Cryptanthus euglossinii (Bromeliaceae: Bromelioideae), a new species from Chapada Diamantina, Bahia

Abstract

A new species of Cryptanthus, known exclusively from Chapada Diamantina, in the municipalities of Miguel Calmon and Jacobina, state of Bahia, Northeast Brazil, is described and illustrated. Cryptanthus euglossinii is characterized by having leaves that are reddish in the marginal region, white-scaly near the base and glabrous adaxially towards the apex, with the abaxial surface covered by trichomes that obscure the color of the leaf. Comparisons are made with two similar species, C. reisii and C. bibarrensis, that are considered closely related. Euglossinii bees were observed visiting the flowers of C. euglossinii and collecting floral essences on petals, a relationship that is the basis of the epithet of the new species. Cryptanthus euglossinii is considered Endangered (EN) based on an extent of occurrence of 860 km², an area of occupancy of 1,000 km², and criteria established by the IUCN.

Keywords:
Cryptanthoid complex; morphology; Seasonal Semideciduous Forest; taxonomy

Resumo

Uma nova espécie de Cryptanthus, conhecida exclusivamente da Chapada Diamantina, nos municípios de Miguel Calmon e Jacobina, estado da Bahia, Nordeste do Brasil, é descrita e ilustrada. Cryptanthus euglossinii é caracterizado por apresentar folhas avermelhadas na região marginal, branco-escamosas próximo à base e glabras adaxialmente ao ápice, com a face abaxial coberta por tricomas que obscurecem a cor da folha. Comparações são feitas com duas espécies semelhantes, C. reisii e C. bibarrensis, que são consideradas intimamente relacionadas. Abelhas Euglossinii foram observadas visitando as flores de C. euglossinii e coletando essências florais nas pétalas, relação que está na base do epíteto da nova espécie. Cryptanthus euglossinii é considerado em perigo de extinção (EN) com base em uma extensão de ocorrência de 860 km², uma área de ocupação de 1.000 km², e critérios estabelecidos pela IUCN.

Palavras-chave:
complexo Cryptanthoid; morfologia; Floresta Estacional Semidecidual; taxonomia

Introduction

The genus Cryptanthus Otto & A. Dietr. possesses 60 endemic species of Brazil ( Gouda et al., continuously updated ), of which four occur in the Caatinga domain ( Maciel 2020). Species of Cryptanthus generally occur up to 400 meters in elevation, and rarely exceed 700 meters, in phytophysiognomies associated with Atlantic Forest, Cerrado and Caatinga, such as ombrophilous forest, seasonal forest, restinga, campos de altitude and campos rupestres ( Leme et al. 2017 ).

Ecotones favor the occurrence of species of Cryptanthus within the Caatinga phytogeographical domain because of the high humidity of higher altitudes. These places possess Seasonal Semideciduous Forest ( Funch et al. 2005 ) and are situated between the Caatinga and the Atlantic Forest. They may also occur as patches of moist vegetation surrounded by a drier matrix in the mountainous parts of Chapada Diamantina.

Located at altitudes above 500 meters, Chapada Diamantina includes the highest areas of the Caatinga. It possesses a predominance of lithic soils and has suffered intense exploitation of its mineral resources due to is rich geological composition. The climate varies from tropical to semi-arid, with precipitation ranging from 500 to 1,000 mm, depending on altitude ( Velloso et al. 2002 ).

This paper describes and illustrates a new species of Cryptanthus (Bromeliaceae) from Seasonal Semideciduous Forest in the state of Bahia, Brazil.

Material and Methods

Botanical material was collected at sites that were selected with the specific objective of finding areas of Cryptanthus diversity for the study of their ecology and taxonomy. Field surveys were conducted with the purpose of expanding knowledge about the genus Cryptanthus in the Caatinga and its ecotones. The second author found the first populations of the new species described herein near the village of Itaitu in the municipality of Jacobina, state of Bahia, Brazil. Subsequently, in 2010, Fontana et al. documented the same species in the region (Fontana et al. 6385), after which the species was not collected again until 2017 (Bezerra et al. 23). Due to these records, field studies were intensified in the region, with deepening taxonomic investigation revealing the taxon to be a new species for the genus.

The descriptions and illustrations presented here are based on the examination of live and fertile specimens, which included the use of stereomicroscopes for observing characters (flower, sepals, petals, filaments, anthers, stigma, ovary, ovules, fruits and seeds) and performing dissections prior to the preparation of herborized specimens. Descriptive terminology follows Smith & Downs (1979), with adaptations suggested by Scharf & Gouda (2008). Definitions for the genera of the “Cryptanthoid” complex follow Leme et al. (2017 )

Specimens were herborized according to Fidalgo & Bononi (1989), and deposited in herbaria HVASF and HUEFS. Live specimens were introduced for cultivation at the Coleção de Plantas Vivas do Vale do São Francisco (Vivasf) in Petrolina, state of Pernambuco, and in Refúgio dos Gravatás, in Teresópolis, state of Rio de Janeiro, following guidelines recommended by the Convention on Biological Diversity (1992). The following herbaria were visited to investigate other records of the species: ALCB, HUEFS, HVASF and UFP (acronyms according to Index Herbariorum; Thiers, continuously updated).

The species of bees that visit the flowers in anthesis were registered by in situ observation. The total area of occupation of the species was obtained using Geospatial Conservation Assessment Tool (GeoCAT®; Bachman et al. 2011 ), in order to classify its conservation status.

Results

Taxonomy treatment

Cryptanthus euglossinii E.D.S. Almeida & Leme, sp. nov. Type: BRAZIL. BAHIA: Miguel Calmon, trail to the waterfall Véu de Noiva, 11°20’05.6”S, 40°30’12.9”W, 669 m elevation, 12.VI.2017, fl. and fr., E.D.S. Almeida 101 (Holotype: HVASF!; isotype: RB!). Figs. 1- 2

Plant stemless, terrestrial or saxicolous, propagating by basal shoots. Leaves 13–15 in number, recurvate, forming an open rosette. Leaf sheath trapeziform to sub-reniform, 1.5–2 × 2.5–3 cm, hyaline. Leaf blade linear-lanceolate, slightly narrowed toward the base, 27–45 × 1.8–2.5 cm, reddish adaxially with green or red margins, white-lepidote near the base, glabrous toward the apex, abaxially densely lepidote with the trichomes obscuring the blade color, margins slightly undulate, subdensely spinose, spines 1–1.5 mm long, antrorse, 4–8 mm apart, apex acuminate Inflorescence sessile, corymbose. Primary bracts foliaceous; Fascicles 6–8 in number, the basal ones ca. 38 × 17 mm (excluding the petals), with 5–6 flowers. Floral bracts narrowly triangular to lanceolate, 26–27 × 10–15 mm (at the base), brown-lepidote toward the apex, inconspicuously spinulose at the apex, equaling the midpoint of the sepals, apex acuminate. Flower sessile, 42–46 mm long (with extended petals). Sepals 18–21 mm long, hyaline at the base, greenish toward the apex. Sepals lobe ovate-lanceolate, 8–9 × 3–3.5 mm, sparsely brown-lepidote, entire to remotely spinulose, apex acuminate. Petals subspathulate, bearing lateral callosities, 30 × 6–6.5 mm, white, glabrous, connate at the base for ca. 5 mm, apex rounded. Filaments adnate to the petals for ca. 5 mm. Anthers dorsifixed near the middle, 5–7 mm long, white. Stigma conduplicate-patent, lobes ca. 5 mm long, margins crenulate. Ovary trigonous,

Figure 1 –
a-e. General aspects of Cryptanthus euglossini – a. habit; b. male flowers; c. hermaphrodite flower in the foreground and male flower in the background; d. Euglossa melanotricha (Euglossini, Apidae) visiting a flower of C. euglossinii; e. individuals of C. euglossinii blooming.

subclavate, 11–12 mm long, ca. 6 mm in diameter, glabrous. Ovules obtuse. Fruits 3–10 in number, baccate, 6–7 × 3–4 mm. Seeds ca. 3 × 2 mm.

Supplementary material examined (paratypes): Jacobina, Itaitu village, near the Véu de Noiva waterfall, 11°05’50.8”S, 40°39’05.8”W, 610 m elevation, 13.VI.2017, fl. and fr., E.D.S. Almeida 115 (HUEFS!); 26.I.2010, fl., A.P. Fontana et al. 6385 (HVASF!); 26.VIII.2016, fl., T.T. Bezerra et al. 23 (HVASF!).

The new species has morphological affinity with C. reisii Leme from the Atlantic Forest in the municipality of Itapetinga of southern Bahia State. However, C. euglossinii differs by having the following: greater number of leaves (13–15 vs. ca. 8 for C. reisii Leme); leaf blade with reddish adaxial face with a green or completely reddish marginal region ( vs. completely green), narrower leaf blade (1.8 –2.5 cm vs. 2.7–4.2 cm) with larger marginal spines (1–1.5 mm vs. 0.5 mm); basal fascicles with a greater number of flowers (5–6 vs. 3), sub-squamous brown floral bracts ( vs. squamous- lepidote) and larger floral bracts (26–27 × 10–15 mm vs. 16 × 8–10 mm); larger sepals (18–21 × 6 mm vs. 15 × 10 mm), longer sepal lobe (8–9 × 3–3.5 mm vs. 5 × 4 mm) and oval-lanceolate sepal lobe ( vs. sub-orbicular); petals with lateral callosities ( vs. absent callosities) and longer anthers (5–7 mm vs. 2–3 mm).

The morphological characteristics of C. euglossinii also approximate those of C. bibarrensis Leme. However, C. euglossinii differs by having the following: acaulescent habit ( vs. caulescent habit of C. bibarrensis Leme); rosette with fewer leaves (13–15 vs. ca. 20); leaf blade with reddish adaxial face, with green or completely reddish marginal region ( vs. leaf completely green) and sparsely distributed spines on leaf margins (4–8 mm vs. 2–5 mm); basal floral fascicles with greater number of flowers (5–6 vs ca. 3) and wider floral bracts (10–15 mm ( vs. 16 × 9 mm); longer and narrower sepal lobe (8–9 × 3–3.5 mm vs. 6 × 5 mm) and oval-lanceolate sepal lobe ( vs. largely elliptic to sub-orbicular).

It should be noted that C. reisii and C. bibarrensis are sympatric species, with the type locality of both being in Seasonal Semideciduous Forest in the municipality of Itapetinga, Bahia ( Leme 2002).

The epithet euglossinii refers to the observed phenomenon of male euglossine bees (Euglossini) visiting the flowers of the new species and collecting floral essences on petals, a relationship the remains poorly known for the family Bromeliaceae ( Siqueira Filho & Machado 2008).

Cryptanthus euglossinii occurs in areas of Seasonal Semideciduous Forest in the municipalities of Miguel Calmon and Jacobina of Bahia state, close to small perennial streams under forest shade between 400 and 600 meters of elevation. Due to its natural beauty, the region receives visitors throughout the year as disorganized ecotourism. In contrast to the drier Caatinga, and especially during the long droughts of recent years (2011–2017) in the Brazilian semi-arid region, farmers take their animals to pastures in the mountains where forage supply is greater due to the amount of vegetation and high humidity. Such animals are known to trample sites of occurrence of C. euglossini, thus increasing the risk of its local extinction.

Flowering of C. euglossini occurs between May and June, during the dry season, with each individual flowering for up to 42 days, with up to three flowers per day. Anthesis is diurnal and lasts for 7 to 16 hours. Euglossinie bees (Euglossini, Apidae, Hymenoptera), namely of the species Euglossa ( Euglossa) melanotricha Moure, 1967, Eulaema ( Apeulaema) nigrita Lepeletier, 1841, and Eulaema ( Apeulaema) cingulate (Fabricius, 1804), were observed visiting the flowers of C. euglossinii. During their visits these bees collected floral perfumes directly from the surface of petals. This Euglossini- Cryptanthus relationship was described by Siqueira Filho & Machado (2008), who reported bees of the genera Euglossa and Eulaema visiting flowers of Cryptanthus dianae Leme of the Atlantic Forest in the state of Pernambuco and performing similar behaviors of scraping the petals to collect floral perfumes.

An extent of occurrence of 860 km² and an area of occupancy of 1,000 km² were obtained based on areas of occurrence. Thus, the species is considered Endangered (EN) by criteria B1B2abi of the International Union for the Conservation of Nature (IUCN 2012).

Discussion

Within the Bromeliaceae family, the subfamily Bromelioideae has raised several questions about the monophyly of the genera that make up the clade, where molecular data has suggested that genera with high diversity are, in fact, polyphyletic, thus turning their attention to the morphological innovations of these groups ( Schulte et al. 2009 ; Silvestro et al. 2014 ). Cryptanthus, in molecular analyzes, presents itself as a monophyletic genus, closely related to Orthophytum, forming a monophyletic group ( Evans et al. 2015 ).

Figure 2 –
a-h. Illustration of Cryptanthus euglossinii – a. habit; b. leaf; c. longitudinal section of hermaphrodite flower; d. flower in lateral view; e. anther and stigma conduplicate-patent; f. calyx; g. fruit; h. seed.

The so-called “Cryptanthoid” complex contains the genera Cryptanthus Otto & A. Dietr.; Forzzaea Leme, S. Heller & Zizka; Hoplocryptanthus Leme, S. Heller & Zizka; Lapanthus Louzada & Versieux; Orthophytum Beer; Rokautskyia Leme, S. Heller & Zizka; and Sincoraea Ule, being the characteristics of Cryptanthus andromonoecious plants with compound or rarely pseudosimple, sessile, and shortly corymbose inflorescences ( Leme et al. 2017 ). Cryptanthus euglossinii, which conforms to the new strict concept of the genus, occurs in areas of Seasonal Semideciduous Forest in association with moist environments in the Caatinga phytogeographic domain, unlike C. bahianus L.B.Sm. and C. warren-loosei Leme, which occur in Caatinga sensu stricto. The evolutionary history of the genus includes rare biome shifts, with the reconstruction of the ancestral biome indicating a high degree of niche conservatism ( Cruz et al. 2017 ).

There are, in general, little field data for Cryptanthus species, and their populations suffer mainly from drastic reductions to their habitats, with most newly described species already being at high risk of extinction ( Leme et al. 2020 ). The area of occurrence of C. euglossinii is one kilometer from Parque Estadual Sete Passagens, an integral conservation unit located in the municipality of Miguel Calmon (BA). Intense land speculation, disorderly tourism and extensive agricultural activities occur in the surroundings of the park, all of which can have negative impacts on populations of C. euglossinii. A large contingent of species of this genus are exposed to similar negative impacts. Some species of Cryptanthus are Endangered exclusively in the Atlantic Forest and Cerrado, whereas other species are Data Deficient or Near Endangered ( Martinelli & Moraes 2013). Faced with this reality, and considering the threats to C. euglossinii, it is suggested that the species be included in the list of endangered species of Centro Nacional de Conservação da Flora.

Acknowledgements

The authors thank G.A.R. da Silva, for help in field works; A.C.R. Andrade-Silva, for help with the species identification of the collected bees; G. Surlo, for botanical illustration; and CNPq, for the scholarship granted to the first author during the period of preparation of this study.

• Bachman S, Moat J, Hill A, de la Torre J & Scott B (2011) Supporting Red List threat assessments with GeoCAT: Geospatial Conservation Assessment Tool. ZooKeys 150: 117-126.
• Convention on Biological Diversity (1992) Estudos avançados 6: 193-233.
• Cruz GAS, Zizka G, Silvestro D, Leme EMC, Schulte K & Benko-Iseppon AM (2017) Molecular phylogeny, character evolution and historical biogeography of Cryptanthus Otto & A. Dietr. (Bromeliaceae). Molecular Phylogenetics and Evolution 107: 152-165.
• Evans TM, Jabaily RS, Faria APG, Sousa LOF, Wendt T & Brown GK (2015) Phylogenetic relationships in Bromeliaceae subfamily Bromelioideae based on chloroplast DNA sequence data. Systematic Botany 40: 116-128.
• Fidalgo O & Bononi VLR (1989) Técnicas de coleta, preservação e herborização de material botânico. Instituto de Botânica, São Paulo. 62p.
• Funch LS, Funch RR, Harley R, Giulietti AM, Queiroz LP, França F, Melo E, Gonçalves CN & Santos T (2005) Florestas estacionais semideciduais. In: Juncá FA, Funch L & Rocha W (eds.) Biodiversidade e conservação da Chapada Diamantina. Ministério do Meio Ambiente, Brasília. Pp. 181-193.
• Gouda EJ, Butcher D & Gouda CS (continuously updated) Encyclopaedia of Bromeliads, Version 4. University Botanic Gardens, Utrecht. Available at <http://bromeliad.nl/encyclopedia/>. Access on 9 September 2020.
  » http://bromeliad.nl/encyclopedia/
• IUCN (2012) IUCN Red List categories and criteria: Version 3.1. 2nd ed. IUCN, Gland and Cambridge. 32p.
• Leme EMC (2002) Two new sympatric Cryptanthus species. The Cryptanthus Society Journal 12: 86-89.
• Leme EMC, Heller H, Ziska G & Halbritter H (2017) New circumscription of Cryptanthus and new Cryptanthoid genera and subgenera (Bromeliaceae: Bromelioideae) based on neglected morphological traits and molecular phylogeny. Phytotaxa 318: 1-88.
• Leme EMC, Ribeiro OBC, Souza FVD, Souza EH, Kollmann LJC & Fontana AP (2020) Miscellaneous new species in the “Cryptanthoid complex” (Bromeliaceae: Bromelioideae) from Eastern Brazil. Phytotaxa 430: 157-202.
• Maciel JR (2020) Cryptanthus in Flora do Brasil 2020 (continuously updated). Jardim Botânico do Rio de Janeiro. Available at <http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB5991>. Access on 6 May 2021.
  » http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB5991
• Martinelli G & Moraes MA (2013) Livro vermelho da flora do Brasil. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro - RJ. Andrea Jakobsson Studio Editorial. 1100p.
• Scharf U & Gouda EJ (2008) Bringing Bromeliaceae back to homeland botany. Journal of the Bromeliad Society 58: 123-129.
• Schulte K, Barfuss MHJ & Zizka G (2009) Phylogeny of Bromelioideae (Bromeliaceae) inferred from nuclear and plastid DNA loci reveals the evolution of the tank habit within the subfamily. Molecular Phylogenetics and Evolution 51: 327-339.
• Silvestro D, Zizka G & Schulte K (2014) Disentangling the effects of key innovations on the diversification of Bromelioideae (Bromeliaceae). Evolution 68: 163-175.
• Siqueira Filho JA & Machado ICM (2008) Flowering phenology and pollination ecology of Cryptanthus dianae Leme: a case of floral fragrance-collecting by Euglossinae bees in Bromeliaceae. Selbyana 29: 226-232.
• Smith LB & Downs RJ (1979) Bromeliaceae (Bromelioideae). Flora Neotropica Monograph. 14: 1493-2142.
• Thiers B (continuously updated) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at <http://sweetgum.nybg.org/science/ih/>. Access on September 2020.
  » http://sweetgum.nybg.org/science/ih/
• Velloso AL, Sampaio EVSB & Pareyn FGC (2002) Ecorregiões propostas para o Bioma Caatinga. Instituto de Conservação Ambiental The Nature Conservancy do Brasil. Associação Plantas do Nordeste, Recife. 76p.

• The authors thank G.A.R. da Silva, for help in field works; A.C.R. Andrade-Silva, for help with the species identification of the collected bees; G. Surlo, for botanical illustration; and CNPq, for the scholarship granted to the first author during the period of preparation of this study.

Edited by

Area Editor:

Dr. Luiz Menini Neto

Data availability

Data citations

Gouda EJ, Butcher D & Gouda CS (continuously updated) Encyclopaedia of Bromeliads, Version 4. University Botanic Gardens, Utrecht. Available at <http://bromeliad.nl/encyclopedia/>. Access on 9 September 2020.

Publication Dates

• Publication in this collection
  04 Nov 2022
• Date of issue
  2022

History

• Received
  13 Nov 2020
• Accepted
  06 Sept 2021