Vascular epiphytes on Pseudobombax (Malvaceae) in rocky outcrops (inselbergs) in Brazilian Atlantic Rainforest: Basis for conservation of a threatened ecosystem

Abstract

This study evaluated the richness of vascular epiphytes on Pseudobombax sp. nov. in three inselbergs in the Atlantic Forest Domain in state of Espírito Santo and evaluated the floristic similarity between the areas. We sampled 111 phorophytes in three regions in the southern of Espírito Santo state and identified 151 species, 77 genera and 21 families of vascular epiphytes, of which the families Orchidaceae and Bromeliaceae showed the highest richness. Non-parametric estimators (Chao 2, Jackknife 1) indicate that 90 and 95% of species richness of epiphytes was recorded. The most diversified ecological category was the characteristic holoepiphytes. The ratio of the number of epiphytes and number of phorophytes sampled in a montane inselberg, in this study, was greater than the richness of vascular epiphytes found in the rocky outcrops of quartzite, and, in general, different types of Atlantic Domain forests, but smaller in richness for some Dense Ombrophilous Forests of southern Brazil. The three inselberg areas had distinct floras. The high richness, the endemism found, and the number of endangered species of epiphytes demonstrate the important role of Pseudobombax sp. nov., because of its architecture and size, in the maintenance of biodiversity on the inselbergs in southeastern Brazil.

Full text

Abstract
This study evaluated the richness of vascular epiphytes on Pseudobombax sp. nov. in three inselbergs in the
Atlantic Forest Domain in state of Espírito Santo and evaluated the floristic similarity between the areas. We
sampled 111 phorophytes in three regions in the southern of Espírito Santo state and identified 151 species,
77 genera and 21 families of vascular epiphytes, of which the families Orchidaceae and Bromeliaceae
showed the highest richness. Non-parametric estimators (Chao 2, Jackknife 1) indicate that 90 and 95% of
species richness of epiphytes was recorded. The most diversified ecological category was the characteristic
holoepiphytes. The ratio of the number of epiphytes and number of phorophytes sampled in a montane
inselberg, in this study, was greater than the richness of vascular epiphytes found in the rocky outcrops of
quartzite, and, in general, different types of Atlantic Domain forests, but smaller in richness for some Dense
Ombrophilous Forests of southern Brazil. The three inselberg areas had distinct floras. The high richness,
the endemism found, and the number of endangered species of epiphytes demonstrate the important role
of Pseudobombax sp. nov., because of its architecture and size, in the maintenance of biodiversity on the
inselbergs in southeastern Brazil.
Key words: conservation, non-parametric estimators richness, specific phorophyte, vascular flora, industrial
granite quarries.
Resumo
Este estudo avaliou a riqueza de epífitas vasculares sobre Pseudobombax sp. nov. em três inselbergs do
Domínio Atlântico no estado do Espírito Santo e avaliou a similaridade florística entre as áreas. Foram
amostrados 111 forófitos, em três regiões no sul do estado do Espírito Santo e identificados 151 espécies, 77
gêneros e 21 famílias de epífitos vasculares, das quais as famílias Orchidaceae e Bromeliaceae apresentaram
maior riqueza. Estimadores não-paramétricos (Chao 2, Jackknife 1) indicam que 90 e 95% da riqueza específica
de epífitas foi registrada. A categoria ecológica mais diversificada foi a dos holoepífitos característicos. A
razão entre o número de epífitas e número de forófitos amostrados em um inselberg montano, neste estudo,
foi maior do que a riqueza de epífitos encontrados nos campos rupestres, e, em geral, em diferentes tipos de
florestas do Domínio Atlântico, mas menor em riqueza para algumas Florestas Ombrófilas Densas do sul
do Brasil. As três áreas de inselbergs tinham floras distintas. A elevada riqueza, o endemismo encontrado e
o número de espécies ameaçadas dos epífitos evidenciam a importante função de Pseudobombax sp. nov.,
por sua arquitetura e tamanho, para a manutenção da biodiversidade em inselbergs do sudeste brasileiro.
Palavras-chave: conservação, estimadores não-paramétricos de riqueza, forófito específico, flora vascular,
pedreira de granito industrial.
Vascular epiphytes on Pseudobombax (Malvaceae) in rocky outcrops
(inselbergs) in Brazilian Atlantic Rainforest: basis for conservation
of a threatened ecosystem
Epífitas vasculares sobre Pseudobombax (Malvaceae) em afloramentos rochosos (inselbergs)
na Mata Atlântica Brasileira: bases para a conservação de um ecossistema ameaçado
Dayvid Rodrigues Couto1,4, Henrique Machado Dias1, Mirian Cristina Alvarez Pereira2,
Cláudio Nicoletti de Fraga3 & José Eduardo Macedo Pezzopane1
Rodriguésia 67(3): 583-601. 2016
http://rodriguesia.jbrj.gov.br
DOI: 10.1590/2175-7860201667304
1 Universidade Federal do Espírito Santo (CCA/UFES), Programa de Pós-graduação em Ciências Florestais, Depto. Ciências Florestais e da Madeira, Centro de
Ciências Agrárias, Av. Governador Lindemberg 316, 29550-000, Jerônimo Monteiro, ES, Brazil.
2 Universidade Federal do Espírito Santo (CCA/UFES), Depto. Ciências Biológicas, Centro de Ciências Agrárias, Alto Guararema s/n, 29500-000, Alegre, ES, Brazil.
3 Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, R. Pacheco Leão 915, 22460-030, Rio de Janeiro, RJ, Brazil.
4 Author for correspondence: dayvidcouto@hotmail.com

584 Couto, D.R. et al.
Rodriguésia 67(3): 583-601. 2016
Introduction
Epiphytes represent a strategy since the
appearance of trees in the late Devonian and
Carboniferous (Dilcher et al. 2004) evolving
convergently in a large number of lineages of
vascular and non-vascular plants (Gentry &
Dodson 1987). Vascular epiphytes represnt about
9% of the world’s vascular plant flora and are
most abundant in tropical rain forests, where they
comprise a significant part of the diversity and
complexity found in these ecosystems (Krömer
et al. 2007; Zotz 2013).
In Brazil, studies on this group of plants
are concentrated mainly in the south and
southeast regions, especially in forest ecosystems
associated with the Atlantic Forest Domain.
Several investigators have described the high
richness of vascular epiphytic species in these
regions, associated with multiple phorophytes
(Buzatto et al. 2008; Kersten & Kuniyoshi 2009;
Fontoura et al. 2009; Geraldino et al. 2010;
Mania & Monteiro 2010; Blum et al. 2011) or
specific phorophytes (Werneck & Espírito-Santo
2002; Gonçalves & Waechter 2003; Obermüller
et al. 2012) with predominance of members of
the families Orchidaceae and Bromeliaceae,
representing the most diverse ecological category
of true holoepiphytes, spending their entire life
cycle on phorophytes.
The few studies focusing on specific
phorophytes in Brazil have shown the
importance of these plants for maintaining
epiphyte biodiversity. In the present study, we
selected Pseudobombax sp. nov. (Malvaceae,
Bombacoideae) as a specific phorophyte. This
large tree commonly occurs in the Atlantic Forest
Domain on granite-gneiss rocky outcrops known
as inselbergs, and is usually densely covered by
epiphytes. Inselbergs are isolated islands covered
by different vegetation within the original forest
matrix, and harbor a highly distinctive flora with
high species richness and endemism (Barthlott
& Porembski 2000).
Among the three major regions recognized
worldwide for vegetation of inselbergs,
southeastern Brazil stands out (Porembski
2007). In this context, the inselbergs situated
in the southern portion of the state of Espírito
Santo, are recognized as priority for floristic
studies and the creation of protected area,
although knowledge of their biodiversity is still
incipient (Martinelli 2007). In addition to these
gaps, these environments are highly threatened
by industrial granit quarrying. This industry
was first established in Brazil in Espírito Santo,
which is now the largest stone-processing center
in Latin America (Chiodi-Filho 2009). Based on
the high species richness and endemism, and on
these anthropogenic pressures, the inselbergs
of southeastern Brazil are recognized as one
of the three most important area for inselberg
conservation (Porembski 2007).
In view of the importance of epiphytes
to species richness in tropical ecosystems,
especially in the Atlantic Forest Domain (Kersten
2010), and of the limited knowledge of epiphytes
associated with granite-gneiss inselbergs in
Brazil, the present study evaluated the richness
of vascular epiphytic species associated with
Pseudobombax sp. nov. on three inselbergs of the
Atlantic Forest. We also categorized these species
according to their ecological relationships with
the phorophyte, and evaluated the floristic
similarity among the three inselbergs, generating
an important basis for conservation of these
threatened ecosystems.
Material and Methods
Study area
Three populations of Pseudobombax sp.
nov. occurring on granite-gneiss inselbergs in
southern Espírito Santo state were sampled
(Fig. 1). In each inselberg 37 phorophytes were
sampled (111 total).
Upper montane Inselberg - UMI (Fig.
2a-b) - Granitic-gneissic Inselberg of Pedra
Roxa (PR) is located in the Caparaó National
Park, municipality of Ibitirama (20o23’43’’S
and 41o44’05”W), with a sampling area of ca.
2 ha, approximate elevation of 1,114 m, in a
humid valley on the banks of the Pedra Roxa
River, within a matrix of Dense Ombrophilous
Montane Forest (Veloso et al. 1991). The climate
is Köeppen Cwb (highland tropical climate),
with a mean annual rainfall of 1,391 mm and a
mean annual temperature of 17oC. In Caparaó
National Park, Pseudobombax sp. nov. forms
large groupings; it is the only tree species found
on rocky outcrops, and reaches a mean height of
4.8 m (± 2.2) and mean diameter at 1.3 m above
ground level (diameter at breast height, dbh) of
22.4 cm (± 17.5).
Montane Inselberg - MI (Fig. 2c,e) -
Granitic-gneissic Inselberg of Pedra dos Pontões
(PP) is located in the municipality of Mimoso
do Sul (20o56’18’’S and 41o32’38”W), between

Vascular epiphytes in inselbergs from the Atlantic Rainforest
Rodriguésia 67(3): 583-601. 2016
585
700 and 730 m elevation, surrounded by a
human-impacted matrix of fragments of Montane
Seasonal Semideciduous Forest (Veloso et al.
1991). The climate is Köeppen Cwb, with a mean
annual rainfall of 1,375 mm and mean annual
temperature of 21ºC. In Pedra dos Pontões,
sparse stands of Pseudobombax sp. nov. are a
prominent feature of the rocky outcrop, with
some large individuals, in some cases forming
small groups, with a mean height of 7.7 m (± 3.3)
and mean dbh of 46.4 cm (± 31.9). In this area,
the richness of epiphytic Bromeliaceae is great,
as described by Couto et al. (2013).
Submontane Inselberg - SMI (Fig. 2d) -
Granitic-gneissic Inselberg of Pedra Lisa (PL) is
located in the district of Burarama, municipality
of Cachoeiro de Itapemirim (20o41’55’’S and
41o18’28”W), between 180 and 300 m elevation,
within an anthropogenic matrix of fragments of
Submontane Seasonal Semideciduous Forest
(Veloso et al. 1991). The climate is Köeppen
Cwa, with a mean annual rainfall of 1,293 mm
and mean temperature of 24oC. In this area,
Pseudobombax sp. nov. grows sparsely, directly
on the rock, and reaches a mean height of 6.2 m
(± 3.9) and mean dbh of 35.8 cm (± 13.8).
Phorophyte sampling
Pseudobombax sp. nov. (Malvaceae;
Bombacoideae) shows a morphological (leaves,
flowers, fruits and seeds) and evolutionary
affinity to Pseudobombax petropolitanum
A.Robyns, since they belong to the same clade,
which has apparently recently evolved (J.G.
Carvalho-Sobrinho, unpublished data). Currently
the phorophyte taxon used in the present study
is an undescribed species of Pseudobambax
and being described with name Pseudobombax
rupicola Carvalho-Sobrinho & D.R. Couto
(indet.), referring to strictly rupicolous habit.
The individuals sampled were caespitose shrubs
or trees, with heights of 2.5m up to 15.3 m with
patent branches and large surface roots on the
rock.
Data collection and analysis
To develop the list of epiphytic vascular
plants, 111 individuals of Pseudobombax sp. nov.
were surveyed. When necessary, the trees were
climbed using mountain-climbing techniques
adapted to the canopy (Perry 1978).
Epiphytes found fertile were collected,
following the usual procedures of floristic
Figure 1 – Location of three populations of Pseudobombax sp. nov. on granitic-gneissic inselbergs in the southern
part of Espírito Santo state, where the epiphytic vascular flora was recorded.

586 Couto, D.R. et al.
Rodriguésia 67(3): 583-601. 2016
Figure 2 – Occurrence of environments of Pseudobombax sp.nov. in the Brazilian Atlantic Rainforest, where vascular
epiphytes were recorded. – a. general view of the vegetation on Caparao National Park; b. general view of population
the of Pseudobombax sp.nov. from upper montane inselberg of Pedra Roxa; c. general view of the montane inselberg of
Pedra dos Pontões; d. submontane inselberg of Pedra Lisa; e. detail of a phorophyte sampled from Pedra dos Pontões .
a
b c
de

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Rodriguésia 67(3): 583-601. 2016
587
surveys (Mori et al. 1989), with the collections,
when possible, made in triplicate, to send to
experts on the respective taxa. Specimens
were collected sterile when necessary, grown
until they flowered, and herborized for later
identification.
The botanical material was identified using
analytical taxonomic keys, or by comparison
with material deposited in herbaria, or by
sending duplicate specimens to the specialists.
The voucher specimens are deposited mostly in
the herbarium of the Museum of Biology Prof.
Mello Leitão (MBML) and the material from the
most recent surveys (2010–2012) was deposited
in the herbarium of the Federal University of
Espírito Santo (VIES). Duplicates were sent to
the following herbaria: R (National Museum of
Rio de Janeiro), RB (Research Institute of the
Botanical Garden of Rio de Janeiro), UFRN
(Herbarium of the Federal University of Rio
Grande do Norte) and VIC (Herbarium of the
Federal University of Viçosa).
The circumscription of species in families
for angiosperms follows the Angiosperm
Phylogeny Group (APG III 2009), Smith
et al. (2006) for monilophytes (ferns) and
Christenhusz et al. (2011) for lycophytes
with taxa names being updated according to
supplementary materials in BFG (2015) for
angioesperms and Prado et al. (2015) for ferns
and lycophytes, and the Missouri Botanical
Garden (<http://tropicos.org>). Abbreviations of
author names follow Brummitt & Powell (1992)
and IPNI (<http://www.ipni.org>).
In order to estimate the total number of
epiphytic species for each sampled inselberg
(SMI, MI and UMI) and for the total sample,
rarefaction curves were constructed, based on the
presence or absence of epiphytes on phorophytes
using three statistical non-parametric estimators:
ICE, Chao 2 and Jackknife 1 (Gotelli & Colwell
2011), performed by 100 random resampling
of the data, using EstimateS software (Colwell
2013).
Threatened species are cited according
to the Official List of Endangered Species of
the Brazilian Flora, through Ministerial Order
number 443, of 17 December 2014 (MMA
2014), and specifically for Espírito Santo, as
listed by the State Institute of the Environment
(Espírito Santo 2005), under the protection of
Decree 1499-R, published by Simonelli & Fraga
(2007).
From field observations, the epiphytes
were classified into four ecological categories,
according to Benzing (1990), with modifications
according to Kersten & Kuniyoshi (2009), as:
characteristic holoepiphytes (Epi), facultative
holoepiphytes (Fac), accidental holoepiphytes
(Aci), hemiepiphytes (Hem).
To assess the floristic similarity among
the three inselbergs, was prepared a matrix
of binary data (presence/absence) compiled
from the occurrence of epiphytes in 111
sampled phorophytes. We used the unweighted
pair group method with arithmetic mean
(UPGMA), incorporating Jaccard´s coefficient
as a measure of distance, with the aid of software
Paleontological Statistics - PAST v. 1.89
(Hammer et al. 2001). Species not identified to
species level (sp.) were excluded and species
with dubious identification (order [aff.]) were
considered.
The species richness was compared with
that found in other locations, based on studies
that treated similar numbers of phorophytes
(Kersten & Silva 2001, 2002; Werneck &
Espírito-Santo 2002; Gonçalves & Waechter
2003; Giongo & Waechter 2004; Alves et al.
2008; Dettke et al. 2008; Fontoura et al. 2009;
Kersten & Kuniyoshi 2009; Blum et al. 2011).
The ratios of the numbers of epiphytes and
phorophytes were also obtained.
Results
One hundred and fifty-one species
of vascular epiphytes were recorded on
Pseudobombax sp. nov., distributed in 77
genera and 21 families (Tab. 1). Angiosperms
contributed 125 species, 65 genera and 15
families, while monilophytes and licophytes
were represented by 26 species, 12 genera
and six families. Orchidaceae contributed 57
species, followed by Bromeliaceae with 31.
The genera with the highest number of species
were Epidendrum (Orchidaceae) with eight
species, followed by Tillandsia (Bromeliaceae)
and Octomeria (Orchidaceae) each with seven
species, and Vriesea (Bromeliaceae) and
Peperomia (Piperaceae) with six species each.
Campyloneurum centrobrasilianum
Lellinger, Isabelia virginalis Barb. Rodr.,
Nephrolepis exaltata (L.) Schott, Peperomia
itatiaiana Yunck., Rhipsalis cf. crispata (Haw.)
Pfeiff. and Vanhouttea leonii Chautems are
new records for the state of Espírito Santo.

588 Couto, D.R. et al.
Rodriguésia 67(3): 583-601. 2016
Family (number species) / Species Locality Cat Voucher
PL PP PR
AMARYLLIDACEAE (1)
Hippeastrum aulicum (Ker Gawl.) Herb. XFac DRC 2245 (VIES)
ANEMIACEAE (3)
Anemia aspera (Feé) Baker XAci DRC 2209 (VIES)
Anemia tomentosa var. anthriscifolia (Schard.) Mickel XAci DRC 2153 (VIES)
Anemia villosa Humb. & Bonpl. ex Willd. XAci DRC 2262 (VIES)
ARACEAE (6)
Anthurium scandens (Aubl.) Engl. X X Epi DRC 214 (MBML)
Anthurium solitarium Schott XFac DRC 1323 (VIES)
Anthurium sp.1 XAci DRC 2103 (VIES)
Anthurium sp.2 X X Epi DRC 2105 (VIES)
Philodendron cordatum Kunth ex Schott XHem DRC 1347 (VIES)
Philodendron edmundoi G.M.Barroso X X Aci DRC 1556 (VIES)
ARALIACEAE (1)
Oreopanax capitatus (Jacq.) Decne. & Planch. XHem DRC 2072 (VIES)
ASPLENIACEAE (3)
Asplenium auritum Sw. XEpi DRC 1452 (VIES)
Asplenium harpeodes Kunze XEpi DRC 2120 (VIES)
Asplenium praemorsum Sw. XEpi DRC 2230 (VIES)
ASTERACEAE (2)
Cyrtocymura scorpioides (Lam.) H.Rob. XAci DRC 1390 (VIES)
Eremanthus crotonoides (DC.) Sch.Bip. XAci DRC 1375 (VIES)
BEGONIACEAE (3)
Begonia angularis Raddi XAci DRC 2246 (VIES)
Begonia curtii L.B.Sm. & B.G.Schub. XAci LK 6793 (MBML)
Begonia reniformis Dryand. X X Aci DRC 2244 (VIES)
BROMELIACEAE (31)
Aechmea nudicaulis (L.) Griseb. X X X Epi DRC 208 (MBML)
Aechmea ramosa Mart. ex Schult. & Schult.f. XFac DRC 180 (MBML)
Aechmea squarrosa Baker XFac DRC 1457 (VIES)
Alcantarea extensa (L.B.Sm.) J.R.Grant XAci DRC 1428 (VIES)
Alcantarea patriae Versieux & Wand. X X Aci DRC 2153 (vies)
Billbergia horrida Regel XFac DRC 175 (MBML)
Table 1 – Vascular epiphytes on Pseudobombax sp. nov. from granitic-gneissic inselbergs in Atlantic Forest, southern
Espírito Santo state, Brazil. Locality: PL = Pedra Lisa (submontane inselberg); PP = Pedra dos Pontões (montane
inselberg); PR = Pedra Roxa (upper montane inselberg); Cat = Ecological category (Epi = characteristic holoepiphytes;
Fac = facultative holoepiphyte; Aci = accidental holoepiphytes; Hem = hemiepiphyte). Collectors: DRC = Dayvid
Rodrigues Couto; LK= Ludovic Kollmann.

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Rodriguésia 67(3): 583-601. 2016
589
Family (number species) / Species Locality Cat Voucher
PL PP PR
Billbergia tweedieana Baker XEpi DRC 1346 (VIES)
Billbergia zebrina (Herb.) Lindl. XEpi DRC 2111 (VIES)
Catopsis sessiliflora (Ruiz & Pav.) Mez XEpi DRC 1350 (VIES)
Edmundoa lindenii (Regel) Leme XFac DRC 1456 (VIES)
Neoregelia dayvidiana Leme & A.P.Fontana XEpi LK 7566 (MBML)
Neoregelia pauciflora L.B.Sm. XFac DRC 2106 (MBML)
Neoregelia sp. XEpi DRC 2253 (VIES)
Pitcairnia abyssicola Leme & Kollmann XAci LK 7873 (MBML)
Pitcairnia flammea Lindl. XAci DRC 1451 (VIES)
Quesnelia arvensis (Vell.) Mez XAci DRC 2068 (VIES)
Quesnelia kautskyi C.M.Vieira XAci DRC 276 (MBML)
Quesnelia strobilispica Wawra XFac DRC 174 (MBML)
Tillandsia gardneri Lindl. X X Epi DRC 186 (MBML)
Tillandsia geminiflora Brongn. XEpi DRC 2228 (VIES)
Tillandsia loliacea Mart. ex Schult. & Schult.f. XEpi DRC 2137 (VIES)
Tillandsia recurvata (L.) L. X X Epi DRC 2126 (VIES)
Tillandsia stricta Sol. X X X Epi DRC 2222 (VIES)
Tillandsia tenuifolia L. XEpi DRC 2110 (VIES)
Tillandsia usneoides (L.) L. X X Epi DRC 2223 (VIES)
Vriesea capixabae Leme XEpi not collected
Vriesea gigantea Gaudich. XEpi DRC 2128 (VIES)
Vriesea lubbersii (Baker) E.Morren X X Epi DRC 242 (MBML)
Vriesea poenulata (Baker) E.Morren ex Mez XEpi DRC 2257 (VIES)
Vriesea aff. procera (Mart. ex Schult. & Schult.f.) Wittm. XEpi DRC 2138 (R)
Vriesea vagans (L.B.Sm.) L.B.Sm. X X Epi DRC 1857 (VIES)
CACTACEAE (8)
Epiphyllum phyllanthus (L.) Haw. XEpi not collected
Hatiora salicornioides (Haw.) Britton & Rose XEpi DRC 2081 (MBML)
Hylocereus setaceus (Salm-Dyck) R.Bauer XEpi DRC 2219 (VIES)
Lepismium cruciforme (Vell.) Miq. XEpi LK 6804 (MBML)
Rhipsalis crispata (Haw.) Pfeiff. XEpi LK 6803 (MBML)
Rhipsalis lindbergiana K.Schum. X X Epi DRC 2121 (VIES)
Rhipsalis neves-armondii K. Schum XEpi DRC 1952 (VIES)
Rhipsalis teres (Vell.) Steudt. X X Epi DRC 1238 (VIES)
CLUSIACEAE (1)
Clusia aemygdioi Gomes da Silva & B.Weinberg XHem DRC 2073 (VIES)
GESNERIACEAE (5)

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Family (number species) / Species Locality Cat Voucher
PL PP PR
Nematanthus hirtellus (Schott) Wiehler XEpi DRC 1334 (VIES)
Paliavana prasinata (Ker Gawl.) Benth. XAci DRC 311 (MBML)
Sinningia magnifica (Otto & A.Dietr.) Wiehler XFac DRC 2226 (VIES)
Sinningia speciosa (Lodd.) Hiern XAci DRC 2207 (VIES)
Vanhouttea leonii Chautems XAci DRC 2247 (VIES)
LOMARIOPSIDACEAE (1)
Nephrolepis exaltata (L.) Schott XFac DRC 1348 (VIES)
MELASTOMATACEAE (1)
Tibouchina heteromalla (D.Don) Cogn. XAci DRC 1374 (VIES)
MORACEAE (1)
Ficus arpazusa Casar. XHem DRC 1406 (VIES)
ORCHIDACEAE (57)
Acianthera auriculata (Lindl.) Pridgeon & M.W.Chase X X Epi DRC 1385 (VIES)
Acianthera crinita (Barb.Rodr.) Pridgeon & M.W.Chase XEpi DRC 91 (MBML)
Acianthera heliconiscapa (Hoehne) F.Barros XEpi DRC 324 (MBML)
Acianthera leptotifolia (Barb.Rodr.) Pridgeon & M.W.Chase XEpi DRC 2096 (MBML)
Acianthera luteola (Lindl.) Pridgeon & M.W.Chase XEpi DRC 268 (MBML)
Acianthera saurocephala (Lodd.) Pridgeon & M.W.Chase XEpi DRC 172 (MBML)
Aspasia lunata Lindl. XEpi DRC 1328 (VIES)
Barbosella spiritusanctensis (Pabst) F.Barros & Toscano XEpi DRC 618 (MBML)
Brasilidium crispum (Lodd.) Campacci X X Epi DRC 239 (MBML)
Brasiliorchis marginata (Lindl.) R.B.Singer et al. X X Epi DRC 147 (MBML)
Brasiliorchis phoenicanthera (Barb.Rodr.) R.B.Singer et al. XEpi DRC 125 (MBML)
Brasiliorchis picta (Hook.) R.B.Singer et al. XEpi DRC 2220 (VIES)
Bulbophyllum cantagallense (Barb.Rodr.) Cogn. X X Epi DRC 1449 (VIES)
Bulbophyllum micropetaliforme J.E.Leite XEpi DRC 2276 (VIES)
Bulbophyllum sp. XEpi DRC 2225
Christensonella pachyphylla (Schltr. ex Hoehne) Szlach. et al. XEpi DRC 23 (MBML)
Christensonella subulata (Lindl.) Szlach. et al. X X Epi DRC 2252 (VIES)
Cyclopogon argyrifolius Barb.Rodr. XAci not collected
Cyrtopodium glutiniferum Raddi X X Aci DRC 190 (MBML)
*Dendrobium nobile Lindl. XEpi not collected
Elleanthus brasiliensis (Lindl.) Rchb.f. XFac DRC 1400 (VIES)
Encyclia patens Hook. X X Epi DRC 1243 (VIES)
Epidendrum avicula Lindl. XEpi DRC 2124 (VIES)
Epidendrum campaccii Hágsater & L.Sánchez X X Epi DRC 2123 (VIES)
Epidendrum densiflorum Hook. X X Fac DRC 2260 (VIES)

Vascular epiphytes in inselbergs from the Atlantic Rainforest
Rodriguésia 67(3): 583-601. 2016
591
Family (number species) / Species Locality Cat Voucher
PL PP PR
Epidendrum filicaule Lindl. XEpi DRC 2149 (VIES)
Epidendrum rigidum Jacq. XEpi DRC 2122 (VIES)
Epidendrum secundum Jacq. XAci DRC 2083 (MBML)
Epidendrum tridactylum Lindl. XEpi DRC 90 (MBML)
Grandiphyllum divaricatum (Lindl.) Docha Neto XEpi not collected
Heterotaxis brasiliensis (Brieger & Illg) F.Barros X X Epi DRC 76 (MBML)
Isabelia virginalis Barb.Rodr. XEpi DRC 2234 (VIES)
Isochilus linearis (Jacq.) R.Br. X X Epi DRC 2236 (VIES)
Laelia gloriosa (Rchb.f.) L.O.Williams XEpi DRC 2208 (VIES)
Lankesterella longicollis (Cogn.) Hoehne XEpi DRC 1404 (VIES)
Masdevallia infracta Lindl. XEpi DRC 2275 (VIES)
Maxillariella robusta (Barb.Rodr.)M.A.Blanco & Carnevali XEpi DRC 320 (MBML)
Mormolyca rufescens (Lindl.) M.A.Blanco X X Epi DRC 30 (MBML)
Octomeria crassifolia Lindl. X X Epi DRC 2240 (VIES)
Octomeria decumbens Cogn. XEpi DRC 325 (MBML)
Octomeria cf. diaphana Lindl. XEpi DRC 2256
Octomeria sp. 1 XEpi DRC 2237 (VIES)
Octomeria sp. 2 XEpi DRC 297 (MBML)
Octomeria sp. 3 XEpi DRC 2115 (VIES)
Octomeria sp. 4 XEpi DRC 2132 (VIES)
Promenaea xanthina (Lindl.) Lindl. XEpi DRC 2235 (VIES)
Ornithidium rigidum (Barb.Rodr.) M.A.Blanco & Ojeda XEpi DRC 234 (MBML)
Polystachya concreta (Jacq.) Garay & Sweet X X X Epi DRC 2216 (VIES)
Prescottia plantaginifolia Lindl. ex Hook. XAci DRC 140 (MBML)
Prosthechea cf. bulbosa (Vell.) W.E.Higgins X X Epi DRC 2259
Prosthechea calamaria (Lindl.) W.E.Higgins XEpi DRC 2268
Prosthechea fragrans (Sw.) W.E.Higgins XEpi DRC 2217 (VIES)
Sophronitis cernua Lindl. XEpi DRC 2148 (VIES)
Specklinia grobyi (Batem. ex Lindl.) F.Barros X X Epi DRC 139 (MBML)
Stelis argentata Lindl. X X Epi DRC 2079 (MBML)
Xylobium variegatum (Ruiz & Pav.) Garay & Dunst. XAci DRC 189 (MBML)
Zygopetalum intermedium Lodd. XAci DRC 254 (MBML)
PIPERACEAE (6)
Peperomia alata Ruiz & Pav. XFac DRC 2284 (VIES)
Peperomia glabella (Sw.) A.Dietr. var. glabella XFac DRC 2301 (VIES)
Peperomia itatiaiana Yunck. XAci DRC 2102 (VIES)
Peperomia rubricaulis (Nees) A.Dietr. XEpi DRC 1380 (VIES)

592 Couto, D.R. et al.
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Family (number species) / Species Locality Cat Voucher
PL PP PR
Peperomia tetraphylla (G.Forst.) Hook. & Arn. XEpi DRC 2097 (MBML)
Peperomia trinervis Ruiz & Pav. var. trinervis XFac DRC 1237 (VIES)
POACEAE (1)
**Melinis minutiflora P.Beauv. X X Aci DRC 2231 (VIES)
POLYPODIACEAE (14)
Campyloneurum acrocarpon Fée XAci DRC 1331 (VIES)
Campyloneurum centrobrasilianum Lellinger X X Epi DRC 2254 (VIES)
Microgramma percussa (Cav.) de la Sota XEpi DRC 1445 (VIES)
Microgramma squamulosa (Kaulf.) de la Sota X X Epi DRC 2270 (VIES)
Microgramma tecta (Kaulf.) Alston XEpi DRC 2116 (VIES)
Niphidium crassifolium (L.) Lellinger X X Epi DRC 2109 (VIES)
Pecluma pectinatiformis (Lindm.) M.G.Price XEpi DRC 2118 (VIES)
Pecluma plumula (Willd.) M.G.Price XEpi DRC 2221 (VIES)
Phlebodium aureum (L.) J.Sm. XAci DRC 2271 (VIES)
Pleopeltis astrolepis (Liebm.) E.Fourn. XEpi DRC 2108 (VIES)
Pleopeltis hirsutissima (Raddi) de la Sota XEpi DRC 2088 (MBML)
Pleopeltis minima (Bory) J. Prado & R.Y. Hirai X X Epi DRC 2127 (MBML)
Pleopeltis monoides (Weath.) Salino XEpi DRC 2270 (VIES)
Pleopeltis pleopeltifolia (Raddi) Alston XEpi DRC 1954 (VIES)
PTERIDACEAE (4)
Doryopteris collina (Raddi) J. Sm. XAci DRC 1955 (VIES)
Doryopteris magdalenensis (Brade) Brade XAci DRC 2261 (VIES)
Doryopteris sp. XAci DRC 1558 (VIES)
Hemionitis tomentosa (Lam.) Raddi XAci DRC 2210 (VIES)
SELAGINELLACEAE (1)
Selaginella convoluta (Arn.) Spring X X Aci DRC 2152 (VIES)
SOLANACEAE (1)
Markea atlantica Stehmann & Giacomin XEpi DRC 1455 (VIES)
TOTAL 24 105 62
(*) casual alien species; (**) invasive species
In addition, two species, Neoregelia dayvidiana
Leme & A.P.Fontana and Pitcairnia abyssicola
Leme & L.Kollmann (Bromeliaceae) are endemic
to the Pedra dos Pontões region; and two species,
Dendrobium nobile Lindl. (Orchidaceae) and
Melinis minutiflora P.Beauv. (Poaceae), are exotic.
Of the total number of species, 24 were
recorded for Submontane Inselberg (PL), 105 for
Montane Inselberg (PP) and 62 for Upper montane
Inselberg (PR). Orchidaceae (57 species) was the
richest family in all areas, followed by Bromeliaceae
(26 species) (Fig. 3). Polypodiaceae ranked third

Vascular epiphytes in inselbergs from the Atlantic Rainforest
Rodriguésia 67(3): 583-601. 2016
593
in PP and PR, whereas Cactaceae ranked third
in PL. Members of Bromeliaceae, Cactaceae,
Gesneriaceae, Orchidaceae, Polypodiaceae and
Pteridaceae were common to all three inselbergs.
Of the 77 genera found, 10 were common to all
three areas (Aechmea, Alcantarea, Tillandsia,
Vriesea, Brasiliorchis, Bulbophyllum, Epidendrum,
Polystachya, Prosthechea and Pleopeltis), while
21 were unique to PP, nine to PR and six to PL.
Overall, considering the 111 sampled
phorophytes, we recorded 151 species of vascular
epiphytes, while non-parametric estimators
indicated asymptotic richness between 159.0 (ICE)
and 166.8 (Jachnife 1), suggesting that few species
inventoried would be expanded if the sampling
indicate that 90 and 95% of species richness of
Figure 4 – Rarefaction curve and richness estimations for the 111 phorophytes sampled on Atlantic Rainforest inselbergs (a) and the
three inselbergs sampled: Submontane inselberg (b), Montane inselberg (c) and Upper montane inselberg (d) showing the observed
number of species in our dataset (black solid line), its 95% confidence interval (dotted black lines) and the number of species estimated
for the three inselbergs, using three usual richness estimators: ICE (incidence-based coverage estimator), Chao 2 and Jackknife 1.
Figure 3 – Species richness of the most important
families of epiphytes on Pseudobombax sp. nov. from
three granite-gneiss inselbergs in Atlantic Rainforest,
southern Espírito Santo state, Brazil.
a
cb d

594 Couto, D.R. et al.
Rodriguésia 67(3): 583-601. 2016
gardneri Lindl. and Pleopeltis minima (Bory)
J.Prado & R.Y. Hirai. Alcantarea patriae is
endemic to inselbergs in southern Espírito Santo,
and the other two are widely distributed in South
America. PL and PR shared only one species,
Selaginella convoluta (Arn.) Spring, which is
widely distributed on rocky outcrops in Brazil
and South America as a whole. Only three species
were shared among all three areas: Aechmea
nudicaulis (L.) Griseb., Tillandsia stricta Sol.
and Polystachya concreta (Jacq.) Garay & Sweet.
Of the total of 151 species, 64% were
classified as characteristic holoepiphytes,
including all species of Aspleniaceae, Cactaceae
and Solanaceae; 23% as accidental holoepiphytes,
represented by all types of families: Anemiaceae,
Asteraceae, Begoniaceae, Pteridaceae,
Selaginellaceae and Melastomataceae;
10% as facultative holoepiphytes; and 3%
as hemiepiphytes, including the primary
hemiepiphytes Clusia aemygdioi Gomes da
Silva & Weinberg, Ficus arpazusa Casar and
Oreopanax capitatus (Jacq.) Decne. & Planch.
and the secondary hemiepiphyte Philodendron
cordatum Kunth ex Schott.
Among the species registered, 19 are
present on official lists of endangered species.
Eight species are under some degree of threat
according to the list of endangered flora of Brazil.
Four species are listed as “Vulnerable”: Begonia
curtii L.B.Sm. & B.G.Schub., Quesnelia kautskyi
C.M.Vieira, Grandiphyllum divaricatum (Lindl.)
Docha Neto and Isabelia virginalis Barb.Rodr.;
and four as “Endangered”: Clusia aemygdioi,
Vanhouttea leonii Chautems, Peperomia itatiaiana
Yunck. and Pleopeltis monoides (Weath.) Salino.
Among the species found, 14 species are
threatened according to the list of endangered
flora of Espírito Santo: Eight species are listed
as “Vulnerable”: Begonia angularis Raddi,
Begonia curtii, Quesnelia kautskyi, Sinningia
magnifica (Otto & A.Dietr.) Wiehler, Sinningia
speciosa (Lodd.) Hiern, Brasilidium crispum
(Lodd.) Campacci, Brasiliorchis phoenicanthera
(Barb.Rodr.) R.B.Singer et al. and Pleopeltis
monoides; three as “Endangered”: Nematanthus
hirtellus (Schott) Wiehler, Acianthera crinita
(Barb.Rodr.) Pridgeon & M.W.Chase and A.
saurocephala (Lodd.) Pridgeon & M.W.Chase;
and three as “Critically Endangered”: Barbosella
spiritusanctensis (Pabst) F.Barros & Toscano,
Bulbophyllum cantagallense (Barb.Rodr.) Cogn.
and Epidendrum tridactylum Lindl..
epiphytes was recorded. Analyzing the three
inselbergs separately, it is observed that in PL, the
sampled epiphytic community in this study was
an amount equal to the estimated values (Chao 2,
ICE and Jackknife 1), already in PP and PR can be
found new occurrences epiphytic species. In PP is
estimated that 87% (120, Jackknife 1) and 91%
(114, ICE), while in PR 93% (64, ICE) and 96%
(66, Jackknife 1) the total specific richness was
inventoried (Fig. 4).
The analysis of the floristic relationships
among the three study areas, calculated using
the Jaccard coefficient (Fig. 5) and represented
in the Venn diagram (Fig. 6) demonstrated the
existence of three distinct floras. PR and PP, both
within montane forests, were most similar to each
other, with 30 shared species. The most distinct
was PL, within a lower montane semideciduous
forest, with only three species shared with PP:
Alcantarea patriae Versieux & Wand., Tillandsia
Figure 5 – Dendrogram of floristic similarity (Jaccard,
binary data) of vascular epiphytes on 111 individuals
of Pseudobombax sp. nov. from three granitic-gneissic
inserbergs inventoried in Atlantic Rainforest, southern
Espírito Santo state, Brazil. PP = montane inselberg; PR
= upper montane inselberg; PL = submontane inselberg.

Vascular epiphytes in inselbergs from the Atlantic Rainforest
Rodriguésia 67(3): 583-601. 2016
595
Discussion
The present study provides the first
contributions to the knowledge of vascular
epiphytic flora on inselbergs. We assessed the
vascular epiphytic richness associated with the
phorophyte Pseudobombax sp. nov. on three
inselbergs in the Brazilian Atlantic Rainforest.
Non-parametric estimators (Chao 2, Jackknife 1)
indicate that 90 and 95% of species richness of
epiphytes was recorded. The ratio of number of
vascular epiphytes and number of phorophytes
sampled on Pseudobombax sp. nov., in a montane
inselberg, was higher than the richness of vascular
epiphytes found on quartzite rocky outcrops located
in the Cerrado Domain, and in general, in different
forest types of the Atlantic Domain, but smaller
in riches for some areas of rain forest of southern
Brazil. The inselbergs differ in their floristic
composition, although members of Orchidaceae
and Bromeliaceae predominate. The inselbergs
even being inserted in a completely different
vegetation surrounding matrix do not represent a
barrier for distribution of vascular epiphytes.
These families of epiphytic flora are also
among the most speciose in Brazil (Kersten & Silva
2001, 2002; Giongo & Waechter 2004; Kersten &
Kuniyoshi 2009; Blum et al. 2011) and also in the
extra-tropical regions of the country (Küper et al.
2004; Krömer et al. 2005, 2007). In the present
study, Orchidaceae and Bromeliaceae contributed
55% of the total number of species recorded on
Pseudobombax sp. nov., a similar percentage to
that observed by other studies (Geraldino et al.
2010; Blum et al. 2011).
The high species richness of epiphytes is an
unusual aspect of the types of rocky vegetation such
as on inselbergs, where extreme environmental
factors (e.g., total or partial absence of soil and
nutrients, water scarcity, and direct wind exposure)
limit the establishment and longevity of larger
trees that support a greater richness of epiphytes
(Hernández-Rosas & Carlsen 2003; Woods et
al. 2014). The high richness of epiphytes on the
inselbergs studied here (about 151 species on
111 phorophytes) may be related to the size and
architecture of Pseudobombax sp. nov. These trees
have thick, often horizontal branches, can reach a
height of 15 m and a DBH over 100 cm, and have
thick, exposed roots on the rocky surface, thus
forming an important site for epiphyte colonization.
For a precise comparison of the richness of
epiphytes in different vegetation types, we used
only studies in which the number of phorophytes
sampled was provided (see Methods). The richness
of epiphytes recorded on the inselbergs studied here
was higher than the richness of epiphytes found
on quartzite rocky outcrops in the Cerrado and
different subtypes of the Atlantic Forest, except
in Dense Ombrophilous Forest and Anthropic
Vegetation, both located in southern Brazil (Tab.
2). In comparison with rocky physiognomies in
the Cerrado, our data showed that the highest
richness occurred either when epiphytes of a
specific host tree, for example, Vellozia piresiana
L.B.Sm. (Werneck & Espírito-Santo 2002),
were considered, or when the epiphyte flora
associated with different species of phorophytes
was considered (Alves et al. 2008). In both cases,
the factor that contributed most to the lower species
richness in these environments seems to be related
to the Cerrado Domain, which supports a lower
epiphytic richness than is found in the Atlantic
Domain (Bataghin et al. 2012). However, trunks
of Vellozia are colonised by specific epiphytes of
inselbergs and rocky fields (Porembski 2005),
supporting an endemic epiphytic flora of rupestrian
ecosystems of Orchidaceae (e.g., Constantia
cipoensis Porto & Brade; Leptotes vellozicola
van den Berg et al.; Grobya cipoensis F.Barros
& Lourenço, Lepanthopsis vellozicola R.C. Mota
et al.) as well as most of the 12 species of genus
Pseudolaelia (Menini Neto et al. 2013) and
the bromeliad Vriesea vellozicola Leme & J.A.
Siqueira. On the other hand Pseudobombax sp.
Figure 6 – Venn diagram showing exclusive and shared
species among the three study areas: PL = Submontane
inselberg; PP = Montane inselberg; and PR = Upper
montane inselberg, Espírito Santo state, Brazil.

596 Couto, D.R. et al.
Rodriguésia 67(3): 583-601. 2016
nov., houses a typical epiphytic flora of the forest
ecosystems, although it is an endemic species of
inselbergs.
This marked difference in epiphytic
composition on these two phorophytes enables
understand that Pseudobambax sp.nov. is directly
responsible for the homogeneous distribution
of the population of epiphytes in the inselbergs
of the region, because even being inserted in
a completely different vegetation surrounding
matrix do not represent a barrier for distribution
of species.
The Atlantic Forest Domain, of which
these inselbergs are a part, harbors the main
centers of diversity and endemism for many
typically epiphytic families and genera (Pabst &
Dungs 1975, 1977; Smith & Downs 1977, 1979;
Martinelli et al. 2008). The marked climatic
and geomorphological diversity (Rizzini 1997)
contributes to the floral richness of this region,
which is an important depository of vascular
epiphytic flora (Kersten 2010). Comparing the
results of this study with those obtained in surveys
conducted in forest ecosystems with multiple
phorophytes, the epiphytic richness found on
Table 2 – Studies performed on vascular epiphytes in different vegetation formations in the Atlantic Forest and
Cerrado domains in Brazil, the number of phorophytes sampled, richness of epiphytes, and ratio of epiphytes to
phorophytes (Nspe = number of epiphytic species; NfA = number of sampled phorophytes), ordered by this last
column. (Physiognomy: DOF = Dense Ombrophilous Forest; MOF = Mixed Ombrophilous Forest; SSF = Seasonal
Semideciduous Forest; GF = Gallery Forest; RF = Restinga Forest; SMI = Submontane Inselberg; MI = Montane
Inselberg; UMI = Upper Montane Inselberg; QRO = Quartzite Rocky Outcrops; Antro. = Anthropic Vegetation).
Referece Phytogeographic
Domain Physiognomy Phorophyte type
Number
phorophyte
sampled
Richness of
epiphytes
Ratio
Nspe/ NfA
This study Atlantic Forest MI Pseudobombax sp. nov. 37 89 2,4
Blum et al. 2011 Atlantic Forest DOF Several 120 278 2,3
This study Atlantic Forest UMI Pseudobombax sp. nov. 37 51 1,4
Gonçalves & Waechter 2003 Atlantic Forest Antro. Ficus organensis 60 77 1,3
Kersten & Kuniyoshi 2009 Atlantic Forest MOF Several 100 114 1,1
Alves et al. 2008 Cerrado QRO Several 56 53 0,9
Giongo & Waechter 2004 Atlantic Forest GF Several 60 50 0,8
Kersten & Silva 2001 Atlantic Forest RF Several 110 77 0,7
This study Atlantic Forest SMI Pseudobombax sp. nov. 37 19 0,5
Kersten & Silva 2002 Atlantic Forest SSF Several 110 49 0,4
Fontoura et al. 2009 Atlantic Forest RF Several 110 34 0,3
Dettke et al. 2008 Atlantic Forest SSF Several 90 29 0,3
Werneck & Espírito-Santo 2002 Cerrado QRO Vellozia piresiana 98 60,1
Pseudobombax sp. nov. can be considered high
(Tab. 2). This richness is higher than in different
forest types in the Atlantic Forest Domain, such as
Dense Ombrophilous Forest (Giongo & Waechter
2004), Mixed Ombrophilous Forest (Kersten &
Silva 2002; Kersten & Kuniyoshi 2009), Seasonal
Semideciduous Forest (Dettke et al. 2008) and
Restinga Vegetation Forest (Kersten & Silva 2001;
Fontoura et al. 2009). The high richness found
on Pseudobombax sp. nov. appears to be related
to the peculiar structure of these morphological
phorophytes, which extend large roots over the
rock surface, allowing extensive colonization of
epiphytic flora.
The vegetation heterogeneity of the matrix
surrounding the three sites (Lower Montane,
Montane Semideciduous Forest and Dense
Ombrophilous Forest) is another factor that
contributes to the high richness of epiphytes.
This was also observed in other studies conducted
in areas with a wide range of vegetation types
in ecotone zones with a confluence of forest
formations (Kersten & Kuniyoshi 2009; Menini-
Neto et al. 2009; Geraldino et al. 2010), greatly
increasing the epiphytic richness. The epiphyte

Vascular epiphytes in inselbergs from the Atlantic Rainforest
Rodriguésia 67(3): 583-601. 2016
597
richness on inselbergs was lower compared to the
Dense Ombrophilous Forest in Paraná (Blum et al.
2011), where 278 species were recorded on 120
phorophytes (Tab. 2); this is the highest epiphytic
richness ever recorded in Brazil. According to
the authors, this richness was associated with the
steep altitudinal gradient, which encompassed two
distinct forest types (Montane and Submontane
Dense Ombrophilous Forest), where the high
humidity with rainfall well distributed throughout
the year provided a favorable environment for
epiphytes.
In contrast to the many reports on multiple
phorophytes, few studies is available for vascular
epiphytes richness on particular phorophyte
species. Studies conducted in the Neotropics
with specific phorophytes have highlighted
the importance of some tree species for the
maintenance and conservation of epiphytic flora
(Freiberg 1996; Werneck & Espírito-Santo 2002;
Gonçalves & Waechter 2003; Reis & Fontoura
2009; Obermüller et al. 2012). In our study, the
richness of epiphytes on Pseudobombax sp. nov.
is high compared both to a study of 60 individuals
of Ficus organensis (Miq.) Miq. in the Atlantic
Domain (Gonçalves & Waechter 2003) and to the
richness of epiphyte species on 98 individuals of
the specialist phorophyte of rocky environments,
Vellozia piresiana (Werneck & Espiríto-Santo
2002). In the first comparison, although the
relationship between the numbers of epiphytes/
phorophytes is similar (Tab. 2), the high richness
found might be related to the environments where
Pseudobombax sp. nov. and Ficus organensis were
studied. The inselbergs areas are steep and difficult
to access, which preserves the epiphytic flora
associated with this host tree; while in the area
where Ficus organensis was studied is disturbed
and are more exposed to indiscriminate extraction
of ornamental species, which depauperates the
epiphyte flora. In the second comparison, the small
size of individuals of V. piresiana (maximum 2
m high), compared with Pseudobombax sp. nov.
(maximum of 15.3 m high and up to 120 cm DBH),
influences the results, since larger phorophytes
typically support more-diverse epiphytic floras
(Woods et al. 2014) and can accommodate a larger
number of rare species.
The vascular epiphytic flora expresses itself
in different ecological categories in the relationship
established with its phorophytes (Benzing 1990).
Brazilian forest epiphyte floras contain a high
proportion of characteristic holoepiphytes (83%)
and low proportions of facultative holoepiphytes
(7%), accidental holoepiphytes (5%) (Kersten &
Silva 2002; Rogalski & Zanin 2003; Dettke et al.
2008; Buzatto et al. 2008; Kersten & Kuniyoshi
2009; Mania & Monteiro 2010; Geraldino et al.
2010; Blum et al. 2011). This composition is due
primarily to the marked environmental differences
between the canopy and the forest floor, for
example the levels of solar radiation, humidity and
temperature, which provide different habitats for
epiphyte colonization from the base of the trees to
the more-exposed branches in the canopy (Nieder
& Zotz 1998). In contrast to forest ecosystems,
in rocky environments the contribution of the
categories of facultative holoepiphytes (43%),
when evaluating the average of the Menini-Neto
et al. (2009), Alves et al. (2008), is similar to that
of the characteristic holoepiphytes (44%) in our
study. However, the characteristic holoepiphytes
were also the principal component (64%) on
Pseudobombax sp. nov., but the contribution
of accidental holoepiphytes (23%) was more
significant than that of facultative holoepiphytes
(10%). The higher proportion on inselbergs of
accidental epiphytic species that can grow both
on rocks exposed to full sun and on the trunks
and surface roots of trees, sometimes protected by
canopies, can be explained by the strong affinity
between epiphytic and rupicolous floras in the
tropics, especially in South America (Barthlott &
Porembski 2000). The similarity between these
floras relates to the xeromorphic conditions on
both trees and rocks (e.g., limitation on nutrients
and water, high sunlight irradiation, wide swings
in temperature and exposure to strong winds),
result in similar morphological and physiological
adaptations primarily to resist water scarcity,
as it directly affects the physiology of the plant
(Benzing 1990; Burke 2002).
The enormous climate and geomorphological
heterogeneity in the Atlantic Forest Domain, which
forms a wide variety of habitats (Rizzini 1979),
leads to low similarity between geographically
close floras (Menini Neto et al. 2009; Blum et
al. 2011). Some investigators have suggested that
this low epiphyte similarity is mainly due to the
different composition of the orchid family, which
is dominant in the canopy of tropical forests
(Gentry & Dodson 1987; Benzing 1990), giving
it an important role in similarity indexes of the
epiphytic flora (Kersten 2010; Blum et al. 2011).
Our results showed the existence of three
distinct floras, which differ especially between

598 Couto, D.R. et al.
Rodriguésia 67(3): 583-601. 2016
the areas influenced by montane forests (PP and
PR) and the lowest-altitude area, influenced by
Semideciduous Submontane Forest (PL) (Fig. 5).
The floristic composition of PP more closely
resembles the PR, due to the 30-shared species
(Fig. 6), and the higher richness in PP may be
related to its location at an intermediate elevation
of the Atlantic Forest Domain (730 m a.s.l.). This
relationship to elevation has been observed in
several studies of the epiphytic flora in neotropical
regions, where the highest richness is associated
with intermediate elevations, decreasing toward the
highest and lowest elevations (Gentry & Dodson
1987; Krömer et al. 2007). Another important factor
for the higher richness observed in PP may be that
the phorophytes are larger (mean dbh 46.4 cm) than
in the other areas (PL - 35.8 cm dbh and PR - 22.4
cm dbh). These differences agree with many reports
that have shown that higher epiphyte richness is
associated with large phorophytes, which normally
have a longer exposure time, area available for
colonization and microhabitat heterogeneity
(Hernández-Rosas & Carlsen 2003; Woods et al.
2014). In particular, for rocky environments, the
factors that limit the establishment of plants (e.g.,
complete or partial absence of soil, low water
retention, nutrient shortage) make the species
slow-growing and longer-lived (Larson et al.
2000), leading phorophytes of these ecosystems
support a past flora of the original forests (e.g.,
vascular epiphytes) that made contact with these
environmental elements.
As expected, PL was more dissimilar than PR
and PP, since PL lies in a region of drier climate than
the other areas and is influenced by the epiphytic
flora of the Semideciduous Submontane Forest,
which has a lower proportion of epiphytes than the
Dense Ombrophilous Forest of the Atlantic Domain
(Kersten 2010). As reported by Gentry & Dodson
(1987) that dry-climate regions are generally poor
in epiphytic species, whereas ombrophilous areas
have the most distinctive epiphyte flora (Benzing
1990). Montane forests (or Cloud forests) are
characterized by the frequent incidence of fog and
low clouds, and this characteristic promotes greater
abundance and species richness of epiphytes in the
tropics (Richards 1996).
Only three species were common to all
three areas: the bromeliads Aechmea nudicaulis,
Tillandsia stricta and the orchid Polystachya
concreta. These plants are widely distributed in
southeastern Brazil and outside Brazil, occurring in
diverse environments (Pabst & Dungs 1975; Smith
& Downs 1977, 1979). Similarly, the families that
are common to the three inselbergs (Orchidaceae,
Bromeliaceae, Polypodiaceae, Cactaceae and
Gesneriaceae) are among the epiphyte families
with wide distribution associated with the Brazilian
Atlantic Rainforest ecosystems (Kersten 2010).
Direct implications for conservation
The implications of our results for the
conservation and management of vascular
epiphytes on inselbergs lie in the importance of the
architecture and size of the host tree that supports
this vegetation. The structure of Pseudobombax
sp. nov. promotes the maintenance of epiphytic
flora, acting as a refuge for biodiversity on granitic-
gneissic inselbergs in the Atlantic Domain of
southern Espirito Santo state. The high species
richness of the vegetation mats and of most other
plant communities on eastern Brazilian inselbergs
is exceptional when compared to other tropical
areas; at last, rocky outcrops usually do not attract
much agricultural interest: they have frequently
been preserved from human impact and have kept
their refugial character (Porembski et al. 1998).
However, only one of the three inselbergs is
presently within a conservation area, indicating the
need for conservation actions for the other areas,
as well as adding the endemic species to the lists
of endangered flora of Brazil and Espírito Santo.
Although do not attract agricultural interest, these
results point to the need for stricter oversight of
the exploitation of ornamental stones in southern
Espírito Santo, where fragile ecosystems and a
unique and threatened vascular flora are being
destroyed, requiring wthout dash more-detailed
study on strategies for maintaining and restoring
these ecosystems.
In summary, our data showed that the species
richness of vascular epiphytes on Pseudobombax
sp. nov. on inselbergs in the Atlantic Forest Domain
in southeastern Brazil is higher than that found on
quartzite rocky outcrops in the Cerrado Domain
and in different forest types of the Atlantic Domain.
Exceptions were the higher richness in Dense
Ombrophilous Forest and the similar richness of
Anthropic Vegetation, both located in southern
Brazil. The most diversified ecological category
was characteristic holoepiphytes, although with
a high proportion of accidental holoepiphytes.
The inselbergs located in higher and intermediate
elevation areas were more similar to each other
and differed from the inselberg at a lower altitude,
and members of Orchidaceae and Bromeliaceae

Vascular epiphytes in inselbergs from the Atlantic Rainforest
Rodriguésia 67(3): 583-601. 2016
599
predominated. The high richness and endemism
and the number of endangered species of epiphytes
illustrate the important role of Pseudobombax
sp. nov., because of its architecture and size, in
maintaining biodiversity on the southeastern
Brazilian inselbergs. Effective monitoring and
management are needed to appropriately conserve
the unique and threatened flora of these neglected
ecosystems.
Acknowledgements
The authors express their gratitude to the
Coordenação de Aperfeiçoamento de Pessoal
de Nível Superior (CAPES), for the Master’s
scholarship granted to the first author. We are
grateful to the many taxonomists, Drs. Alice
Calvente Versieux, Elsie Franklin Guimarães,
Jefferson Guedes de Carvalho Sobrinho, Marcus
Nadruz and Pedro Bond Schwartsburd, for their
help in the identification of species. Our thanks
to Dr. Vera Lúcia de Moraes Huszar and Andrea
Ferreira da Costa (National Museum of Rio de
Janeiro), for their important suggestions and review
of this manuscript. To Hélio Q.B. Fernandes,
curator of the MBML herbarium (Museum of
Biology Prof. Mello Leitão), for granting us free
access to the collection. To Thaís F. Rodrigues and
Waldomiro P. Lopes (ICMBio), for their support
for this study in the Caparaó National Park. To Dr.
Janet Reid, for the English version. This research
was part of the Master’s dissertation of the first
author from the Postgraduate program in Forest
Sciences of the Federal University of Espírito
Santo, Brazil. The authors wish to acknowledge the
two anonymous reviewers and Marcelo F. Moro, for
his detailed and helpful comments and suggestions
to the manuscript.
References
Alves, R.J.V.; Kolbek, J. & Becker, J. 2008. Vascular
epiphyte vegetation in rocky savannas of
southeastern Brazil. Nordic Journal of Botany
26: 101-117.
Barthlott, W. & Porembski, S. 2000. Vascular plants on
inselbergs: systematic overview. In: Porembski, S.
& Barthlott, W. (eds.). Inselbergs: biotic diversity
of isoleted rock outcrops in tropical and temperate
regions. Springer-Verlag, Berlin. Pp. 103-116.
Bataghin, F.A.; Barros, F. & Pires, J.S.R. 2010.
Distribuição da comunidade de epítos vasculares
em sítios sob diferentes graus de pertubação na
Floresta Nacional de Ipanema, São Paulo, Brasil.
Revista Brasileira de Botânica 33: 501-512.
Bataghin, F.A.; Muller, A.; Pires, J.S.R.; Barros, F.;
Fushital, A.T. & Scariot, E.C. 2012. Riqueza e
estraticação vertical de epítas vasculares na
Estação Ecológica de Jataí - área de Cerrado no
Sudeste do Brasil. Hoehnea 39: 615-626.
Benzing, D.H. 1990. Vascular epiphytes. Cambridge
University Press, New York. 354p.
BFG. 2015. Growing knowledge: an overview of Seed
Plant diversity in Brazil. Rodriguésia 66: 1085-1113.
Buzatto, C.R.; Severo, B.M.A. & Waechter, J.L. 2008.
Composição florística e distribuição ecológica de
epítos vasculares na Floresta Nacional de Passo
Fundo, Rio Grande do Sul. Iheringia série Botânica
62: 231-239.
Blum, C.T.; Roderjan, C.V. & Galvão, F. 2011.
Floristic composition and altitudinal distribution
of vascular epiphytes in the ombrophilous dense
forest of the Prata Mountain Range, Morretes,
Paraná state, Brazil. Biota Neotropica. Available
at <http://www.biotaneotropica.org.br/v11n4/en/
abstract?inventory+bn00811042011>. Access on
14 January 2012.
Brummitt, R.K. & Powell, C.E. 1992. Authors of plant
names. Royal Botanical Gardens, Kew. 275p.
Burke, A. 2002. Island: matrix relationships in Nama
Karoo inselberg landscape part II. Are some
inselbergs betters sources than others? Plant
Ecology 158: 41-48.
Chiodi-Filho, C. 2009. Balanço das exportações e
importações brasileiras de rochas ornamentais em
2008. Vol. 3. Abirochas, São Paulo. 23p.
Colwell, R. K. 2013. EstimateS: statistical estimation of
species richness and shared species from samples.
Version 9. User’s Guide and application. Available
at <http://purl.oclc.org/estimates>. Access on 23
January 2014.
Couto, D.R.; Manhães, V.C.; Favoreto, F.C. & Faria,
A.P.G. 2013. Checklist of the Bromeliaceae from
Pedra dos Pontões, Mimoso do Sul, Espírito Santo,
Brazil, with four rst records for the state. Biota
Neotropica 13: 113-120.
Christenhusz, M.J.M.; Zhang, X.-C. & Schneider, H.
2011. A linear sequence of extant families and
genera of lycophytes and ferns. Phytotaxa 19: 7-54.
Dettke, G.A.; Orfrini, A.C. & Milaneze-Gutierre, M.A.
2008. Composição florística e distribuição de
epítas vasculares em um remanescente alterado
de floresta estacional semidecidual no Paraná,
Brasil. Rodriguésia 59: 859-872.
Dilcher, D.L.; Lott, T.A.; Wang, X. & Wang, Q.
2004. A history of tree canopies. In: Lowman,
M. & Rinker, H. (eds.). Forest Canopies. 2nd ed.
Elsevier Academic Press, Burlington, New York.
Pp. 118-137.
Espírito Santo. 2005. Lista estadual da flora ameaçada
de extinção. Decreto de Lei número 1.499-R de 13
de junho de 2005. Diário Ocial, Vitória, Espírito
Santo, 14 de junho de 2005.

600 Couto, D.R. et al.
Rodriguésia 67(3): 583-601. 2016
Fontoura, T.; Rocca, M.A.; Schilling, A.C. & Reinert,
F. 2009. Epífitas da floresta seca da reserva
ecológica estadual de Jacarepiá: Relações com a
comunidade arbórea. Rodriguésia 60: 171-185.
Freiberg, M. 1996. Spatial distribution of vascular
epiphytes on three emergent canopy trees in
French Guiana. Biotropica 28: 345-355.
Gentry A. & Dodson, C.H. 1987. Diversity and
biogeography of neotropical vascular epiphytes.
Annals of the Missouri Botanical Garden 74:
205-233.
Geraldino, H.C.L.; Caxambu, M.G. & Souza, D.C.
2010. Composição florística e estrutura da
comunidade de epítas vasculares em uma área
de ecótono em Campo Mourão, PR, Brasil. Acta
Botanica Brasilica 24: 469-482.
Giongo, C. & Waechter, J.L. 2004. Composição
florística e estrutura comunitária de epífitos
vasculares em uma floresta de galeria na depressão
central do Rio Grande do Sul. Revista Brasileira
de Botânica 27: 563-572.
Gonçalves, C.N. & Waechter, J.L. 2003. Aspectos
florísticos e ecológicos de epítos vasculares sobre
gueiras isoladas no norte da planície costeira
do Rio Grande do Sul. Acta Botanica Brasilica
17: 89-100.
Gotelli, N.J. & Colwell, R.K. 2011. Estimating species
richness. In: Magurran, A.E. & McGill, B.J. (eds.).
Biological diversity: frontiers in measurement and
assessment. Oxford University Press, Oxford.
Pp. 39-54.
Hammer, Ö.; Harper, D.A.T. & Ryan, P.D. 2001.
PAST: Paleontological statistics software package
for education and data analysis. Palaeontologia
Electronica 4: 1-9.
Hernández-Rosas, J.I. & Carlsen, M. 2003. Estructura
de las sinusias de plantas del dosel en un portador
(Eschweilera parviflora, Lecythidaceae) del
bosque húmedo tropical del Alto Orinoco, Estado
Amazonas, Venezuela. Ecotrópicos 16: 1-10.
Kersten, R.A. 2010. Epítos vasculares: Histórico,
participação, taxonomia e aspectos relevantes,
com ênfase na Mata Atlântica. Hoehnea 37: 9-39.
Kersten, R.A. & Kuniyoshi, Y.S. 2009. Conservação
das florestas na Bacia do Alto Iguaçu, Paraná -
avaliação da comunidade de epítas vasculares
em diferentes estágios serais. Floresta 39: 51-66.
Kersten, R.A. & Silva, S.M. 2001. Composição
florística e distribuição espacial de epífitos
vasculares em floresta de planície litorânea da
Ilha do Mel, Paraná, Brasil. Revista Brasileira de
Botânica 24: 213-226.
Kersten, R.A. & Silva, S.M. 2002. Floristica e estrutura
do componente epifítico vascular em floresta
ombróla mista aluvial do rio barigui, Paraná,
Brasil. Revista Brasileira de Botânica 25: 259-267.
Krömer, T.; Kessler, M.; Gradstein, S.R. & Acebey,
A. 2005. Diversity patterns of vascular epiphytes
along an elevational gradient in the Andes. Journal
of Biogeography 32: 1799-1809.
Krömer, T.; Kessler, M. & Gradstein, S.R. 2007.
Vertical stratication of vascular epiphytes in
submontane and montane forest of the Bolivian
Andes: the importance of the understory. Plant
Ecology 189: 261-278.
Küper, W.; Kreft, H.; Nieder, J.; Köster, N. & Barthlott,
W. 2004. Large-scale diversity patterns of vascular
epiphytes in Neotropical montane rain forests.
Journal of Biogeography 31: 1477-1487.
Larson, D.W.; Matthes, U. & Kelly, P.E. 2000. Cliff
Ecology: pattern and process in cliff ecosystems.
Cambridge University Press, Cambridge. 340p.
Mania, L.F. & Monteiro, R. 2010. Florística e ecologia
de epítas vasculares em um fragmento de floresta
de restinga, Ubatuba, SP, Brasil. Rodriguésia 61:
705-713.
Martinelli, G. 2007. Mountain biodiversity in Brazil.
Revista Brasileira de Botânica 30: 587-597.
Martinelli, G.; Magalhães, C.V.; Gonzalez, M.;
Leitman, P.; Piratininga, A.; Costa, A.F. & Forzza,
R.C. 2008. Bromeliaceae da Mata Atlântica
brasileira: Lista de espécies, distribuição e
conservação. Rodriguésia 59: 209-258.
Menini Neto, L.; Forzza, R.C. & Zappi, D. 2009.
Angiosperm epiphytes as conservation
indicators in forest fragments: A case study from
southeastern Minas Gerais, Brazil. Biodiversity
and Conservation 18: 3785-3807.
Menini Neto, L.; van den Berg, C. & Forzza,
R.C. 2013. Taxonomic revision of Pseudolaelia
Porto & Brade (Laeliinae, Orchidaceae). Acta
Botânica Brasilica 27: 418-435.
MMA - Ministério do Meio Ambiente. 2014. Portaria
No 443, de 17 de dezembro de 2014 - lista nacional
ocial de espécies da flora ameaçadas de extinção.
Diário Ocial da União - seção 1, No 245, 18 de
dezembro de 2014. Pp. 110-121.
Mori, S.A.; Silva, L.A.M.; Lisboa, G. & Coradini,
L. 1989. Manual de manejo do herbário
fanerogâmico. Centro de Pesquisa do Cacau,
Ilhéus. 104p.
Nieder, J. & Zotz, G. 1998. Methods of analyzing
the structure and dynamics of vascular epiphyte
communities. Ecotropica 4: 33-39.
Obermüller, F.A.; Silveira, M.; Salimon, C.I.
& Daly, D.C. 2012. Epiphytic (including
hemiepiphytes) diversity in three timber species
in the southwestern Amazon, Brazil. Biodiversity
and conservation 21: 565-575.
Pabst, G.F.J. & Dungs, F. 1975. Orchidaceae Brasilienses
Vol. 1. Kurt Schmersow, Hildesheim. 408p.
Pabst, G.F.J. & Dungs, F. 1977. Orchidaceae Brasilienses
Vol. 2. Kurt Schmersow, Hildesheim. 418p.
Perry, D.R. 1978. A method of access into the crowns
of emergent and canopy trees. Biotropica 10:
155-157.

Vascular epiphytes in inselbergs from the Atlantic Rainforest
Rodriguésia 67(3): 583-601. 2016
601
Porembski, S. 2005. Epiphytic orchids on arborescent
Velloziaceae and Cyperaceae: Extremes of
phorophyte specialisation. Nordic Journal of
Botany 23: 505-513.
Porembski, S. 2007. Tropical inselbergs: habitat types,
adaptive strategies and diversity patterns. Revista
Brasileira de Botânica 30: 579-586.
Porembski, S.; Martinelli, G.; Ohlemuller, R. & Barthlott,
W. 1998. Diversity and ecology of saxicolous
vegetation mats on the inselbergs in the Brazilian
Atlantic rainforest. Diversity and Distributions 4:
107-119.
Prado, J. et al. 2015. Diversity of ferns and lycophytes
in Brazil. Rodriguésia 66: 1-11.
Richards, P.W. 1996. The Tropical Rain Forest. 2nd ed.
Cambridge University Press, Cambridge. 600p.
Rizzini, C.T. 1979. Tratado de togeograa do
Brasil. Vol. 2. Hucitec, São Paulo. 374p.
Reis, J.R.M. & Fontoura, T. (2009). Diversidade
de bromélias epífitas na Reserva Particular do
Patrimônio Natural Serra do Teimoso - Jussari, BA.
Biota Neotropica 9: 073-079.
Rogalski, J.M. & Zanin, E.M. 2003. Composição
florística de epífitos vasculares no estreito de
Augusto César, floresta estacional decidual do Rio
Uruguai, RS. Revista Brasileira de Botânica 26:
551-556.
Simonelli, M. & Fraga, C.N. 2007. Espécies da flora
ameaçadas de extinção no Estado do Espírito Santo.
IPEMA, Vitória. 144p.
Smith, A.R.; Pryer, K.M.; Schuettpelz, E.; Korall, P.;
Schneider, H. & Wolf, P.G. 2006. A classication
for extant ferns. Taxon 55: 705-731.
Smith, L.B. & Downs, R.J. 1977. Bromeliaceae, sub-
family Tillandsioideae. Flora neotropica monograph
14. Hafner Press, New York. Pp. 663-1492.
Smith, L.B. & Downs, R.J. 1979. Bromeliaceae, sub-
family Bromelioideae. Flora neotropica monograph
14. Hafner Press, New York. Pp. 1493-2142.
The Angiosperm Phylogeny Group - APG III. 2009.
An update of the Angiosperm Phylogeny Group
classication for the orders and families of flowering
plants: APG III. Botanical Journal of the Linnean
Society 61: 105-121.
Veloso, H.P.; Rangel Filho, A.L.R. & Lima, J.C.A. 1991.
Classificação da vegetação brasileira, adaptada
a um sistema universal. IBGE, Departamento de
Recursos Naturais e Estudos Ambientais, Rio de
Janeiro. 124p.
Werneck, M.S. & Espírito-Santo, M.M. 2002. Species
diversity and abundance of vascular epiphytes on
Vellozia piresiana in Brasil. Biotropica 34: 51-57.
Woods, C.L.; Cardelús, C.L. & DeWalt, S.J. 2014.
Microhabitat associations of vascular epiphytes
in a wet tropical forest canopy. Journal of
Ecology. Journal of Ecology 103: 421-430. DOI:
10.1111/1365-2745.12357
Zotz, G. 2013. The systematic distribution of vascular
epiphytes: a critical update. Botanical Journal of the
Linnean Society 171: 453-481.
Artigo recebido em 09/06/2015. Aceito para publicação em 24/01/2016.