O R I G I N A L P A P E R
Angiosperm epiphytes as conservation indicators
in forest fragments: A case study from southeastern
Minas Gerais, Brazil
Luiz Menini NetoÆ Rafaela Campostrini Forzza Æ Daniela Zappi
Received: 26 September 2008 / Accepted: 18 June 2009 / Published online: 1 July 2009 Ó Springer Science+Business Media B.V. 2009
Abstract Epiphytes play an important role in the flora and ecology of the tropical
regions. Most floristic studies within the state of Minas Gerais focus on terrestrial, woody plant diversity, but this is a different approach, looking at epiphytic angiosperms in three highland areas in Southeastern Minas Gerais, namely Mata do Bau´ (MB), Reserva Biol-o´gica da Represa do Grama (RBRG) and Parque Estadual de Ibitipoca (PEI). Regular collections were performed in these sites between 1999 and 2007, complemented by herbarium records for PEI, and 181 species of epiphytic angiosperms were recorded in 66 genera, within 12 families. Orchidaceae, with 89 species, was by far the largest, and the most species rich genera were Peperomia (Piperaceae) and Pleurothallis s.l. (Orchida-ceae), with 12 species each. Similarity analysis has shown a closer relationship between MB and RBRG, both composed by seasonal semideciduous forest, however, Jaccard (0.163) index are low. A similarity analysis including other 21 areas of southeastern and southern Brazil revealed strong influence of sazonality, vegetation type and altitude in the composition of the epiphytic flora, and a relative independence regarding the geographic proximity of the areas sampled. From the conservation standpoint, 30 species recorded for this work appear in the red list for the state of Minas Gerais, under different conservation categories. The low similarity indices obtained between the studied areas underline the importance of the conservation of each one of the remaining forest fragments in Minas
L. Menini Neto (&)
Centro de Ensino Superior de Juiz de Fora, Campus Arnaldo Janssen, Luz Interior 345, Juiz de Fora, MG 36030-776, Brazil
e-mail: menini_neto@hotmail.com L. Menini Neto R. C. Forzza
Escola Nacional de Botaˆnica Tropical/Jardim Botaˆnico do Rio de Janeiro, Pacheco Lea˜o 915, Rio de Janeiro, RJ 22460-030, Brazil
e-mail: rafaela@jbrj.gov.br D. Zappi
HLAA, Royal Botanic Gardens, Kew TW9 3AB, UK DOI 10.1007/s10531-009-9679-2
Gerais, as their relative geographical proximity does not necessarily mean that their epiphytic flora is similar.
Keywords Atlantic forest Montane forest Seasonal semi-deciduous forest
Similarity analysis Southeastern Brazil Southern Brazil
Resumo Angiospermas epı´fitas como indicadores para conservac¸a˜o em fragmentos
flo-restais. Um estudo de caso do sudeste de Minas Gerais, Brasil. Epı´fitas desempenham um importante papel na flora e ecologia de regio˜es tropicais. A maioria dos estudos florı´sticos no estado de Minas Gerais teˆm como foco a diversidade das plantas arbo´reas, sendo apresentada aqui uma abordagem diferente, visando as angiospermas epı´fitas de treˆs a´reas de altitude no sudeste de Minas Gerais, Mata do Bau´ (MB), Reserva Biolo´gica da Represa do Grama (RBRG) e Parque Estadual de Ibitipoca, (PEI). Coletas regulares foram realizadas nestas localidades entre 1999 e 2007, complementadas por registros de herba´rio para o PEI, sendo registradas 181 espe´cies de angiospermas epı´fitas, distribuı´das em 66 geˆneros e 12 famı´lias. Orchidaceae, com 89 espe´cies, foi a mais rica, enquanto os geˆneros com o maior nu´mero de espe´cies foram Peperomia (Piperaceae) e Pleurothallis s.l. (Orchidaceae), com 12 espe´cies cada. Ana´lises de similaridade mostraram uma relac¸a˜o mais pro´xima entre MB e RBRG, ambas compostas por floresta estacional semidecidual, no entanto, o ı´ndice de Jaccard (0,163) foi baixo. Uma ana´lise de similaridade incluindo outras 21 a´reas do sudeste e sul do Brasil revelou forte influeˆncia da sazonalidade, tipo de vegetac¸a˜o e altitude na composic¸a˜o da flora epifı´tica e uma relativa independeˆncia no que tange a proximidade geogra´fica das a´reas amostradas. Em relac¸a˜o a` conservac¸a˜o, 30 espe´cies registradas neste trabalho aparecem citadas na lista vermelha para o estado de Minas Gerais, sob diferentes categorias de conservac¸a˜o. Os baixos ı´ndices de similaridade obtidos entre as a´reas estudadas destacam a importaˆncia da conservac¸a˜o de cada um dos fragmentos florestais remanescentes em Minas Gerais, bem como sua relativa proximidade geogra´fica na˜o necessariamente significa que sua flora epifı´tica seja similar.
Palavras Chave Floresta atlaˆntica Floresta montana Floresta estacional semidecidual
Ana´lise de similaridade Sudeste do Brasil Sul do Brasil
Abbreviations AA Anthropic area c. Circa CA ‘‘Campo de altitude’’ CER ‘‘Cerrado’’ CR ‘‘Campo rupestre’’
DEF Dense evergreen forest
Disp Dispersal syndrome
DSF Deciduous seasonal forest
EC Ecological category
E.E. Ecological Station
GF Gallery forest
HeP Primary hemiepiphyte
HeS Secondary hemiepiphyte
HLC Characteristic holoepiphyte
MB Mata do Bau´
MG Minas Gerais State
P.E. State Park
PEI Parque Estadual de Ibitipoca
P.N. National Park
PR Parana´ State
RBRG Reserva Biolo´gica da Represa do Grama
RE ‘‘Restinga’’ or coastal forest
ReBio Biological Reserve
RJ Rio de Janeiro State
RS Rio Grande do Sul State
SEF Subtropical evergreen forest
SSF Semideciduous Seasonal Forest
SP Sa˜o Paulo State
Introduction
Brazil is one of the leading countries in terms of the size of its flora (Giulietti et al.2005)
and the state of Minas Gerais is a major contributor towards Brazilian biodiversity
(Mendonc¸a and Lins2000). Knowledge regarding this state’s flora is proportionately low,
and floristic surveys have tended to concentrate on woody plants (Oliveira-Filho and
Fontes2000; Franc¸a and Stehmann2004), while herbaceous species have been
compre-hensively surveyed only for highland areas with open vegetation, known as ‘‘campo
ru-pestre’’ (Giulietti et al.1987; Peron1989; Pedralli et al.1997; Pirani et al.2003; Viana and
Lombardi2007; Alves and Kolbek2009).
Epiphytes represent approximately 10% of all vascular plants, and are distributed in over 80 plant families with marked richness and abundance in tropical regions, especially
in the Neotropics (Gentry and Dodson 1987). Mainly herbaceous in habit, they are
con-centrated in the families Orchidaceae, Araceae and Bromeliaceae amongst Angiosperms,
and Polypodiaceae, Aspleniaceae and Hymenophyllaceae amongst ferns (Kress 1986;
Benzing 1990). In terms of species richness, around 80% of epiphytic species occur in
Orchidaceae, Bromeliaceae, Polypodiaceae and Araceae (Gentry and Dodson1987). The
epiphytic community supplies the local fauna with diverse resources, such as fruits, nectar, pollen and water, and maintains fundamental specialized microhabitats for the
establish-ment and survival of other organisms (Benzing1990; Ingram and Nadkarni1993).
Only two previous studies involving epiphytes in Minas Gerais exist, both focused on
epiphytic communities in ‘‘campo rupestre’’ vegetation (Werneck and Espı´rito-Santo2002;
Alves et al.2008). Most previous research on this topic has focused on the southern states
of Brazil (Waechter1998; Dittrich et al.1999; Kersten and Silva2002; Borgo and Silva
2003; Gonc¸alves and Waechter2003; Rogalski and Zanin 2003; Giongo and Waechter
2004; Gaiotto and Acra2005; Kersten and Kuniyoshi2009), with only a few in
south-eastern Brazil: Sa˜o Paulo (Dislich and Mantovani1998; Piliackas et al.2000) and Rio de
Janeiro (Fontoura et al.1997).
The three studied areas, Mata do Bau´ (MB), Reserva Biolo´gica da Represa do Grama (RBRG) and Parque Estadual de Ibitipoca (PEI), feature in the atlas of priority areas for
and ‘special’ (PEI) status, these being the highest levels used to categorize the importance of regional flora in terms of the conservation of its species richness. The localities are found within Brazilian biodiversity hotspots, the ‘‘Cerrado’’ (MB) and the Atlantic forest (RBRG and PEI), where high biodiversity and endemism are paired with accelerated
habitat loss (Myers et al.2000), supporting the need to investigate their biological diversity
as a whole and to promote their conservation.
This qualitative survey of epiphytic angiosperms in three areas of montane and upper montane forest in Minas Gerais uses the epiphytic angiosperm flora to compare the sim-ilarity between the studied areas and 21 others in Southeastern and Southern Brazil, contributing towards the knowledge of the Flora of Minas Gerais and its conservation.
Study areas
The three study areas (Mata do Bau´—MB, Reserva Biolo´gica da Represa do Grama— RBRG and Parque Estadual de Ibitipoca—PEI) are located in southeastern Minas Gerais,
relatively close to each other (between 70 and 110 km, within an area of c. 2,900 km2)
(Fig.1). The climate is classified as Cwb, mesothermic with clearly defined seasons
(CETEC1983). Mata do Bau´ lies in the seasonal savanna ecosystem known as ‘‘Cerrado’’
(Menini Neto et al. 2004b), while RBRG and PEI are part of Brazil’s Atlantic forest
(Menini Neto et al.2004a,2007).
Mata do Bau´ (MB)—this private reserve in the Municipality of Barroso, in the district
of Campo das Vertentes (c. 21°110S and 43°560W), covers approximately 10 ha of seasonal
semi-deciduous montane and gallery forests, at c. 900 m alt., with mean temperature of
Reserva Biolo´gica da Represa do Grama (RBRG)—within the ‘Zona da Mata’ (‘forest
zone’) of Minas Gerais, in the Municipality of Descoberto (c. 21°250S–42°560W),
repre-sents 263.8 ha of seasonal semi-deciduous montane and gallery forests, at c. 750 m alt., with mean temperature of approx. 21°C and rainfall around 1,600 mm/year (Menini Neto
et al.2004b).
Parque Estadual de Ibitipoca (PEI)—this State Park, also within the ‘Zona da Mata’ of Minas Gerais, although considered as part of the highland area known as Serra da Man-tiqueira, lies between the municipalities of Lima Duarte and Santa Rita de Ibitipoca (c.
21°400–21°440S and 43°520–43°550W), comprising 1923.5 ha. Altitude ranges between
1,200 and 1,784 m. It supports a complex vegetation mosaic known as ‘‘campo rupestre’’, including mostly open highland vegetation on quartzitic/arenitic rock, but also a varied combination of gallery forest along rivers, evergreen upper montane forest and seasonal montane forest groves (‘‘capo˜es de mata’’), between 1,200 and 1,400 m, and cloud forest above 1,500 m. The mean temperature is approx. 18.9°C and rainfall is around 2,200 mm/
year (Menini Neto et al. 2007). The most important forested areas within PEI are two
fragments of evergreen upper montane forest covering 94 and 30 ha (Fontes1997).
Methods
Monthly plant collections were carried out in RBRG (between August 1999 and August 2002), MB (between February 2001 and June 2003) and PEI (between October 2003 and December 2007), targeting fertile specimens of all flowering plants in selective walks in the three areas. Data were collected in the field, and herbarium specimens were databased and deposited at CESJ and RB herbaria. Former collections from PEI, dating back to the 1970s, from herbaria BHCB, CESJ, HB, RB and VIC, were also included in the database. Herbarium acronyms are according Holmgren et al. (1990). Threatened species cited in the
Minas Gerais Red List (Biodiversitas2007) were highlighted and symbols were added for
different threat categories (Table1).
The ecological categories were classified according to Benzing (1990) as characteristic holoepiphyte (HLC), facultative holoepiphyte (HLF) and hemiepiphyte (divided in primary hemiepiphyte—HeP and secondary hemiepiphyte—HeS). The dispersal syndromes were classified in two categories, anemochory (wind dispersal) and zoochory (animal dispersal)
(Table1).
Two similarity analyses (using Jaccard’s coefficient with UPGMA to cluster
similari-ties) were carried out with PAST v. 1.89 software (Hammer et al.2001). The cophenetic
values were calculated to test strength of the fit between the clusters in the dendrograms and the similarity index matrix, generating 1,000 permutations in order to stabilize the data matrix.
The first analysis used a similarity matrix combining the three species lists from this
survey with those from 21 other studies (Fig.1), focusing on epiphytes or including/
highlighting epiphytic and hemiepiphytic species among their data (Table2). A total of 24
floristic lists and 618 species were included in this analysis. The second analysis used the same 24 floristic lists but excluded the rare species (species with only one occurrence) in a matrix with 301 species.
Amongst these, the lists from Parque Nacional do Itatiaia and Parque Nacional da Serra
dos O´ rga˜os (both in Rio de Janeiro state) were complemented with database data (RB
Table 1 Angiosperm species list of epiphytes and hemiepiphytes recorded at Mata do Bau´ (MB), Reserva Biolo´gica da Represa do Grama (RBRG) and Parque Estadual de Ibitipoca (PEI), Minas Gerais, Brazil
Species Area Habitat EC Disp Voucher specimens
MB RBRG PEI ARACEAE
Anthurium boudetii Nadruz X GF HeS Zo Temponi 397 (@)
A. contum Schott. X X SSF/GF HeS Zo Forzza 1750 (?),
Temponi 400 (@)
A. leonii E.G.Gonc¸. X GF HLF Zo Forzza 4270 (@)
A. minarum Sakuragui & Mayo
X GF HeS Zo Temponi 390 (@)
A. pentaphyllum (Aubl.) G. Don
X SSF HeS Zo Forzza 1729 (?)
A. scandens (Aubl.) Engl. X X SSF/GF HLC Zo Almeida 14 (?), Forzza 2663 (@)
A. solitarium Schott X SSF HLF Zo Almeida 9 (?)
Anthurium sp. X SSF HLC Zo Castro 539 (?)
Heteropsis salicifolia Kunth X SSF HeS Zo Forzza 1697 (?) Monstera adansonii Schott X SSF HeS Zo Faria s.n. (CESJ 31035) Philodendron
appendiculatum Nadruz & Mayo
X X SSF/DEF/GF HeS Zo Almeida 13 (?), Forzza 3638 (@)
P. bipinnatifidum Schott X GF HeS Zo Temponi 410 (@)
P. cordatum Kunth ex Schott X SSF HeS Zo Assis 418 (?)
P. curvilobum Schott X SSF HeS Zo Forzza 1698 (?)
P. hastatum K.Koch & Sellow?
X SSF HeS Zo Forzza 1699 (?)
P. minarum Engl. X GF HeS Zo Forzza 2653 (@)
P. ornatum Schott X SSF HeS Zo Almeida 32 (?)
P. propinquum Schott X X X SSF/DEF/ GF HeS Zo Forzza 1935 (?), Sakuragui 1638 (@), Temponi 398 (@) P. speciosum Schott ex
Endl.
X SSF HeS Zo Almeida 18 (?)
Rhodospatha latifolia Poepp. X SSF HeS Zo Almeida 17 (?) BEGONIACEAE
Begonia angulata Vell. X DEF HeS An Temponi 393 (@)
B. fruticosa A. DC. X SSF HeS An Faria s.n. (CESJ 34482)
Begonia sp. X DEF HLF An Forzza 4287 (@)
BROMELIACEAE Aechmea bromeliifolia
(Rudge) Baker
X SSF HLC Zo Assis 180 (?)
A. nudicaulis (L.) Griseb. X SSF HLF Zo Monteiro 13 (@) A. ramosa Mart. ex Schult. F. X SSF HLF Zo Almeida 5 (?) Billbergia alfonsijoanis Reitz X SSF HLC Zo Martinelli 15283 (@)
B. euphemiae E. Morren X SSF HLC Zo Almeida 11 (?)
Table 1 continued
Species Area Habitat EC Disp Voucher specimens
MB RBRG PEI
B. zebrina (Herb.) Lindl. X X SSF HLC Zo Assis 19 (?), Forzza 2052 (?) Neoregelia farinosa (Ule)
L.B.Sm.€
X SSF HLC Zo Almeida 22 (?)
N. ibitipocensis (Leme) Leme
X ? HLF Zo Forzza 3338 @
N. lymaniana R. Braga & Sucre§ X ? HLC Zo Leme 1478 (#) N. oligantha L.B.Sm.§ X GF HLF Zo Monteiro 38 (@) Nidularium ferdinandocoburgii Wawra X GF HLF Zo Martinelli 15290 (@)
N. longiflorum Ule? X SSF HLC Zo Almeida 27 (?)
N. marigoi Leme? X GF HLF Zo Forzza 3232 @
Portea petropolitana (Wawra) Mez
X SSF HLC An Castro 563 (?)
Quesnelia arvensis (Vell.) Mez
X SSF HLF Zo Almeida 8 (?)
Q. augusto-coburgii Wawra X SSF HLF Zo Almeida 20 (?) Racinaea aerisincola (Mez)
Spencer & L.B.Sm.
X GF HLC An Sucre 7147 (@)
Tillandsia gardneri (Vell.) Mez
X X SSF HLF An Assis 118 (?), Sucre
7184 (@)
T. geminiflora Brongn. X X X SSF/GF HLC An Assis 20 (?), Forzza 1695 (?), Krieger s.n. (CESJ 8595)
T. tenuifolia L. X X SSF/DEF/GF HLF An Assis 11 (?), Andrade 1131 (*)
T. recurvata (L.) L. X X SSF HLC An Assis 28 (?), Sucre 7234 (@)
T. stricta Sol. ex Sims X X SSF/GF/CR HLC An Faria s.n. (CESJ 34138), Caˆmara s.n. (CESJ 9405)
T. usneoides (L.) L. X X X SSF HLC An Assis 397 (?), Almeida 34 (?) Forzza 3022 (@) Vriesea bituminosa L.B.Sm. X SSF/GF/DEF HLF An Monteiro 28 (@)
V. carinata Wawra X ? HLC An Paula s.n. (VIC 26470)
V. friburgensis Mez X SSF/GF/CR HLF An Martinelli 15281 (@) V. gigantea Mart. ex Schult.
F.
X SSF HLC An Castro 463 (?)
V. gradata (Baker) Mez X SSF HLC An Castro 146 (?)
V. guttata Linden & Andre´ X GF HLC An Monteiro 25 (@) V. heterostachys (Baker)
L.B.Sm.
X DEF/GF HLF An Martinelli 15301 (@) V. longicaulis (Baker) Mez X DEF/GF HLF An Martinelli 15314 (@) V. pauperrima E. Pereira X SSF HLC An Forzza 2205 (?)
Table 1 continued
Species Area Habitat EC Disp Voucher specimens
MB RBRG PEI
V. penduliflora L.B.Sm.? X GF/CR HLF An Leme 1476 (#)
V. scalaris E. Morren X SSF HLC An Forzza 2188 (?)
Wittrockia gigantea (Baker) Leme X DEF/GF HLC Zo Martinelli 15313 (@) CACTACEAE Epiphyllum phyllanthus (L.) Haw. X SSF HLC Zo Forzza 2957 (?)
Hatiora salicornioides (Haw.) Britton & Rose
X DEF/CR HLF Zo Bru¨gger s.n. (CESJ 21541) Hylocereus setaceus
(Salm-Dyck) Ralf Bauer
X X SSF HLF Zo Assis 300 (?); Forzza
2062 (?) Lepismium cruciforme (Vell.)
Miq. X SSF HLC Zo Forzza 2044 (?) L. houlletianum (Lem.) Barthlott X ? HLC Zo Oliveira s.n. (CESJ 24194) Rhipsalis elliptica G. Lindb. ex
K. Schum.
X SSF HLC Zo Forzza 2057 (?)
R. floccosa Salm-Dyck ex Pfeiff.
X GF/CR HLC Zo Krieger s.n. (CESJ 8589) R. juengeri Barthlott & N.P.
Taylor
X DEF/GF HLC Zo Krieger s.n. (CESJ 8594) R. lindbergiana K. Schum. X SSF HLC Zo Forzza 2920 (?)
R. pulchra Loefgr. X GF HLC Zo Krieger s.n. (9269)
R. russellii Britton & Rose? X GF HLC Zo Forzza 3226 (@) Schlumbergera opuntioides
(Loefgr. & Duse´n) D.R. Hunt?
X GF HLF Zo Forzza 3180 (@)
CYCLANTHACEAE Asplundia brachypus (Drude)
Harling
X SSF HeS Zo Forzza 1743 (?)
GESNERIACEAE Nematanthus crassifolius
(Schott) Wiehler?
X X SSF/DEF HLC Zo Forzza 1738 (?), Forzza 4274 (@)
N. lanceolatus (Poir.) Chautems€
X SSF HLF Zo Castro 67 (?)
Sinningia magnifica (Otto & A.Dietr.) Wiehler€
X GF HLF An Forzza s.n. (CESJ 27323) GRISELINIACEAE
Griselinia ruscifolia (Goy) Taub.
X ? HeP Zo Krieger s.n. (14340) MARCGRAVIACEAE
Marcgravia polyantha Delp. X SSF HeS Zo Castro 100 (?)
Marcgravia sp. X SSF HeS Zo Franco 64 (?)
MELASTOMATACEAE
Table 1 continued
Species Area Habitat EC Disp Voucher specimens
MB RBRG PEI ORCHIDACEAE
Bifrenaria vitellina Lindl.§ X GF HLC An Forzza 8 (?) Bulbophyllum cribbianum
Toscano
X CR HLF An Forzza 10 (?)
B. glutinosum (Barb. Rodr.) Cogn.
X SSF HLC An Menini Neto 125 (?) B. granulosum Barb. Rodr. X GF HLC An Menini Neto 107 (?)
B. pabstii Garay X SSF HLC An Assis 788 (?)
B. regnellii Rchb. f. X SSF HLC An Menini Neto 124 (?)
Campylocentrum aromaticum Barb. Rodr. X SSF HLC An Assis 350 (?) C. linearifolium Schltr. ex Mansf. X X SSF HLC An Assis 470 (?), Assis 878 (?)
C. micranthum (Lindl.) Rolfe X SSF HLC An Assis 815 (?) C. neglectum (Rchb. f. &
Warm.) Cogn.
X GF HLC An Menini Neto 28 (?)
C. robustum Cogn. X X SSF HLC An Assis 257 (?), Menini
Neto 193 (?) Capanemia thereziae Barb.
Rodr.
X SSF HLC An Assis 819 (?)
Catasetum cernuum (Lindl.) Rchb. f.
X SSF HLF An Almeida 23 (?)
Cattleya bicolor Lindl.? X SSF HLC An Menini Neto 178 (?) C. loddigesii Lindl.§ X X SSF HLC An Assis 269 (?), sem
coletor (CESJ 27534) Centroglossa macroceras Barb.
Rodr.
X DEF HLC An Forzza 54 (?)
Comparettia coccinea Lindl. X X SSF HLC An Assis 469 (?), Faria s.n. (CESJ 31100) Dichaea cogniauxiana Schltr. X GF HLC An Forzza 21 (?) Encyclia patens Hook. X X X SSF/DEF HLF An Assis 691 (?), Salimena
s.n. (CESJ 31246), Menini Neto 165 (?) Epidendrum armeniacum
Lindl.
X SSF HLC An Menini Neto 175 (?) E. chlorinum Barb. Rodr. X GF HLC An Menini Neto 171 (?) E. cristatum Ruiz & Pav. X SSF HLF An Assis 839 (?) E. densiflorum Hook. X X SSF HLF An Assis 849 (?), Menini
Neto 2 (?)
E. difforme Lindl. X SSF HLC An Menini Neto 97 (?)
E. ochrochlorum Barb. Rodr.§
X DEF HLC An Forzza 36 (?) E. paranaense Barb. Rodr. X DEF/GF HLF An Forzza 83 (?) E. rigidum Jacq. X X SSF/GF HLF An Assis 847 (?), Menini
Table 1 continued
Species Area Habitat EC Disp Voucher specimens
MB RBRG PEI Eurystyles actinosophila (Barb. Rodr.) Schltr. X X SSF HLC An Assis 808 (?), Castro 125 (?) E. cogniauxii (Kraenzl.) Pabst X GF HLC An Forzza 61 (?)
Gomesa glaziovii Cogn. X GF HLC An Forzza 51 (?)
G. recurva Lodd. X X X SSF/DEF HLF An Menini Neto 17 (?), Faria s.n. (CESJ 31067), Forzza 38 (?) G. sessilis Barb. Rodr. X SSF HLC An Menini Neto 7 (?) Grobya amherstiae Lindl. X SSF HLC An Forzza 26 (?) Hadrolaelia coccinea
(Lindl.) Chiron & V.P. Castro§
X SSF/CR HLF An Forzza 17 (?)
Huntleya meleagris Lindl. X SSF HLC An Almeida 26 (?) Isabelia violacea (Lindl.)
Van den Berg & M.W.Chase
X CR HLF An Salimena-Pires s.n. (CESJ 24458)
I. virginalis Barb. Rodr. X SSF HLC An Menini Neto 47 (?) Isochilus linearis (Jacq.) R.
Br. X X SSF HLC An Assis 647 (?), Forzza 40 (?) Lankesterella gnomus (Kraenzl.) Hoehne X GF HLC An Menini Neto 139 (?) Masdevallia infracta Lindl. X DEF HLC An Menini Neto 173 (?) Maxillaria acicularis Herb.
ex Lindl.
X SSF HLC An Forzza 35 (?)
M. madida Lindl. X CR HLF An Forzza 47 (?)
M. notylioglossa Rchb. f. X SSF HLC An Menini Neto 119 (?) M. ochroleuca Lodd. ex
Lindl.
X SSF HLC An Forzza 71 (?) M. valenzuelana (A. Rich.)
Nash
X SSF HLF An Assis 848 (?)
Notylia aff. sagittifera (Kunth) Link, Klotzsch & Otto
X SSF HLC An Menini Neto 16 (?)
Octomeria alpina Barb. Rodr. X CR/GF HLF An Forzza 77 (?)
O. aff. diaphana Lindl. X DEF HLC An Forzza 89 (?)
O. grandiflora Lindl. X GF HLC An Forzza 63 (?)
O. aff. rubrifolia Barb. Rodr. X SSF/CR HLC An Sousa s.n. (BHCB 14766) O. wawrae Rchb. f. ex
Wawra
X SSF/CR HLC An Forzza 41 (?) Oncidium ciliatum Lindl. X SSF HLC An Assis 31 (?)
O. divaricatum Lindl. X DEF HLC An Forzza 2190 (@)
O. gardneri Lindl. X SSF HLC An Assis 455 (?)
O. gravesianum Rolfe X SSF/DEF HLC An Forzza 23 (?)
Table 1 continued
Species Area Habitat EC Disp Voucher specimens
MB RBRG PEI
O. longipes Lindl. X SSF HLC An Menini Neto 163 (?)
O. pubes Lindl. X SSF HLC An Assis 266 (?)
O. pumilum Lindl. X SSF HLC An Assis 353 (?)
O. truncatum Pabst X SSF HLC An Menini Neto 95 (?)
Pleurothallis cryptophoranthoides Loefgr.§ X DEF HLC An Sousa s.n. (BHCB 16647) P. heterophylla (Barb. Rodr.) Cogn. X SSF HLC An Andrade 1160 (*) P. hypnicola Lindl. X X SSF/DEF HLC An Forzza 2187 (?), Menini
Neto 134 (?)
P. luteola Lindl. X DEF HLC An Menini Neto 158 (?)
P. malachantha Rchb. f.? X SSF/DEF HLC An Sousa s.n. (BHCB 9832) P. marginalis Rchb. f. X SSF HLC An Menini Neto 162 (?)
P. pubescens Lindl. X SSF HLC An Menini Neto 18 (?)
P. quartzicola (Barb. Rodr.) Cogn.
X DEF HLC An Menini Neto 114 (?)
P. recurva Lindl. X DEF HLC An Menini Neto 236 (?)
P. rubens Lindl. X SSF/DEF/CR HLF An Forzza 78 (?)
P. saundersiana Rchb. f. X SSF HLC An Forzza 32 (?) P. tricarinata Poepp. & Endl. X DEF HLC An Menini Neto 118 (?) Polystachya estrellensis
Rchb. f.
X X SSF HLF An Assis 188 (?), Almeida 6
(?)
P. hoehneana Kraenzl.? X SSF HLC An Forzza 37 (?)
P. micrantha Schltr.? X SSF HLC An Assis 193 (?)
Promenaea xanthina Lindl. X DEF HLC An Eiterer s.n. (CESJ 25549) Prosthechea allemanoides
(Hoehne) W.E.Higgins
X SSF/CR HLF An Forzza 55 (?) P. vespa (Vell.) W.E.Higgins X SSF/CR HLF An Forzza 67 (?) Rodrigueziella gomezoides
(Barb. Rodr.) Berman
X GF HLC An Sousa s.n. (BHCB 16117) Scaphyglottis modesta Schltr. X SSF HLF An Forzza 4 (?)
Scuticaria aff. kautskyi Pabst X GF HLC An Forzza 15 (?)
Stelis aprica Lindl. X GF HLC An Menini Neto 127 (?)
S. intermedia Poepp. & Endl. X DEF HLC An Menini Neto 159 (?)
S. megantha Barb. Rodr. X DEF HLC An Forzza 60 (?)
S. papaquerensis Rchb. f. X GF HLC An Sousa s.n. (BHCB 14764)
S. parvula Lindl. X GF HLC An Krieger s.n. (CESJ 8593)
Thysanoglossa organensis Brade
X SSF HLC An Menini Neto 89 (?) Vanilla cf. gardneri Rolfe X SSF HeS An Forzza 2115 (?) Xylobium variegatum (Ruiz
& Pav.) Garay & Dunst.
X SSF HLF An Almeida 24 (?)
The map was prepared using Arc View GIS 3.2Òon the Americas Base Map (Bletter
et al.2004).
Results
One hundred and eighty-one species of epiphytes (MB—41 spp., RBRG—59 spp. and PEI—113 spp.), representing 65 genera and 12 families of epiphytes were recorded. Most species (102, 56.3%) were characteristic holoepiphytes, while 54 (29.8%) were facultative holoepiphytes and 25 (13.8%) were hemiepiphytes (3 primary hemiepiphytes and 22 secondary hemipiphytes). Of these species, 113 showed dispersion by anemochory while
68 had evidence of zoochory (Table1).
A comparison between the number of epiphytic species found and the total angiosperm species listed for each area shows that the percentage of the flora represented by epiphytes is around 9–11%, being slightly lower in MB, the area influenced by ‘‘Cerrado’’ vegetation, which is drier than other two areas.
Araceae, Bromeliaceae, Cactaceae, Orchidaceae and Piperaceae are the only flowering plant families common to all three areas. Exclusive occurrences at family level were
Table 1 continued
Species Area Habitat EC Disp Voucher specimens
MB RBRG PEI
Peperomia alata Ruiz & Pav. X X SSF HLF Zo Assis 105 (?), Castro 55 (?)
P. blanda (Jacq.) Kunth X SSF HLF Zo Forzza 2101 (?) P. corcovadensis Gardner X SSF HLF Zo Assis 265 (?)
P. decora Dahlst. X HLF Zo Krieger s.n. (CESJ
13193)
P. mandioccana Miq. X SSF/DEF HLF Zo Krieger s.n. (CESJ 8578)
P. martiana Miq. X SSF HLF Zo Assis 104 (?)
P. polystachyoides Dahlst. X SSF HLF Zo Assis 456 (?) P. quadrifolia (L.) Kunth X SSF HLF Zo Assis 103 (?)
P. stenocarpa Regel X SSF HLF Zo Castro 498 (?)
P. subpilosa Yunck. X SSF HLF Zo Forzza 2099 (?)
P. tetraphylla (Forst.) Hook. X SSF/DEF HLF Zo Krieger s.n. (CESJ 8523) P. urocarpa Fisch. & C.A.
Mey ¤
X X SSF HLF Zo Assis 593 (?)
RUBIACEAE
Hillia parasitica Jacq. X DEF HeP An Pereira s.n. (CESJ 28425) EC ecological category (Benzing1990), HLC characteristic holoepiphyte, HLF facultative holoepiphyte, HeP primary hemiepiphyte, HeS secondary hemiepiphyte, Disp dispersal syndromes, An Anemochory, Zo Zoochory. Voucher specimens are found at BHCB (*), CESJ (?), HB (#), RB (@) and VIC (°) herbaria. Habitat: SSF seasonal semideciduous forest (at PEI, these are the groves at 1,200 m elev.), DEF dense evergreen forest, GF gallery forest or forests near depressions or ‘grutas’ (highlands of PEI, above 1,500 m elev.), CR ‘‘campo rupestre’’
Species in bold are cited in the Minas Gerais Red List (Biodiversitas2007) as: Critically Endangered (); Endangered (§); Vulnerable (?); Near Threatened (¤); Data Deficient (€)
2 Lists used in florist ic similarity an alysis Local ity Altit ude N ° spp A rea (h a) Co ordina tes Ve getatio n types Refe rence Estreito Augus to Ce ´sar , Rio Uru guai (RS ) 650 63 – 2 7 °24 0S–5 1 °27 0W DSF Ro galski and Zani n ( 2003 ) Bertiog a (SP ) 0 96 – 2 3 °45 0S–4 5 °58 0W R E Mar tins et al. ( 2008 ) Fragment os Curitiba (PR) 900 80 96,9 25 °25 0S–4 9 °16 0W MEF Bo rgo and Silva ( 2003 ) Reserva d a C idade Univ ersita ´ria Armando Sal les de Oliveira (SP ) 735– 770 29 10 23 °33 0S–4 6 °43 0W SSF, DEF D islich an d Mantovan i ( 1998 ) G roppo and Pirani ( 2005 ) Estac ¸a˜ o Experi mental Agr ono ˆmic a (RS) 40 40 – 3 0 °04 0S–5 1 °40 0W G F G iongo and Wae chter ( 2004 ) Fazend a Gralha Azul (PR) 870– 920 30 475 25 °37 0S–4 9 °17 0W MEF G aiotto an d Acra ( 2005 ) Figuei ras iso ladas planı ´cie costei ra (RS ) 20 70 – 2 9 °35 0S–5 0 °04 0W A A G onc ¸alves and Waechter ( 2003 ) Ilha do Mel (PR) 0 6 1 2,76 0 2 5 °30 0S–4 8 °23 0W DEF , R E K ersten and Silva ( 2001 ) E. E. Jure ´ia-Itat ins (SP ) 0–1, 400 96 79,8 30* 24 °18 0S–4 7 °30 0W DEF , R E Mam ede et al. ( 2004 ) Mata do Bau ´(MG) 900 41 10 21 °11 0S–4 3 °56 0W SSF, GF Prese nt wor k Nu ´cleo Curu cutu, P. E. da Serr a d o Mar (SP ) 750– 850 45 12,0 90 23 °59 0S–4 6 °44 0W DEF , C A G arcia and Pir ani ( 2005 ) P. E. do Cerr ado de Jaguar iaı ´va (PR ) 750– 900 16 426, 62 24 °09 0S–5 0 °18 0W SSF, GF, CE R Lin singen et al. ( 2006 ) P. E. Ib itipoca (MG) 1,20 0–1,784 113 1923 ,5 21 °40 0S–4 3 °52 0W SSF, GF, DEF , C R Prese nt wor k P.E. Itapua ˜ (RS ) 50–2 65 48 5,56 6 3 0 °24 0S–5 0 °58 0W R E Muss kopf ( 2006 ) P. E. In tervales, Base Sai badela (SP) 70–2 50 55 48,0 00* 24 °14 0S–4 8 °04 0W SSF Zip arro et al. ( 2005 ) P. E. da Serra do Bri gadei ro (MG ) 1,00 0–2,000 111 13,2 10 20 °43 0S–4 2 °29 0W SSF, CA Leoni and Tinte ( 2004 ) Parqu e d o Inga ´ (PR ) 550 25 47,3 23 °25 0S–5 1 °25 0W SSF D ettke et al. ( 2008 ) P. N . do Itatiaia (RJ) 500– 2,789 106 30,0 00* 22 °30 0S–4 4 °35 0W DEF , C A JABOT ** P. N . Serra dos O´ rga ˜os (RJ) 1,20 0–2,263 87 10,6 53* 22 °26 0S–4 3 °06 0W DEF , C A JABOT **
2 cont inued Loca lity Alt itude N ° spp Area (ha) Co ordina tes Vege tation typ es Refere nce Rio Barigu ¨i (PR) 900 33 8,6 25 °34 0S–4 9 °20 0W MEF Kers ten an d Silva ( 2002 ) ReB io da Represa d o Grama (MG) 750 59 263,8 21 °25 0S–4 2 °56 0W SSF, GF Present work Baci a d o Rio Ig uac ¸u (PR) 865– 950 83 53,9 25 °40 0S–5 4 °26 0W MEF Kers ten an d Kuniyosh i ( 2009 ) Serr a d e S a˜o Jose ´(M G) 900– 1,430 41 – 2 1 °05 0S–4 4 °09 0W SSF, GF, CR, CER Alves and Kolb ek ( 2009 ) Torr es (RS) 0 103 – 2 9 °18 0S–4 9 °41 0W DEF Waechter ( 1986 ) of species refers onl y to epip hytic Angiosper ms, excludin g fern species. ReBi o Biol ogica l Reserve, P.E. State Park, P.N . Na tional Park, E.E. Ecologi cal Sta tion, SSF duous seasonal forest, DS F deciduous se asonal forest, DEF dense evergr een for est, MEF mixed eve rgreen forest, RE ‘‘rest inga’ ’ o r coastal forest, GF gallery forest, ‘‘campo rupest re’ ’, CA ‘‘campo de alt itude’ ’, CER ‘‘Cer rado’ ’, AA anthropi c area ns signall ed with * refer to the whole conserva tion area as the author s did not specify the area sa mpled. JABOT ** is the database of the Jardim Bo taˆ nico do Rio de (RB), av ailable at www .jbrj.go v.br
recorded for RBRG (Cyclanthaceae—1 sp., Marcgraviaceae—2 spp., Melastomataceae—1 sp.) and PEI (Griseliniaceae—1 spp., Rubiaceae—1 spp.).
Highest species richness was found in Orchidaceae (89 spp.), Bromeliaceae (36 spp.), Araceae (20 spp.), Cactaceae and Piperaceae (12 spp. each), these families representing 93% of the total species recorded. However, such families occupied different positions
within the three areas (Fig.2). While Orchidaceae was the largest family at MB and PEI
(24 and 66 spp. respectively), followed by Bromeliaceae (7 and 22 spp.), Piperaceae at MB (6 spp.) and Araceae at PEI (9 spp.), it appears only in third position at RBRG (13 sp.), after Bromeliaceae (16 spp.) and Araceae (14 spp.).
Of the 65 genera found, only 12 were common to all three areas, while 25 were exclusive to PEI, 11 were found only at RBRG and two were exclusive to MB.
Of the 181 species recorded, approximately 58% belong to 13 genera (i.e. less than one third of all recorded genera), of which eight were Orchidaceae. The most diverse genera were Peperomia and Pleurothallis s.l. (12 spp.), followed by Epidendrum, Oncidium and Philodendron (9 spp.), Anthurium (8 spp.), Rhipsalis and Tillandsia (6 spp.), Bulbophyl-lum, Campylocentrum, Maxillaria, Octomeria and Stelis (5 spp.). Amongst the top five species-rich genera, Tillandsia was the only one common to all areas.
The floristic analysis of similarity between the three study areas, calculated using Jaccard’s coefficient (MB/RBRG = 0.163, MB/PEI = 0.085 and RBRG/PEI = 0.067),
and also represented in the Venn diagram (Fig.3), shows three rather distinct floras. A
small overlap exists between the epiphytic floras of the areas, with only five species common to all three: Encyclia patens, Gomesa recurva Philodendron propinquum, Til-landsia geminiflora and T. usneoides. Even in the two areas with more similar vegetation formations, RBRG and MB, the overlap covers only nine species: Billbergia zebrina, Hylocereus setaceus, Campylocentrum linearifolium, Comparettia coccinea, Epidendrum densiflorum, Eurystyles actinosophila, Polystachya estrellensis, Peperomia alata and P. urocarpa: all commonly found in seasonal semi-deciduous forests throughout South America.
Results of the similarity analyses performed between the three study areas and another 21 surveys from the states of Minas Gerais, Sa˜o Paulo, Rio de Janeiro, Parana´ and Rio
Grande do Sul show slighthly different results in the dendrograms (Figs.4,5).
Fig. 2 Species richness of the five most representative families in the three study areas: Mata do Bau´ (MB), Reserva Biolo´gica da Represa do Grama (RBRG) and Parque Estadual de Ibitipoca (PEI)—Minas Gerais, Brazil
The similarity indices presented in the analyses are relatively low. The dendrogram generated in the first analysis (all species included) obtained a cophenetic value of 0.8339
(Fig.4). Two major groups, A and B, can be recognized in both dendrograms. Group A
includes primarily areas of Southeastern Brazil (Minas Gerais, Rio de Janeiro and Sa˜o Paulo), including PEI, while group B shows a predominance of Southern Brazilian areas (Parana´ and Rio Grande do Sul), but includes the study areas MB and RBRG. In the second
analysis (excluding rare species, Fig.5), a reconfiguration of the subgroups is seen, and all
studied groups are included within group A, the Jaccard’s coefficient is slightly higher than before, with only one subgroup at more than 0.5 (Curitiba and Rio Barigui). The cophe-netic value is 0.8289.
Discussion
The 12 angiosperm families registered in this study correspond to approx. 30% of those with epiphytes in the Neotropics, according to the estimates provided by Gentry and Dodson (1987). The families common to all studied areas, Araceae, Bromeliaceae, Cact-aceae, Orchidaceae and PiperCact-aceae, coincided with the largest proportion of epiphytic
species generally found (Benzing 1990), repeating the pattern found in other epiphytic
plant surveys (Ingram et al. 1996; Kersten and Silva2002; Borgo and Silva2003;
Gon-c¸alves and Waechter2003; Rogalski and Zanin2003; Giongo and Waechter2004; Gaiotto
and Acra2005).
Regarding ecological categories, the characteristc holoepiphytes are the dominant cat-egory, almost two times higher than facultative holoepiphytes, as found in other studies
(e.g., Nieder et al. 2000; Borgo and Silva 2003; Rogalski and Zanin2003; Gaiotto and
Acra 2005). However, Alves and Kolbek (2009) recorded a different proportion for
‘‘campo rupestre’’ vegetation, where they found facultative holoepiphytes to be far more numerous than characteristic holoepiphytes. This opposes what was found during the present study in PEI where ‘‘campo rupestre’’ is also predominant.
Reproductive strategies are an important factor in the success of epiphytes (Gentry and
Dodson1987) and the occurrence of anemochory as the predominant dispersal syndrome
among species was highlighted by Benzing (1987). The results of this study corroborate this hypothesis, as 62.4% are dispersed through anemochory and the remaining 47.6% are zoochoric species. This percentage of anemochory in species reflects the high number of orchid and bromeliads species registered in the surveys, which is also supported by our results.
Fig. 3 Venn diagram showing exclusive and shared species between the three study areas: Mata do Bau´ (MB), Reserva Biolo´gica da Represa do Grama (RBRG) and Parque Estadual de Ibitipoca (PEI)—Minas Gerais, Brazil
The lower epiphyte proportion in MB was an expected result, because the area is drier than PEI or RBRG. Dry environments are generally poorer in epiphytic species, as highlighted by Gentry and Dodson (1987).
Orchidaceae present the highest species richness in most studies of epiphytic flora in
Neotropical vegetations, generally followed by Bromeliaceae (Freiberg1996; Ingram et al.
1996; Freiberg and Freiberg2000; Bussmann 2001; Kersten and Silva2002; Borgo and
Silva 2003; Rogalski and Zanin2003; Giongo and Waechter2004; Hefler and Faustioni
2004; Gaiotto and Acra2005; Kro¨mer et al.2005; Alves et al. 2008; Kersten and
Ku-niyoshi2009). Other flowering plant families occasionally occupy the first position, as was
found by Benavides et al. (2006) in the Colombian Amazon, with Araceae. Are´valo and Betancur (2004) also obtained an unexpected result in four vegetation types in the Colombian Guayana, with two areas where Orchidaceae was the richest family, but another two areas where Araceae was the most species rich. The present study shows that Bro-meliaceae and Araceae were richer than Orchidaceae in RBRG, an unusual result when compared with the studies cited above for the Neotropics. However, most of the research where Orchidaceae appears as the top epiphytic family was carried out either in evergreen lowland or cloud forests, while the present results suggest that family dominance may be more variable in seasonal forests. On the other hand, Ziparro et al. (2005) found more species of Araceae than of Orchidaceae and Bromeliaceae in lowland dense evergreen
Fig. 4 Similarity tree (Jaccard’s coefficient) obtained by the analysis of all species found within the floristic lists of the 24 areas
forest in Sa˜o Paulo, but that area was the subject of specific Araceae studies which may have caused a bias in their results.
The greater similarity of RBRG and PEI (8 genera in common, c. 12%), despite their different altitudes and vegetation types may reflect their position within the Atlantic forest biome, while MB is surrounded by ‘‘Cerrado’’. The results suggest that the distance between the sites, which is greater between PEI and RBRG than MB-RBRG or PEI-MB, is not correlated to generic composition. Given that MB and RBRG share similar altitudes (900 and 750 m) and forest types (seasonal semi-deciduous and gallery forest), it was expected that they would present more commonality than was actually found (only two shared genera, c. 3%).
Each study area presented one genus as its most diverse, highlighting the uniqueness of the epiphytic flora in each particular location: Peperomia, with 6 species, was the largest genus in MB, while 7 Philodendron species were recorded at RBRG and 11 species of Pleurothallis s.l. at PEI. Diverse factors may have contributed towards the species dom-inance of these genera in the different areas: for example, the succulence in species of Peperomia allows for wider tolerance of more marked seasonality in forests associated with the ‘‘Cerrado’’ biome, such as MB, and the fact that most species of this genus were recorded as facultative epiphytes also points towards a wider ecological spectrum, also
Fig. 5 Similarity tree (Jaccard’s coefficient) obtained by the analysis of floristic lists excluding rare species of the 24 areas
supported by its pantropical distribution. On the other hand, the predominance of species of Philodendron and other Araceae at RBRG may be linked to this family’s affinities with the Atlantic forest biome, particularly at lower altitudes. In the case of PEI and Pleurothallis, a genus particularly rich in species from cloud forests, it may indicate floristic links between this site and other highlands in Eastern Brazil.
The position of Tillandsia must be emphasized, as it was the only genus amongst the top five species-rich genera common to all three areas of this study. Versieux and Wendt (2007) remark on the wide distribution of Tillandsia species in the Neotropics, justifying their presence in all three areas, despite the floristic, altitude and/or vegetation type dis-crepancies between them. Also, anemochory could help explain this wide distribution. Martinelli et al. (2008) also remark on the richness and wide distribution of Tillandsia in the Atlantic forest domain. The genus also appears amongst the richest within the epiphytic
flora in other surveys in Southern Brazil (Kersten and Silva2002; Borgo and Silva2003;
Gonc¸alves and Waechter 2003; Rogalski and Zanin 2003; Giongo and Waechter 2004;
Gaiotto and Acra 2005; Linsingen et al. 2006). However, surveys performed within
Southeastern Brazil, in Minas Gerais and Sa˜o Paulo states, do not show Tillandsia amongst the most representative elements of the epiphytic flora: Leoni and Tinte (2004) cite only two species for the Parque Estadual da Serra do Brigadeiro—Minas Gerais—while Ma-mede et al. (2004) (Jure´ia-Itatins), Garcia and Pirani (2005) (Parque Estadual da Serra do Mar—Nu´cleo Curucutu) and Ziparro et al. (2005) (Parque Estadual Intervales—Base Saibadela), all in Sa˜o Paulo, recorded only four, two and one species, respectively, thus highlighting the variation of epiphytic species composition between forests in the South-eastern and Southern regions of Brazil.
The only five species common to all three areas (Encyclia patens, Gomesa recurva, Philodendron propinquum, Tillandsia geminiflora and T. usneoides) are widely distributed species occurring in a variety of habitats, therefore not contradicting the indication that each area has its own particular floristic composition.
The low coefficient of similarity between the two areas with the more similar vegetation formations (seasonal semideciduous forest) can be explained by the isolation caused by the ‘‘Cerrado’’ vegetation surrounding MB, while RBRG is found within the Atlantic forest biome. The low similarity coefficients found between three areas within a total of only
2,900 km2highlights the need for further study of the epiphytes in the forest fragments of
Minas Gerais.
The cophenetic values obtained in the analyses was of 0.8339 (including all species) and 0.8289 (excluding the rare species), supporting the results seen in the dendrograms. The low Jaccard’s index found indicates that the epiphytic floras in Southern and Southeastern Brazil can be considered distinct.
In both analyses, Parque Estadual de Ibitipoca is more similar to Parque Nacional do Itatiaia: a result expected as both areas located in the Serra da Mantiqueira are also geographically close. The association between Parque Estadual da Serra do Brigadeiro and
the Parque Nacional da Serra dos O´ rga˜os may be explained by their similar altitudes rather
than by their vegetation, as the forest in Parque Estadual da Serra do Brigadeiro is
markedly more seasonal than the Parque Nacional da Serra dos O´ rga˜os. However, all four
areas are relatively close geographically and the similarity of their epiphytic flora is more likely to be influenced by species adaptation to high altitude (i.e., their tolerance to low or near freezing temperatures and the particular role played by mist in species establishment) than by their affinities in terms of vegetation associations.
2,000 m. Kro¨mer et al. (2005) pointed at a peak of richness at c. 1,500 m and a diminution above 2,200 m in Bolivia. This reduction was also observed by Bussmann (2001) in Ecuador but the altitudinal ranges in his study are higher: 1,800–3,150 m. Gentry (1988) also found a decrease in species richness at higher altitudes (between 1,500–3,100 m) in the Andes. The data found for PEI (1,200–1,780 m) shows that the species number of epiphytes in highland forest was higher. These trends contrast with those found for woody species in the same region, generally higher in lowland forests and decreasing at higher
altitudes (Oliveira-Filho and Fontes2000).
There aren’t studies about the influence of altitude in epiphyte diversity in Brazil, but
the numbers presented in Table2 appear to confirm higher epiphyte richness in
high-altitude environments, bearing in mind that the high-altitude range considered here is lower than 2,000 m, where cold nights and the occurrence of frost would certainly affect the distri-bution of many tropical species.
The position of MB and RBRG differs between the two analyses. In the analysis that takes into account all species, both areas cluster within branch B, together with areas from southern Brazil, while in the analysis without the rare species MB and RBRG appear in branch A, together with southeastern areas that are closer geographically. This can be explained by the fact that analysis 1 has a trend to group richer floras together in branch A, and MB and RBRG, which are in drier locations and have comparatively poorer epiphytic flora, are excluded from branch A and fall into branch B.
Overall, the comparison of epiphytes from 24 areas from five different states (Table2)
showed remarkably low floristic similarity, except in Parana´, where areas of mixed evergreen forest at altitudes between 865–950 m (RB, FGA, Ctba and RI) have shown similarity higher than 0.5. Nevertheless, some subgroups based on altitudinal quotas could be recognized, such as the subgroup formed by areas within Sa˜o Paulo (PEI-SP, Jur-Ita, Ber, IM, all between 0–250 m except Jur-Ita, 0–1,400 m) and the subgroup from Rio Grande do Sul (Fig, PEI-RS, Tor, DC, between 0–265 m). Elevation is an important factor in composition of both rain and semideciduous forest areas of Atlantic domain, based on analysis of arboreal stratum as presented by Oliveira-Filho and Fontes (2000).
Low similarity coefficients between different areas were also found by Safford (2007) when working on the phytogeography of the Southeastern Brazilian highlands, or Brazilian Pa´ramos. Also, comparative studies developed with woody strata in montane seasonal semideciduous forests in Minas Gerais and Sa˜o Paulo show relatively low similarity
(Oliveira-Filho and Machado1993; Meira-Neto and Martins2002). More surveys focusing
on non-woody plant groups are needed, as most work developed in Brazil is centered on tree studies. Different study approaches would provide a deeper insight both into the actual diversity and the biogeography of the distinct areas.
Conservation
The low similarity coefficients found between the epiphytic floras of the three study areas in Minas Gerais and between 24 forest fragment sites within Southeastern and Southern Brazil underline the importance of conserving all possible fragments, independent of the size of the area or biome where they occur. In comparison with woody plant surveys
(Oliveira-Filho and Fontes2000), it can also be suggested that epiphytes appear to be more
species rich than trees in high altitude forests, therefore representing a better biodiversity indicator for this type of vegetation.
In terms of species conservation, the 30 recorded epiphytic species (c. 16.5%) listed
within the Minas Gerais Red List (Biodiversitas2007; Table1) are found in the following
families: Orchidaceae (12 spp.), Bromeliaceae (8 spp.), Araceae (4 spp.), Gesneriaceae (3 spp.), Cactaceae (2 spp.) and Piperaceae (1 sp.). The breakdown in conservation status is: Critically Endangered (6 spp.); Endangered (7 spp.); Vulnerable (12 spp.); Near Threa-tened (2 spp.); Data Deficient (4 spp.). PEI presents the largest number of threaThrea-tened species (20 spp.), followed by RBRG (9 spp.) and MB (4 spp.). Due to public awareness of epiphytic orchids, bromeliads, aroids and cacti as ornamentals, epiphytic families are
strongly emphasized within the Minas Gerais Red List (Biodiversitas2007), making this
list particularly useful to benchmark the findings of this work.
Acknowledgments The authors would like to thank Eve Lucas, William Milliken and Nigel Taylor (all RBG Kew) for critically reading and suggesting improvements to the manuscript, two anonymous reviewers for their valuable suggestions, and to Marco Antoˆnio Manha˜es (UFJF) for his help with the statistical analysis.
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