glabrous; seeds c. 9 × 7 mm, brown, comose at the microphylar end, c. 200 seeds/fruit.

Additional specimens examined: BRAZIL. GOIÁS: Quirinópolis, Serra da Confusão do Rio Preto, 18°30’8”S, 50°52’29”W, 25.II.2017, fr., I.L. Morais & J.F. Morales 4818 (HUEFS, JAR); 18°24’29.94”S, 50°26’28.11”W, 2.V.2019, fr., D.A.R.B. Ventura 564 (JAR); Serra da Igrejinha, 18°07’34.24”S, 50°28’43.88”W, 6.I.2020, fl., I.L. Morais & J.F. Morales 5875 (JAR).

The species is endemic to Serra da Confusão do Rio Preto and to Serra da Igrejinha, Quirinópolis, state of Goiás, Brazil, growing on cliffs and surrounding areas, at 680–700 m. (Fig. 3). These formations shelter small fragments of rocky savannas that remained almost unexplored floristically until recently.

Figure 3
Distribution map of Ruehssia quirinopolensis with the Brazilian Cerrado in darker gray.

The epithet refers to Quirinopólis, a small city located at the southern base of the Serra da Confusão do Rio Preto, Goiás, Brazil.

Ruehssia quirinopolensis was collected with flowers from November to February, and with fruits from January to July.

The species is restricted to cliffs and surrounding areas, which are fire-prone during the dry season; most of the vegetation in the site was destroyed by a fire in September 2019 and is still regenerating. Due to the narrow distribution (extent of occurrence 12,5 km² and area of occupancy 16 km²), current habitat decreasing, and risk of fire, Ruehssia quirinopolensis is assessed here as Critically Endangered (CR), following criteria B1ab(i ii iii) + 2ab(i ii iii).

Ruehssia quirinopolensis is characterized by the erect shrubby habit, leaves with the lamina basally cordate or rounded, umbelliform inflorescences, flowers with white corolla, adaxially villose, forming five rows of trichomes at the base of the tube, stipitate gynostegium, and corona lobes with the lower part triangular and the upper part lanceolate. Vegetatively, it can be confused with R. rupestris, because of the habit, leaves, and inflorescence architecture, but R. quirinopolensis can be easily distinguished by the features included in the diagnosis. Other eight species of Ruehssia occur in Goiás: a key to separate them is given below. However, only one other species is found in Quirinópolis, R. altissima (Jacq.) F.Esp.Santo & Rapini, which is a woody vine (vs. shrub) with leaves densely pubescent (vs. glabrous).

Key to the species of Ruehssia from Goiás, Brazil

  1. 1. Shrubs.

    1. 2. Leaves with elliptic lamina, > 3.14 mm wide, cuspidate at the apex; corolla white, cream or reddish (not on limestone outcrops).

      1. 3. Sepals > 2.9 × 2.7 mm; corolla white, tubular, basally swollen, tube > 9 × 4.5 mm, lobes ovate to ovate-oblong, > 5.8 × 3.5 mm; corona lobes > 4.1 × 1.8 mm...................Ruehssia quirinopolensis

      2. 3’. Sepals < 2.7 × 1.7 mm; corolla cream or reddish, campanulate, tube < 3 × 3.1 mm, lobes elliptic, < 4 × 2.9 mm; corona lobes < 2.9 × 1.4 mm...................Ruehssia serpentina

    2. 2’. Leaves with lanceolate, narrowly elliptic or linear lamina, < 3.15 mm wide, attenuate to acute at the apex; corolla greenish to greenish-cream (only on limestone outcrops).

      1. 4. Sepals < 2.7 mm long; corolla throat pilose, tube < 2.3 × 4.1 mm, lobes < 5.1 mm long; corona lobes < 3.1 × 1.3 mm; corpusculum < 0.28 × 0.16 mm...................Ruehssia phallica

      2. 4’. Sepals > 3.2 mm long; corolla throat glabrous, tube > 4.9 × 5.9 mm, lobes > 5.9 mm long; corona lobes > 6.7 × 2.4 mm; corpusculum > 0.4 × 0.22 mm...................Ruehssia zehntneri

  2. 1’. Twiners.

    1. 5. Stems tomentose to villous; corolla abaxially pubescent; corpusculum < 0.16 × 0.06 mm; pollinia > 0.79 × 0.29 mm...................Ruehssia altissima

    2. 5’. Stems glabrous or pubescent; corolla abaxially glabrous; corpusculum > 0.16 × 0.07 mm; pollinia < 0.76 × 0.27 mm.

      1. 6. Corolla white.

        1. 7. Stems pubescent to glabrescent; leaves with ovate or cordiform (rarely elliptic) lamina; inflorescences formed by a set of umbelliform cymes; corolla tube < 1.6 mm long, lobes suberect; corona lobes inverted V-shaped (˄), completely fused to the anther, < 0.8 × 0.9 mm...................Ruehssia brasiliensis

        2. 7’. Stems glabrous; leaves with elliptic or oblong-elliptic lamina; inflorescences umbelliform; corolla tube > 3 mm long, lobes recurved; corona lobes with a lower portion with concave auricles, fused to the anther and an upper portion narrowly triangular, caudate, free, > 2.9 × 1.3 mm...................Ruehssia weddellii

      2. 6’. Corola vinaceous or greenish-yellow to brownish-yellow.

        1. 8. Sepals abaxially puberulent; corolla campanulate, vinaceous, tube > 3.9 mm wide, lobes > 2.3 mm wide; corpusculum > 0.34 mm long...................Ruehssia avacanoeira

        2. 8’. Sepals abaxially glabrous; corolla urceolate, greenish-yellow to brownish-yellow, tube < 3.1 mm wide, lobes < 1.7 mm wide; corpusculum < 0.2 mm long.........................................................Ruehssia neomanarae

Acknowledgements

Financial and logistical support was provided by the Universidade Estadual de Goiás (UEG), Campus Quirinópolis, Brazil, and the University of Bayreuth, Germany. The first author thanks Polla Renon Rodrigues, Dara Aparecida Ribeiro Boa Ventura, Aline Bezerra da Silva Santos, and Elisângela Soares, for field work support during 2017–2019. The third author thanks Athena de Morais Morales, for the support in the last two years. Alessandro Rapini is a Pq 2-CNPq researcher.

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Publication Dates

  • Publication in this collection
    20 Sept 2021
  • Date of issue
    2021

History

  • Received
    29 Apr 2020
  • Accepted
    23 June 2020
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