Floristic study of the Bromeliaceae in Lençóis Maranhenses National Park, MA, Brazil

Estudo taxonômico da família Bromeliaceae no Parque Nacional dos Lençóis Maranhenses, MA, Brasil

ABSTRACT

(Taxonomic study of the Bromeliaceae in Lençóis Maranhenses National Park, MA, Brazil). The Lençóis Maranhenses National Park (PNLM) is located in the eastern region of the coast of the state of Maranhão, Northeastern Brazil, through the municipalities of Barreirinhas, Santo Amaro, and Primeira Cruz. It has an area of 155,000 hectares, with gently undulating relief and altitudes of less than 100 m. The vegetation is composed of a mosaic involving Mangrove, Cerrado and Restinga. Part of the Park is covered by a vast area of sand dunes, which form huge pools during the rainy season. Fieldwork was carried out in the municipalities of Barreirinhas and Santa Amaro. The testimonial material is deposited in the Maranhão Continental Herbarium (BMA). Four species in three genera were found: Aechmea (1 sp.), Ananas (1 sp.) and Bromelia (2 spp.). Identification key, descriptions, photographs, and ecological, taxonomic and geographic distribution comments are presented for each species located in the Park.

Keywords:
distribuição geográfica; flora do Maranhão; florística; Poales; taxonomia

RESUMO

(Estudo taxonômico da família Bromeliaceae no Parque Nacional dos Lençóis Maranhenses, MA, Brasil). O Parque Nacional dos Lençóis Maranhenses (PNLM) localiza-se na região oriental do litoral do Estado do Maranhão, Nordeste do Brasil, pelos municípios de Barreirinhas, Santo Amaro e Primeira Cruz. Possui uma área de 155.000 hectares, com relevo suavemente ondulado e altitudes inferiores a 100 m. A vegetação é composta por um mosaico envolvendo Mangue, Cerrado e Restinga. Parte do Parque é coberto por uma vasta área de dunas de areia, que formam imensas piscinas no período chuvoso do ano. Os trabalhos de campo foram feitos nos municípios de Barreirinhas e Santa Amaro. O material testemunho encontra-se depositado no herbário Maranhão Continental (BMA). Foram encontradas quatro espécies distribuídas por três gêneros: Aechmea (1 sp.), Ananas (1 sp.) e Bromelia (2 spp.). São apresentadas chave de identificação, descrições, fotográfias e comentários ecológicos, taxonômicos e de distribuição geográfica para cada espécie localizada no Parque.

Palavras-chave:
Flora of Maranhão; floristics; geographical distribution; Poales; taxonomy

Introduction

Floristic surveys are important because they make possible the advance of knowledge in the most diverse areas of Botany, and taxonomic identity is essential for the development and credibility of any research that depends on it: environmental restoration of degraded areas, providing data on the diversity of plant species and endemism and used to indicate priority regions for conservation in which the respective floras are still poorly documented (Silva et al. 2001).

Maranhão State has a privileged diversity of vegetation formations, as it is located in a transition area between the Amazon Rainforest to the West, the Caatinga to the East, and the Cerrado that extends from the northeast to the South of the state (IBGE 2004). Thus, diverse physiognomies can be found in the state (e.g. cerradão, semidecidual seasonal forest, decidual seasonal forest, ombrophilous forest, floodable grasslands, mangroves and restingas). Due to the great variety of vegetations a high plant richness is expected. However, only 3347 species of Angiosperms have been recorded for this state (Flora and Funga do Brasil cont. updated), a figure considered low due to the size of the state and the variety of vegetational formations. These numbers show that despite the efforts of researchers to inventory the flora of Maranhão, the diversity of plant species is underestimated.

Bromeliaceae Juss., with about 3,742 species grouped in 82 genera (Gouda et al. cont.updated), constitute a group of organisms whose presence in the ecosystem results in greater inclusion effect of new species (Oliveira & Rocha 1997, Benzing 2000). This effect is the result of a complex of characteristics that make bromeliads particularly important for maintaining the biological diversity of the system, ensuring their use by numerous animals as shelter, food source and refuge (Rocha et al. 1997, Mestre et al. 2001).

In Brazil there are 54 genera and 1,389 species of Bromeliaceae (Flora and Funga of Brazil cont. updated), with 1,189 endemic species, distributed throughout all phytogeographic domains. For Maranhão, according to the same Flora and Funga of Brazil (2023), there are 25 species distributed among eight genera. In 2018 (Guarçoni et al. 2018), new records were found for the state: Tillandsia kegeliana, T. loliacea, T. paraensis, T. parvispica, T. recurvata and T. tenuifolia.

Despite their importance in maintaining ecosystems, in general, the Bromeliaceae occurring in the state of Maranhão are unknown and very little studied, or even documented in collections. For the Bromeliaceae family, there are no studies involving floristics in specific areas, revision of the genera that occur in the state, or even studies of the associated fauna. The absence of this information suggests a lack of sampling effort that translates to the entire family.

Thus, this work aims to conduct a taxonomic study of the Bromeliaceae family in PNLM, expanding the knowledge of the family in the State of Maranhão, locating new species, new occurrences or endangered species, also providing ecological data on the species. This information is essential for the proper management and implementation of ecological restoration actions in degraded areas. It is also urgent to support strategies to establish effective measures to protect the remaining natural areas.

Material and methods

Study area - The Lençóis Maranhenses National Park (PNLM) was created on June 2, 1981 and is located in the eastern coastal region of Maranhão State (IBAMA 2002). It has an area of 155,000ha, between coordinates 02º19’S to 02º45’S and 42º44’W to 43º29’W, covering the municipalities of Barreirinhas (44.86%), Santo Amaro (42.15%) and Primeira Cruz (6.89%) (figure 1 a).

Figure 1
Lençóis Maranhenses State Park, MA State, Brazil. a. Study area detaching its boundaries (green) and the buffer zone (yellow) (Source: Maranhão State Road Map DER-MA). b. Partial view of one of the lagoons that form inside the dunes and propitiate the appearance of vegetation when they dry out. c. Region of Rio Negro, the river that cuts through the park. d. Canto do Atins: region of estuarine vegetation. e. Lagoa Bonita region: subarbustive sandbank. (Photos: a. DER-MA; b, c, d and e: Elidio Guarçoni).

The Park has a gently undulating relief of less than 100m, where extensive dune fields and restinga vegetation can be found (IBAMA 2002). The climate, according to the Köppen (1931) classification is of the equatorial zone type, with six dry months and six rainy months. The average annual temperature is relatively high, reaching about 28.5 ºC with an average thermal amplitude of 1.1 ºC, without significant oscillations. The rainfall varies from 1473 mm to 1623 mm of annual precipitation, with March and April as the rainiest months.

The Park protects different types of vegetation: Mangrove, Cerrado, Restinga and has part of its extension covered by a vast area of sand dunes (figure 1 b, c, d, e).

Collection and treatment of botanical material - The collection of botanical material took place in five expeditions between the months of March 2018 and February 2019, for a period of six field days for each excursion. Collections were conducted along existing roads and trails, in addition to random walks. The collections of botanical material followed in compliance with ICMBIO License Number 47854-4.

The collected material was pressed in the field, where general notes on the species were made, and dried in the greenhouse of the Maranhão Continental Herbarium (BMA), where mounting and inclusion of unicates were done according to the usual techniques (Mori et al. 1985).

The identification of subfamilies, genera and species was based on comparative morphology, using as basic bibliography Smith & Downs (1974, 1977 and 1979) as well as recent bibliographies revising genera in the family. Classification adopted for subfamilies is based on Givinish et al. (2011); genera and species are based on Gouda et al. 2018 (cont. updated). Morphological terminology for descriptions was based on the works of Radford et al. (1974) and Brown & Gilmartin (1984, 1988, 1989). Keys and descriptions were prepared based on the morphological characteristics of the collected material. The geographical distribution was based on the Flora e Funga do Brasil website (cont. updated); for the PNLM, exsiccates from the collections deposited in the BMA, MAR and SLUI herbaria were consulted.

Results

The PNLM contains four species distributed among three genera: Ananas ananassoides, Aechmea bromeliifolia, Bromelia araujoi and Bromelia grandiflora. All species were found in the shrub or subshrub vegetation of the restinga.

Identification key to the species of Bromeliaceae from PNLM

• 1. Inflorescence emerging from leaf rosette with peduncle evident

  • 2. Flowers with fused ovaries; inflorescense compound ......................... 2. Ananas ananassoides

  • 2. Flowers with free ovary; Inflorescense simple ...... ........................................ 1. Aechmea bromeliifolia

• 1. Inflorescence included in the leaf rosette.

  • 3. Herb faint, 13.6-14.3 cm tall. . ........................... .............................................. 3. Bromelia araujoi

  • 3. Herb robust, 2-3 m alt. . ..................................... ........................................ 4. Bromelia grandiflora

1. Aechmea bromeliifolia (Rudge) Baker in Bentham & Hooker filius, Gen. P1. 3: 664. 1883.

Figure 2 a-b

Figure 2
a-b. Aechmea bromeliifolia. a. Habit. b. Detail of inflorescence. c. Ananas ananassoides var. nanus - detail of the inflorescence. d-f. Bromelia araujoi. d. Clump in half shade under a subshrub. e. Rosette with dried inflorescence. f. Clump in bloom (Photos: Elidio Guarçoni).

Herb epiphytic, ca. 82.6 cm tall in flower. Leaves ca. 15, coreaceus, suberect-arcuate (basal leaves) and erects (upper leaves), forming an infundibuliform rosette; sheaths 20.4-22 × 6.2-10.6 cm, oblong to elliptical, lower half cream with upper half green in both faces with a purplish macula on the adaxial faces, densely cinereous-lepidote in both faces, intire; blade 27.1-28 × 7.3-7.6 cm, narrowly oblong to lanceolate, lower half caniculate, green, densely cinereous-lepidote, obscuring the leaf color, apex cuspate, curved, margin aculeate, aculeous 4.4-5.1 mm long, dark brown, reflexed, 6-7 mm apart. Peduncle erect, conspicuous, ca. 64.3 cm long., vinaceous with white-lanuginous lower third, internodes ca. 4.5 cm long; bracts peduncle erect, larger than the internodes, 5.5-5.8 × 1.5-1.9 cm, ovate, rosaceous, white-lepidote on the adaxial surface, margin entire, apex rostrate. Fertile part of inflorescence strobilaceae, 7.7-8.1 cm long; white-lanuginous. Floral bract broadly ovate, 7-8.3 × 13-17 mm long, half ovary, apex emarginate, ecarinate, margin entire. Flowers sessile, tubuliform, ca. 2.2 cm long; sepals 9-9.4 × 4.3-4.5 mm, ovate, asymmetrical, very light purple, apex apiculate, inconspicuously with sparse fimbriate trichomes, margin entire; petal 5-5.6 × 1.2-1.8 cm, obtrate, yellow, glabrous, free, apex acute, cuculate, margin entire, a pair of appendages in the lower third, ovate, 1.1 mm long, margin crenate, apex acute; stamens included, 1.1 cm long, adnate to the petals ca. 4.5 mm from the base, included in the petals in pairs; fillets white, terete, with a wing along their entire length, ca. 0.9 mm long, free; anthers oblong to slightly lanceolate, ca. 0.3 mm long, yellow, dorsifixed, acute apex, with a spur gynoecium at the same height as the stamens; stigma included, ca. 0.9 mm long, simple-spiraled, white; ovary inferior; stipe terete, ca. 0.7 mm long, white. Fruits not observed.

Examined material: BRAZIL. Maranhão. Barreirinhas, Mata do Atoleiro, around the PARNA dos Lençóis Maranhenses, 3-III-2018, (fl.), E. Guarçoni 2669 (BMA).

Aechmea bromeliifolia occurs in Argentina, Belize, Colombia, Guatemala, Guyana, French Guyana, Honduras, Paraguay, Peru, Suriname, Trinidad and Venezuela (Gouda et al. 2023 cont. updated). In the Brazil occors in practically all states, in the Phytogeographic Domains of the Amazônia, Caatinga, Cerrado and Mata Atlântica (Flora e Funga do Brasil 2023 continuously updated).

This species belongs to Aechmea subg. Macrochordion for presenting simple and strobilaceous inflorescence, with polystate and sessile flowers, carinate and floral bracts entire, with sepals densely covered by trichomes (Faria et al. 2010). It can be easily recognized by presenting rosette-tank with terminal strobilaceous inflorescence with flowers of sepals asymmetricals and yellow corolla. So far, A. bromeliifolia has been recorded around PNLM, in the Mata do Atoleiro, a shrubby restinga area, as an epiphyte. The species has also been observed in the region of Espigão, in Santo Amaro, within the limits of the park, as an epiphyte.

2. Ananas ananassoides (Baker) L.B.Sm. var. nanus

L. B. Smith, Bromel. Soc. Bull. 12: 54. 1962

Figure 2 c

Herb terrestrial, ca. 67 cm tall when flowering. Leaves ca. 18, coriaceous, suberect-arcuate (basal leaves) and suberect to erects (upper leaves); blade 80.6 × 5.6 cm, linear, caniculate, green, white-lepidote on both sides, with scales between the veins, not obscuring the leaf color, apex acute, sharp margin, 1.9 mm long, light brown, antrorose, varying the distance between them. Inflorescence 38.6 cm long, smaller than leaves; Peduncle erect, conspicuous, ca. 33.8 cm long, ca. 8 mm diam, green, densely white-furaceous, internodes decreasing in length towards the top; peduncle bracts foliaceous, erect, upper much smaller than lower, 12.4 × 0.4 cm, green with reddish spots on the underside, similar to the leaves; fertile part of the inflorescence strobilaceous, ovoid, ca. 4.4 cm long, ending in a small coma; floral bract 1.4 × 0.8 cm long, broadly triangular, erect, covering the ovary, smaller or the same size as the petals, ecarinate, leaving them exposed, green to light green, densely white-lepidote on the abaxial side, glabrous on the adaxial side, acute apex, aculeate margin, irregular nuclei. Flowers sessile, tubular, 1.9 cm long, anthesis in succession; sepals ca. 6.5 × 5.3 mm, triangular to slightly elliptic, asymmetrical, green, white-lepidot, fleshy, conate 1.8 mm long at the base, straight apex, entire margin; petal 1.8 × 0.4 cm, contorted post-anthesis, spatulate, pearly blue, glabrous, free, apex obtuse, margin entire, a pair of appendages in the lower third of the crenate margin, 2.3 mm long; Stamens included, 1.5 cm long, a series adnates the petals indistinctly; fillets aims, complanate, ca. 1,1 cm long, free; anthers oblong, ca. 3.5 mm long, yellow, dorsifixed, apex obtuse; gynogenes above the stamens and included; stigma included, 1.9 mm long, trephidic, white; style terete, 1.2 cm long, white. Ovary inferior. Fruits not observed.

Examined material: BRAZIL. Maranhão. Santo Amaro, Espigão, 6-VII-2018, (fl.), E. Guarçoni 2663 (BMA).

Ananas ananassoides var. nanus occurs in Surinam and Brazil (Gouda et al. 2023 cont. updated). In Brazil it occurs in the states of AC, AL, AM, AP, BA, CE, ES, DF, GO, MA, MG, MS, MT, PA, PB, PE, PI, PN, RJ, RO, RR, SC, SP and TO, in the Phytogeographic Domains of Amazonia, Caatinga and Cerrado (Flora e Funga 2023 continuously updated). The variety has been considered a valid species (Smith & Downs 1979). However, it was synonymized by Coppens d’Eeckenbrugge and Leal (2003) to A. comosus and then recognized as a synonym of A. ananassoides by Butcher & Gouda (2014). It can be easily recognized by having small inflorescence size compared to the genus. A. ananassoides var. nanus was collected as terrestrial in a subarbustive restinga in the region of Espigão, in the municipality of Santo Amaro.

3. Bromelia araujoi P.J.Braun, Esteves & Scharf, Bromelie 2008(2): 88-95. (2008).

Figure 2 d, e, f

Herb terrestrial, 13.6-14.3 cm tall when flowering. Leaves ca. 10, suberect to suberect-recurved; sheath 2.8-3.9 × 1.8-5.1 cm, ovate, white to cream, sericeous on upper abaxial side or both sides, with rusty trichomes, lepidot white when not sericeous on adaxial side, upper half of margin aculeate, aculeles 0.9-1.1 mm long, light brown; blade 50.7-88.5 × 1-1.5 cm, linear, caniculate, green to green-brown, white-lepidot to sparsely white-lepidot above upper third of adaxial side, margin aculeate, aculeles brown, 1.2-7 mm long, apex acute. Peduncle erect, inconspicuous, 1.4-2.7 cm long, 5.9-9.3 mm dia, aim, flocculate; peduncle bracts: sheath 3.7-4.4 × 1-1.5 cm, cream with straw upper half, obovate, glabrous, often sparsely white-lepidot on upper third of adaxial face, margin aculeate, acutely 1-2.2 mm long; blade 5.3-16.3 × 0.4-0.9 cm, linear, rosaceous, white-lepidot, margin aculeate, acutely inconspicuous, apex long-attenuated. Floral bract 2.3-2.9 × 0.2-0.3 cm, oblanceolate, asymmetrical, straw, carinate, laxly rusty-flocculate in the lower half, margin conspicuously aculeate at the apex, aculeules 0.7-1 mm long, apex cleft, cuculate. Flowers pedicelate; pedicels 1.6-2.4 cm long, target to cream, rusty-flocculate; sepals 1.6-1.8 × 0.4-0.3 cm, narrowly elliptic, asymmetrical, white with brown upper half, carinate, one sepal free and two conate, conation ca. 9 mm long, lepidot to rusty-flocose at base, margin entire, apex acute, one sepal cuculate; petal 2.2-2.8 × 0.3-0.5 cm, linear, blue, glabrous, attached to stamen tube by 1-1.6 cm long, apex emarginate-recurved; stamens exerted by a fraction of the anther, 1.6-2.5 cm long; fillets white, monadelfous, tube 1-1.6 cm long; anthers 7.1-8.6 mm long, sagitate, linear, white, dorsifixed, acute, with spur at apex; stigma included, 2.6-2.8 mm long, simple-erect, target; style 1.2-1.9 cm long, target; hypanthium 1.5-2.4 cm long, 3.3 mm diam. Fruits not observed.

Examined material: BRAZIL. Maranhão: Barreirinhas, parte baixa antes da lagoa Bonita, 5-III-2018, (fl.), E.H. Silva s.n. (BMA 1927).

Additional material examined: BRAZIL. Maranhão: Primeira Cruz, entre Caeté e São Bento, 20-VI-1970, Andrade-Lima 705916 (IPA).

Bromelia araujoi is endemic to the state of Maranhão, Brazil (Gouda et al. 2023 continuously updated), occurring in the phytogeographic domain Cerrado (Flora e Funga 2023 continuously updated). The species is poorly known, and is characterized by its small size, inflorescence included in the leaf rosette, and blue flowers (figure 2f). Bromelia araujoi is a common species in the subshrub restinga of PNLM, usually near the shade formed by subshrubs.

4. Bromelia grandiflora Mez, Repert. Spec. Nov. Regni Veg. 16: 3. 1919.

Figure 3 a-b

Figure 3
Bromelia grandiflora. a. Habit; b. Detail of the inflorescence (Photo: Elidio Guarçoni).

Herb robust, terrestrial, ca. 2-3 m tall. Leaves > 20, erect to patent, recurved in upper third; sheath brown, villous or serice on both faces, rusty trichomes, aculeate margin, acutely 4 mm long on top; blade 228-152 × 4.7-4.5 cm, linear triangular, green, with rosaceous base, lepidote on both faces, aculeate margin, acutely 5.1-5.4 mm long, apex attenuate-mucronate. Peduncle erect, ca. 2.5 cm diam., target, villous; peduncle bracts similar to leaves: sheath 4.3-7.3 × 6-6.2 cm, oval, brown, aculeate margin, aculeate 7.8-7.9 mm long; blade 64-85.8 × 2.5-2.7 cm, linear-triangular, rosaceous, lepidote, aculeate margin, aculeate 4.6-5 mm long, attenuate apex. Inflorescence capitulum, 11.3 cm long, 29.6 cm diam. Primary bract not observed. Floral bract 7-8.3 × 1.2-1.5 cm, oval, cream, carinate, lepidot, villous at apex on abaxial side, margin aculeate on the third, aculeulus ca. 1 mm long, apex acute. Flowers 7.5-94 cm long., pedicelate; pedicel 1.7-1.8 cm long; sepals 2.6-2.7 × 0.5-03 cm, linear-lanceolate, entire margin, rusty trichomes, acute apex; petals 3.5-4.1 × 04-03 cm, narrowly oblong, magenta apex, alba, glabrous, united to the stamen tube, rounded apex, cuculate, stamens included, 3.1 -3.4 cm long. , fillets monadelfous, tube 2.8-3.1 cm; anthers sagitate, white, dorsifixed; stigma included 2.3-2.6 mm long, non-spiral, target; stipe 2.1-2.7 cm long, target; hypanthium 1.6-2.0 cm long, oval, target, woolly. Fruit not observed; seeds not observed.

Examined material: BRAZIL. Maranhão: Barreirinhas, estrada de areia em direção a Lagoa Bonita, 22-III-2015, E. Guarçoni 2328 (BMA).

Bromelia grandiflora is endemic to Brazil (Gouda et al. 2019 continuously updated), occurring in the states of: Alagoas, Bahia, Ceará, Distrito Federal, Goiás, Maranhão, Mato Grosso, Minas Gerais, Paraíba, Pernambuco, Piauí, Rio Grande do Norte, SergipeTocantins and Pará, in the phytogeographic domains of Amazonia and Cerrado (Flora e Funga 2023 continuously updated). According to Monteiro (2023), the species has long been confused with B. karatas, which does not occur in Brazil.

Bromelia grandiflora can be confused with B. magnifica, but differs from it mainly by having magenta or purplish petals (vs. purple) and brown (vs. cream) indumentum

Bromelia grandiflora is a common species in the region of the Lagoa Bonita circuit, mainly in the shrubby resting, within the Cerrado phytogeographic domain.

Conclusão

Bromeliaceae presents four species for PNLM. The low number of Bromeliaceae species may be related to edaphic factors that also influence the low number of species for the restinga regions of Pará, Piaui and Rio Grande do Norte. In addition, probably the PNLM is a naturally isolated area, which hinders the migration of new species given the characteristics of the region.

Acknowledgments

The authors thank FAPEMA for funding the project (UNIVERSAL-00855/17). The authors also thank SISBIO, especially the head office of PNLM for all logistical support during the execution of this project. We would like to thank the Dra. Raquel Monteiro for her help in identifying Bromelia grandiflora.

Literature cited

• Benzing, D. 2000. Bromeliaceae: profile of an adaptive radiation. Cambridge University Press, UK.
• Brown, G.K., Gilmartin, A.J. 1984. Stigma structure and variation in Bromeliaceae-neglected taxonomic characters. Brittonia 36: 364-374.
• Brown, G.K., Gilmartin, A.J. 1988. Comparative ontogeny of bromeliaceous stigmas. In: P. Leins, S.C. Tucker & P.K. Endress (eds.). Aspects of floral development. Berlim, Stuttgart, pp. 191-204.
• Brown, G.K., Gilmartin, A.J. 1989. Stigma types in Bromeliaceae. Systematic Botanic 14: 110-132.
• Butcher, D., Gouda, E. 2014. Most Ananas are Cultivars. Newsletter of the Pineapple Working Group, International Society for Horticultural Science. Pineapple News 21: 9-11.
• Faria, A.P.G., Wendt, T. & Brown, G.K. 2010. A revision of Aechmea subgenus Macrochordion (Bromeliaceae) based on phenetic analyses of morphological variation. Botanical Journal of the Linnean Society 162: 1-27.
• Flora e Funga do Brasil. 2023. Jardim Botânico do Rio de Janeiro. Available in http://floradobrasil.jbrj.gov.br/ (access in 6-IV-2023).
  » http://floradobrasil.jbrj.gov.br/
• Givnish, T.J., Barfuss, M.H.J., Ee Van, B., Riina, R., Schulte, K., Horres, R., Gonsiska, P.A., Jabaily, R.S., Crayn, D.M., Smith, J.A.C., Winter, K., Brown, G.K., Evans, T.M., Holst, B.K., Luther, H., Till, W., Zizka, G., Berry, P.E. & Sytsma, K.J. 2011. Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: insights from an eight-locus plastid phylogeny. American Journal of Botanic 98: 872-895.
• Gouda, E.J., Butcher, D. & Dijkgraaf, L. 2023. Encyclopaedia of Bromeliads, Version 5. Utrecht University Botanic Gardens. Available in http://bromeliad.nl/encyclopedia/ (access in 6-IV-2023).
  » http://bromeliad.nl/encyclopedia/
• Guarçoni, E.A.E., Costa. A.F., Silva, E.O, Ferreira, A.W.C. & Oliveira, M.S. 2018. New records of Tillandsia L. (Bromeliaceae, Tillandsioideae) for Maranhão State, Brazil. Check List 14: 951-959.
• IBAMA/MMA. 2002. Plano de Manejo do Parque Nacional dos Lençóis Maranhenses. Brasília, DF.
• IBGE. 2004. Mapa de Biomas do Brasil; primeira aproximação. Rio de Janeiro: IBGE.
• KÖPPEN, W. 1931. Grundrissder Klimakunde: Outline of climate science. Berlin: Walter de Gruyter.
• Mestre, L.A.M., Aranha, J.M.R. & Esper, M.L.P. 2001. Macroinvertebrate fauna associated to the bromeliad Vriesea inflata of the Atlantic Forest (Paraná State, Southern Brazil). Brazilian Archives of Biology and Technology 44: 89-94.
• Mori, S.A., Silva, L.A.M., Lisboa, G. & Coradin, L. 1985. Manual de manejo do herbário fanerogâmico. Ilhéus. BA. CEPLAC.
• Oliveira, M.G.N. & Rocha, C.F.D. 1997. O efeito da complexidade da bromélia-tanque Neoregelia cruenta (R. Graham) L. B. Smith sobre a comunidade animal associada. Bromélia 4: 13-21.
• Radford, A.E., Dickison, W.C., Massey, J.R. & Bell, C.R. 1974. Vascular plant systematics. New York, Harper and Row.
• Rocha, C.F.D., Gocliatti-Carvalho, L., Almeida, D.R. & Freitas, A.F.N. 1997. Bromélias: ampliadoras da biodiversidade. Bromélia 4: 7-10.
• Silva, N.M.F., Carvalho L.A.F. & Baumgratz, J.F.A. 2001. O Herbário do Jardim Botânico do Rio de Janeiro - um expoente na história da flora brasileira. Instituto de Pesquisa Jardim Botânico do Rio de Janeiro, Rio de Janeiro.
• Smith, L.B. & Downs, R.J. 1974. Bromeliaceae, subfamily Pitcairnioideae. Flora Neotropica 14: 1-654.
• Smith, L.B. & Downs, R.J. 1977. Bromeliaceae, subfamily Tillandsioideae. Flora Neotropica 14: 659-1492.
• Smith, L.B. & Downs, R.J. 1979. Bromeliaceae, subfamily Bromelioideae. Flora Neotropica 14: 1493-2142.

Edited by

• Associate Editor:
  José Iranildo Miranda de Melo

Publication Dates

• Publication in this collection
  26 May 2025
• Date of issue
  2025

History

• Received
  27 Apr 2023
• Accepted
  02 Aug 2024