Acessibilidade / Reportar erro
SHORT COMMUNICATION, Conservation of Nature • Floresta Ambient. 30 (1) • 2023 • https://doi.org/10.1590/2179-8087-FLORAM-2022-0080   copy

Vascular Epiphyte Diversity in a Key Atlantic Forest Remnant from Minas Gerais State, Southeastern Brazil

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Vascular epiphytes contribute significantly to the biodiversity of tropical forests. We aimed to identify the epiphyte species occurring in the Muriqui Trail at Serra do Brigadeiro State Park (SBSP), a priority area for Atlantic forest conservation in southeastern Brazil. We selected 10 phorophytes, from which we sampled epiphytes and took light intensity measurements at three strata: up to 4 m, 4 to 8 m, and above 8 m. Phorophytes represented eight species, eight genera, and six families. We found 25 epiphytic species from 17 genera and nine families. Ferns showed highest richness, especially Polypodiaceae. We report herein important data on epiphyte diversity in eastern Minas Gerais state (Zona da Mata), including the occurrence of species rarely cited in surveys. Fomenting local conservation along with environmental education may be pivotal for counteracting anthropic pressure on SBSP.

Keywords:
Epiphyte ecology; eudicots; ferns; magnoliids; monocots

The Atlantic forest is one of the main tropical forests in the world, accounting for a large portion of all animal and plant diversity on the planet. Thereby, it is one of the priority areas for fauna and flora conservation in Brazil (Marchese, 2015Marchese C. Biodiversity hotspots: A shortcut for a more complicated concept. Global Ecology and Conservation 2015; 3:297-309.). Much of the forest has been continuously removed, and currently only few remnants exist in the country (Fundação SOS Mata Atlântica & Instituto Nacional de Pesquisas Espaciais, 2020Fundação SOS Mata Atlântica, Instituto Nacional de Pesquisas Espaciais. Atlas dos remanescentes florestais da Mata Atlântica - período 2018-2019. Relatório Técnico. São Paulo: Fundação SOS Mata Atlântica & INPE; 2020.).

Epiphytes are a major component of the biodiversity of tropical forests, as they play a pivotal role in nutrient dynamics in those ecosystems (Coxson & Nadkarni, 1995Coxson DS, Nadkarni NM. Ecological roles of epiphytes in nutrient cycles of Forest Ecosystems. In: Lowman MD, Nadkarni NM., editors. Forest canopies. New York: Academic Press; 1995.; Taylor et al., 2022Taylor A, Zotz G, Weigelt P, Cai L, Karger DN, König C, et al. Vascular epiphytes contribute disproportionately to global centres of plant diversity. Global Ecology and Biogeography 2022; 31(1):62-74.; Marcusso et al., 2022Marcusso GM, Kamimura VA, Borgiani, Menini Neto L, Lombardi JA. Phytogeographic meta-analysis of the vascular epiphytes in the neotropical region. The Botanical Review 2022; 88(3):388-412.). They are irregularly distributed along phorophytes, showing a vertical variation in terms of species richness, number of individuals and leaf functional traits (Petter et al., 2016Petter G, Wagner K, Wanek W, Delgado EJS, Zotz G, Cabral JS, et al. Functional leaf traits of vascular epiphytes: vertical trends within the forest, intra- and interspecific trait variability, and taxonomic signals. Functional Ecology 2016; 30(2):188-198.; Francisco et al., 2019Francisco TM, Couto DR, Garbin ML, Muylaert RL, Ruiz‐Miranda CR. Low modularity and specialization in a commensalistic epiphyte-phorophyte network in a tropical cloud forest. Biotropica 2019; 51(4):509-518.; Mitchell et al., 2021Mitchell RJ, Hewison RL, Beaton J, Douglass JR. Identifying substitute host tree species for epiphytes: The relative importance of tree size and species, bark and site characteristics. Applied Vegetation Science 2021; 24(2):e12569.; Dias-Pereira et al., 2022Dias-Pereira J, Andrade GC, Silva LC, Ferrari FB, Ribas RF, Menini Neto L, et al. Leaf structural adaptations in vascular epiphytes from the Atlantic rainforest along phorophyte vertical stratification. Flora 2022; 288:1-18.). Among the different ecosystems within the Atlantic forest domain, rainforests alone host approximately 60% of all vascular epiphytes (Ramos et al., 2019Ramos FN, Mortara SR, Monalisa-Francisco N, Elias JPC, Menini Neto L, Freitas L, et al. Atlantic epiphytes: A data set of vascular and non-vascular epiphyte plants and lichens from the Atlantic Forest. Ecology 2019; 100(2):e02541.).

We aimed to identify the epiphyte species occurring on phorophytes in a major fragment of secondary montane forest from southeastern Brazil. Sampling was performed at Serra do Brigadeiro State Park, located at the Mantiqueira Mountain Range, in eastern Minas Gerais, within the Atlantic Forest phytogeographic domain. The study area is known as Muriqui trail, an interpretative trail which is frequently visited by several students from nearby institutions, as well as by residents of the local community and tourists visiting the region. The trail is located in the park central portion, ca. 200 m away from the head office, at a mean altitude of 1260 m (20º 43’ 12” S and 42º 28’ 47” W) (Figure 1).

Figure 1
Map of the study area, the Muriqui trail at Serra do Brigadeiro State Park, in Araponga municipality, Minas Gerais state (MG), southeastern Brazil. Elaborated by Ricardo S. Ramos. (Adapted with permission from Dias-Pereira et al., 2022Dias-Pereira J, Andrade GC, Silva LC, Ferrari FB, Ribas RF, Menini Neto L, et al. Leaf structural adaptations in vascular epiphytes from the Atlantic rainforest along phorophyte vertical stratification. Flora 2022; 288:1-18.).

To sample phorophytes, we chose those that best represent the study trail in terms of number of epiphytic species occurring along vertical stratification, and that also fall into the criteria of having a minimum 10 m in height and a minimum 50 cm of circumference at breast height (CBH), which rendered a total of ten sampled phorophytes. We measured total height, CBH, bole length, and canopy depth (total phorophyte height minus bole length). Phorophytes were divided in three strata: up to 4 m, 4 to 8 m, and above 8 m. All fertile vascular epiphyte species occurring on the selected phorophytes were collected, including true, accidental and facultative epiphytes as well as hemiepiphytes, following the classification by Benzing (1990Benzing DH. Vascular epiphytes. New York: Cambridge University Press; 1990.). Fertile plant material was collected on a bimonthly-basis from August 2007 through August 2008. Collections were performed by tree climbing, from soil to canopy. Vouchers of epiphyte and phorophyte species were deposited in the VIC Herbarium (acronym following Thiers, 2022Thiers B. (continuous updated). Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. [cited 2022 Jul. 8]. Available from: Available from: http://sweetgum.nybg.org/ih/ .
http://sweetgum.nybg.org/ih/... , continuously updated) and were identified by consulting specialists and by comparing vouchers against specimens in the VIC Herbarium collection. We used a quantum/radiometer/photometer (model LI-185B, LI-COR Biosciences, Lincoln, USA) to determine light intensity (µmol photons m-2 s-1) along phorophyte vertical stratification (Figure 2), following the procedure and sampling scheme described in Dias-Pereira et al. (2022Dias-Pereira J, Andrade GC, Silva LC, Ferrari FB, Ribas RF, Menini Neto L, et al. Leaf structural adaptations in vascular epiphytes from the Atlantic rainforest along phorophyte vertical stratification. Flora 2022; 288:1-18.).

Figure 2
Light intensity at the basal (up to 4 m), median (4 to 8 m) and apical (above 8 m) strata of the studied phorophytes from an Atlantic forest fragment in southeastern Brazil. Bars represent standard error. Phorophyte numbers are as follows: #1 and #3 = Bathysa australis (A.St.-Hil.) K.Schum. (Rubiaceae), #2 = Psychotria sessilis Vell. (Rubiaceae), #4 = Dendropanax cuneatus (DC.) Decne & Planch. (Araliaceae), #5 and #8 = Solanum cinnamomeum Sendtn. (Solanaceae), #6 = Alchornea triplinervia (Spreng.) Müll.Arg. (Euphorbiaceae), #7 = Sorocea bonplandii (Baill.) W.C.Burger, Lanj. & Wess.Boer (Moraceae), #9 = Myrcia neoclusiifolia A.R.Lourenço & E. Lucas (Myrtaceae), and #10 = Ps. vellosiana Benth.

The ten sampled phorophytes were represented by eight species, eight genera and six families (Figure 3). Phorophyte height ranged between 12 and 20 m. Minimum CBH was 53.5 cm while maximum was 179.4 cm. The only multi-trunked phorophyte was Psychotria vellosiana (phorophyte #10). Bole height ranged from 7 to 16 m whereas canopy depth (i.e., phorophyte height minus bole height) ranged from 3 to 6 m (Table 1).

Figure 3
Sampled phorophytes in the Muriqui trail at Serra do Brigadeiro State Park, Araponga municipality (Minas Gerais state, southeastern Brazil). A. Phorophyte #1 = Bathysa australis (A.St.-Hil.) K.Schum. (Rubiaceae). B. Phorophyte #2 = Psychotria sessilis Vell. (Rubiaceae). C. Phorophyte #3 = B. australis. D. Phorophyte #4 = Dendropanax cuneatus (DC.) Decne & Planch. (Araliaceae). E. Phorophyte #5 = Solanum cinnamomeum Sendtn. (Solanaceae). F. Phorophyte #6 = Alchornea triplinervia (Spreng.) Müll.Arg. (Euphorbiaceae). G. Phorophyte #7 = Sorocea bonplandii (Baill.) W.C.Burger, Lanj. & Wess.Boer (Moraceae). H. Phorophyte #8 = Sol. cinnamomeum. I. Phorophyte #9 = Myrcia neoclusiifolia A.R.Lourenço & E. Lucas (Myrtaceae). J. Phorophyte #10 = Ps. vellosiana Benth.

Thumbnail
Table 1
Phorophytes sampled for the study of epiphyte diversity in an Atlantic forest fragment from southeastern Brazil.

In the ten analyzed phorophytes, we found 25 vascular epiphyte species from 17 genera and nine families. Ferns were the preponderant group, with 13 species from eight genera and four families (Table 2). We also found aroids on seven phorophytes, yet we did not consider them in our study since all individuals were unfertile during collection period.

Thumbnail
Table 2
Vascular epiphytes occurring in an Atlantic forest fragment from southeastern Brazil, in the Muriqui Trail at Serra do Brigadeiro State Park (Araponga municipality, Minas Gerais state, southeastern Brazil), with their distribution on the sampled phorophytes and values of light intensity at different phorophyte strata. Phorophyte numbers are as follows: #1 and #3 = Bathysa australis (A.St.-Hil.) K.Schum. (Rubiaceae), #2 = Psychotria sessilis Vell. (Rubiaceae), #4 = Dendropanax cuneatus (DC.) Decne & Planch. (Araliaceae), #5 and #8 = Solanum cinnamomeum Sendtn. (Solanaceae), #6 = Alchornea triplinervia (Spreng.) Müll.Arg. (Euphorbiaceae), #7 = Sorocea bonplandii (Baill.) W.C.Burger, Lanj. & Wess.Boer (Moraceae), #9 = Myrcia neoclusiifolia A.R.Lourenço & E. Lucas (Myrtaceae), and #10 = Ps. vellosiana Benth. (Adapted with permission from Dias-Pereira et al., 2022).

Overall, environmental conditions at the canopy are more xeric than on the soil, yet this does not necessarily occur in all regions of the forest, which itself is a dynamic system (Benzing, 1990Benzing DH. Vascular epiphytes. New York: Cambridge University Press; 1990.). Vertical gradients of microclimatic conditions have been shown to determine a stratified structure of epiphytic communities across different phytophisiognomies of the Atlantic rainforest (Cruz et al., 2022Cruz ACR, Correa NM, Murakami MMS, Amorim TA, Nunes-Freitas AF, Sylvestre LS. Importance of the vertical gradient in the variation of epiphyte community structure in the Brazilian Atlantic Forest. Flora 2022; 295:152137.). In that sense, shade-tolerant species usually thrive on the inferior strata of phorophytes, where light intensity is lower (Nunes-Freitas & Rocha, 2007Nunes-Freitas AF, Rocha CFD. Spatial distribution by Canistropsis microps (E. Morren ex Mez) Leme (Bromeliaceae:Bromelioideae) in the Atlantic rain forest in Ilha Grande, Southeastern Brazil. Brazilian Journal of Biology 2007; 67(3):631-637.). In the forest remnant we studied, we found a clear vertical stratification of light intensity. However, the study area is quite shady compared with more open areas, and the mean values of light intensity we found might well be reflecting solely the diffuse radiation during the study period.

Ferns occurred on all phorophytes, showing higher diversity than magnoliids, monocots and eudicots (Tables 1 and 2). Additionally, in high altitude areas such as the one we studied, ferns are usually more species-rich than other groups, probably due to their higher tolerance to low temperatures (Moran, 1995Moran RC. The importance of mountains to pteridophytes, with emphasis on Neotropical Montane Forests. In: Churchill SP, Balsev H, Forero E, Luteyn JL., editors. Biodiversity and conservation of Neotropical Montane Forests. New York: The New York Botanical Garden; 1995.; Furtado & Menini Neto, 2021Furtado SG, Menini Neto L. What is the role of topographic heterogeneity and climate on the distribution and conservation of vascular epiphytes in the Brazilian Atlantic Forest? Biodiversity and Conservation 2021; 30(5):1415-1431.). In regard to other plant groups, we found eudicots occurring on phorophytes #3 - Bathysa australis and #4 - Dendropanax cuneatus; magnoliids on phorophytes #1 - B. australis, #5 - Solanum cinnamomeum, #9 - Myrcia neoclusiifolia and #10 - Ps. vellosiana; and monocots on all phorophytes, represented by Orchidaceae and Bromeliaceae, especially due to the presence of Vriesea heterostachys on all sampled phorophytes (Tables 1 and 2).

We found two species that are only rarely reported in inventories: the angiosperm Sinningia cooperi and the fern Cochlidium punctatum. Sinningia cooperi occurred solely on phorophyte #4 - D. cuneatus (Tables 1 and 2), yet at all three strata. Sinningia cooperi commonly occurs as an epiphyte, and is considered to be widely distributed across the Mantiqueira Mountain Range (Pereira et al., 2021Pereira LC, Chautems A, Menini Neto L. Biogeography and conservation of Gesneriaceae in the Serra da Mantiqueira, southeastern region of Brazil. Brazilian Journal of Botany 2021; 44(1):239-248.). Cochlidium punctatum, on the other hand, occurred solely on phorophyte #6 - Alchornea triplinervia (Tables 1 and 2). This species occurs in the Atlantic forest from the states of Bahia (northeastern Brazil) to Santa Catarina (south) (Labiak, 2022Labiak PH. Cochlidium in Flora e Funga do Brasil. Jardim Botânico do Rio de Janeiro. [cited 2022 Aug. 10]. Available from: Available from: https://floradobrasil.jbrj.gov.br/FB91596 .
https://floradobrasil.jbrj.gov.br/FB9159... ).

The Muriqui trail at Serra do Brigadeiro State Park hosts high epiphyte diversity, especially of ferns. Epiphytic ferns occurred on all sampled phorophytes, which was not seen with epiphytic eudicots and magnoliids. Reports of rare species in the study site, along with the fact that the trail composes the habitat of the northern muriqui monkey (Brachyteles hypoxanthus), a threatened endemic species from the native fauna, reiterate the need to protect the area. Fomenting local conservation activities along with environmental education may be pivotal for counteracting the anthropic pressure on the park, which is a key conservation unit within the Atlantic forest domain.

REFERENCES

  • Benzing DH. Vascular epiphytes. New York: Cambridge University Press; 1990.
  • Coxson DS, Nadkarni NM. Ecological roles of epiphytes in nutrient cycles of Forest Ecosystems. In: Lowman MD, Nadkarni NM., editors. Forest canopies. New York: Academic Press; 1995.
  • Cruz ACR, Correa NM, Murakami MMS, Amorim TA, Nunes-Freitas AF, Sylvestre LS. Importance of the vertical gradient in the variation of epiphyte community structure in the Brazilian Atlantic Forest. Flora 2022; 295:152137.
  • Dias-Pereira J, Andrade GC, Silva LC, Ferrari FB, Ribas RF, Menini Neto L, et al. Leaf structural adaptations in vascular epiphytes from the Atlantic rainforest along phorophyte vertical stratification. Flora 2022; 288:1-18.
  • Francisco TM, Couto DR, Garbin ML, Muylaert RL, Ruiz‐Miranda CR. Low modularity and specialization in a commensalistic epiphyte-phorophyte network in a tropical cloud forest. Biotropica 2019; 51(4):509-518.
  • Fundação SOS Mata Atlântica, Instituto Nacional de Pesquisas Espaciais. Atlas dos remanescentes florestais da Mata Atlântica - período 2018-2019. Relatório Técnico. São Paulo: Fundação SOS Mata Atlântica & INPE; 2020.
  • Furtado SG, Menini Neto L. What is the role of topographic heterogeneity and climate on the distribution and conservation of vascular epiphytes in the Brazilian Atlantic Forest? Biodiversity and Conservation 2021; 30(5):1415-1431.
  • Labiak PH. Cochlidium in Flora e Funga do Brasil. Jardim Botânico do Rio de Janeiro. [cited 2022 Aug. 10]. Available from: Available from: https://floradobrasil.jbrj.gov.br/FB91596
    » https://floradobrasil.jbrj.gov.br/FB91596
  • Marchese C. Biodiversity hotspots: A shortcut for a more complicated concept. Global Ecology and Conservation 2015; 3:297-309.
  • Marcusso GM, Kamimura VA, Borgiani, Menini Neto L, Lombardi JA. Phytogeographic meta-analysis of the vascular epiphytes in the neotropical region. The Botanical Review 2022; 88(3):388-412.
  • Mitchell RJ, Hewison RL, Beaton J, Douglass JR. Identifying substitute host tree species for epiphytes: The relative importance of tree size and species, bark and site characteristics. Applied Vegetation Science 2021; 24(2):e12569.
  • Moran RC. The importance of mountains to pteridophytes, with emphasis on Neotropical Montane Forests. In: Churchill SP, Balsev H, Forero E, Luteyn JL., editors. Biodiversity and conservation of Neotropical Montane Forests. New York: The New York Botanical Garden; 1995.
  • Nunes-Freitas AF, Rocha CFD. Spatial distribution by Canistropsis microps (E. Morren ex Mez) Leme (Bromeliaceae:Bromelioideae) in the Atlantic rain forest in Ilha Grande, Southeastern Brazil. Brazilian Journal of Biology 2007; 67(3):631-637.
  • Pereira LC, Chautems A, Menini Neto L. Biogeography and conservation of Gesneriaceae in the Serra da Mantiqueira, southeastern region of Brazil. Brazilian Journal of Botany 2021; 44(1):239-248.
  • Petter G, Wagner K, Wanek W, Delgado EJS, Zotz G, Cabral JS, et al. Functional leaf traits of vascular epiphytes: vertical trends within the forest, intra- and interspecific trait variability, and taxonomic signals. Functional Ecology 2016; 30(2):188-198.
  • Ramos FN, Mortara SR, Monalisa-Francisco N, Elias JPC, Menini Neto L, Freitas L, et al. Atlantic epiphytes: A data set of vascular and non-vascular epiphyte plants and lichens from the Atlantic Forest. Ecology 2019; 100(2):e02541.
  • Taylor A, Zotz G, Weigelt P, Cai L, Karger DN, König C, et al. Vascular epiphytes contribute disproportionately to global centres of plant diversity. Global Ecology and Biogeography 2022; 31(1):62-74.
  • Thiers B. (continuous updated). Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. [cited 2022 Jul. 8]. Available from: Available from: http://sweetgum.nybg.org/ih/
    » http://sweetgum.nybg.org/ih/

Edited by

Associate editor:

Bruno Araujo Furtado de Mendonça http://orcid.org/0000-0003-0288-0024

Publication Dates

  • Publication in this collection
    10 Mar 2023
  • Date of issue
    2023

History

  • Received
    07 Nov 2022
  • Accepted
    01 Feb 2023
Creative Common - by 4.0
This is an open-access article distributed under the terms of the Creative Commons Attribution License
Instituto de Florestas da Universidade Federal Rural do Rio de Janeiro Rodovia BR 465 Km 7, CEP 23897-000, Tel.: (21) 2682 0558 | (21) 3787-4033 - Seropédica - RJ - Brazil
E-mail: floram@ufrrj.br
Acompanhe os números deste periódico no seu leitor de RSS