Plant species endemism in savanna vegetation on table

Vegetatio 113: 125-139, 1994.
(~) 1994 Kluwer Academic Publishers. Printedin Belgium.
125
Plant species endemism in savanna vegetation on table mountains (Campo
Rupestre) in Brazil
R. J. V. A l v e s I & J. K o l b e k 2
1R. Marquesa de Santos 22/1004, 22240 Rio de Janeiro, RJ, Brazil
2Institute of Botany, Dept. of Geobotany, Academy of Sciences of the Czech Republic, 252 43 Pr~honice, Czech
Republic
Accepted 1.11.1993
Key words: Brazil, Campo rupestre, Endemic species
Abstract
A new theory about the origin of endemism in the campo rupestre vegetation type is proposed and discussed,
based on the studies of endemic species which have been conducted in several campo rupestre areas. Data on
endemic plant species of the studied mountain ranges are provided. New localities are reported for some rare and
endemic plants of Minas Gerais, Brazil. The present knowledge of their distribution is briefly discussed. Vegetation
characteristics were studied in their stands by means of vegetation relevds, and a synthetic constancy table is
provided. The main phytogeographical characteristics of the studied sites are given.
Introduction and site characteristics
Isolated table mountains in the tropics biogeographically represent isolated islands and frequently bear
vegetation rich in endemic species. For example in
Africa these are called 'Bowals', in the equatorial
region of South America 'Tepuis' or 'Sabanas' and in
central Brazil they are known as 'Campos rupestres'.
In the broad sense this vegetation is a type of savanna. Various classifications of savannas were discussed
in great detail by Donselaar (1965), while subsequent
authors have only treated the definitions superficially. In broad terms the vegetation treated herein can be
described as the 'Taffelberg type savannas' as defined
by that author. During the phytocoenological survey
of the vegetation of some campo rupestre communities of Minas Gerais, Brazil in 1989 (Alves 1992a;
Alves & Kolbek 1993), some rare and endemic species
were collected (Alves 1991). Their finding relevantly
expands the present knowledge of their distribution.
While some species were known from only the type
localities (Smith & Ayensu 1976), others are endemic
to small areas, usually confined to specific altitudes
and substrates. Thus, Vellozia kolbekii (Alves 1992b),
for which new localities are cited, is probably the first
species of the genus for which a number of density
surveys in stands was executed even before the species
was described.
Stands with other endemic species are also being
studied. The fact that most species endemic to campo
rupestre have small distribution areas means that they
are usually endangered. Their survival depends on the
protection of their entire stands, rather than protection
of the isolated species. The knowledge of the vegetation in which they grow is scarce, but can be useful
for their protection. Knowledge of local floras is still
limited, and the list of endemic species will surely
grow.
The Serra de Sho Jos6 ranges from 900 to 1430 m
in altitude, roughly between 21 ° 03-07' S. 44 ° 06-13' W. The Serra do Lenheiro rises from 880 to 1212
m.s.m., centred at 21 ° 09' S. 44 ° 19' W. and bordered
at its southern foot by the city of S~o Jo~o Del Rei.
The Itutinga range is truly represented by a series of
relatively lower hillocks in higher ground, from 1000
to 1100 m, and the collection site there is 21 ° 19'
S. 44 ° 39' W. Coordinates for the other ranges are:
Serra de Ouro Branco (20 ° 23' S. 43 ° 42' W.), Ser-
126
ra Bico de Pedra (20 ° 28' S. 43 ° 42' W.), Serra de
Carrancas (21 ° 22' S. 44 ° 40' W.). The Chapada Diamantina in Bahia has several ranges. Though we do
not presently have the coordinates, the table mountains investigated were in the proximity of the town
Rio de Contas, Palmeiras, Lencois, and Mucuge. The
main studied ranges are shown in Fig. 1. The common factor of the sites where the mentioned species
grow is basically the lithosolic composition of soils in
which quartzites greatly predominate. Quartzite outcrops erode in a peculiar style, forming very uneven
surfaces. Many of the white-sand savanna formations
are the result of in situ erosion of these quartzites.
The outcrops themselves provide substrate for Aylthonia tomentosa, Vellozia crassicaulis, and Vellozia kolbekii, while the remaining treated species thrive precisely in the mentioned white sands. The localities
in question are aligned from WSW to ENE, forming
the so-called S~o Jos6 geological formation. These
quartzitic plateaus rise more or less abruptly from a
landscape of red-yellow distrophic latossols with cerrado vegetation. This geomorphology is locally called
'mar de morros' (sea of hills). The dependence of lithophytical plants upon their specific substrate provides a
reason for their restriction to the isolated ranges and
their subsequent endemism. The climate is continental
with a dry winter, 'Cwa' according to Ktippen (1936).
Droughts culminate in July with averages of 8.6 mm
rainfall and 9.9 °C, against 299.6 mm and 17.1 °C in
January. Absolute temperatures range from a minimum
of 1.0 to a maximum of 33.8 °C in that period.
Methods
The vegetation characteristics of these stands have
been studied since 1986. Since 1989, over 600 vegetation relev6s have been executed, and part of this
material, together with the usual floristic research, has
been used as base-data for the present paper. The mean
constancy percentages for each species are rounded to
the nearest whole numbers. The environmental factors
were studied in the main communities. Relevant taxonomic findings were also registered. Based on all theories and materials on the campos rupestres known to
us, enhanced by our own microclimate measurements
(Alves & Kolbek 1993), a new theory explaining the
origin of endemism of the species from this type of
vegetation was developed.
BRAZIL
MAIN CAMPO RUPESTRE RANGES
~
Q ¢c~J
Fig. 1. Location of main studied campo rupestre areas,
Significant
endemism
campo
rupestre
taxa
with
high
Many campo rupestre species are only know from holotypes in herbaria. This is mainly due to their small
areas of distribution and insufficient collecting. This
is true for many species of the families Cactaceae,
Cyperaceae, Eriocaulaceae, Euphorbiaceae, Lamiaceae, Melastomataceae, Myrtaceae, Orchidaceae,
Velloziaceae, etc. According to Burman (1991) endemic species make up about 30% of the Espinhaqo range
flora. Most of those species are actually restricted to
isolated mountains or smaller ranges which make up
part of the Espinhaqo complex. A list of the endemic
species investigated by us is in Table 1.
Species of the family Velloziaceae frequently dominate the stands on quartzitic table mountains of Minas
Gerais. Smith (1990, pers. comm.) points out that the
family is rich in species endemic to small areas, being
many known only from type localities. Most small and
isolated table mountains may be expected to have their
very own species. Among the most representative cam-
127
Table 1. Main endemic species investigated to date in the studied ranges.
D = dominant species, + = species with medium cover values, R = species
with low cover values or rare species, X = occurring species. Ranges: A =
Sao Jos6, B = Lenheiro, C = O u r o Branco, D = Carrancas, E = O u r o Grosso,
F = Cip6, G = Chapada Diamantina.
Species
A
B
C
Ranges
D
E
Eugenia langsdorfii Berg.
Croton gnidiaceus Baiil.
Selaginellafragilima Air. Silv.
Mesadenella meei R.J.V. Alves
Aristolochia claussenii Duchartre
Laelia mantiqueirae Pabst
Aristolochia aff. gracilis Duchartre
Stachytarpheta sellowiana Cham
Pelexia phallocaUosa R.J.V. Alves
Sarcoglottis caudata R.J.V. Alves
Leiothrix prolifera (Bong.) Ruhl.
Arthrocereus melanurus (Schum.)
R
R
R
Braun & al.
+
+
R
D
R
D
D
D
D
D
-
D
Schultes
D
+
D
R
Aristolochia gracilis Duchartre
Aristolochia smilacina Hoehne
Vellozia incurvata Ma~. ex
R
R
-
+
-
+
F
G
+
+
R
R
D
+
R
R
R
Sarcoglottis cogniauxiana (B.Rodr.)
Schltr.
Aylthonia tomentosa (Mart.) Menezes
Vellozia kolbekii R.J.V. Alves
Vellozia crinita Goeth. & Henr.
Vellozia crassicaulis Mart. ex
Schult. f.
Vellozia crispata L.B. Smith
Laelia endsfeldzii Pabst
Jacaranda decurrens Cham
Camarea affmis St. Hil.
Polygala pseudo-erica St. Hil.
po rupestre families, Burman (1991) reveals that all but
6 out of some 200 species of Velloziaceae are endemic
to that vegetation type, in the Xyridaceae 100-150 out
of 450, and that many Eriocaulaceae are also confined
to this formation. The same author also reveals that
some species of Vellozia are resinous and have been
used as locomotive fuel on the Curvelo-Diamantina
railway. The proportion of life forms in some stands
dominated by Velloziaceae are in Table 2 and Fig. 2.
Of the Velloziaceae, Aylthonia tomentosa is commonly found in the S~o Jos6, Lenheiro and Itutinga
ranges, growing on relatively steep walls of quartzite
R
D
+
+
+
+
R
R
+
X
X
X
+
+
+
R
+
X
-
R
cliffs. We also found it in the Carrancas range on micaceous schist walls facing north. The distribution mentioned by Smith & Ayensu (1976) is linked to a single specimen (Irwin et al. 29559). The type locality
is equally vague, somewhere on the 160 km stretch
between Ouro Preto and S~o JoAo Del Rei, or even in
Diamantina, (Smith & Ayensu 1976). Our specimen
matches perfectly that of Mello Barreto 4798, which
was collected in the S~o Jos6 range. A confusion seems
to persist among the species and their sites, which may
be partly due to the variability in populations. Aylthonia
tomentosa dominates saxicolous stands which include
128
Table 2. Species in stands dominated by Aylthonia tomentosa, Vellozia crassicaulis, I( crinita, and V. kolbekii (species endemic to campo
rupestre are in boldface) in the S~to Jos6 Range. Mean constancy values
are given based on 102 relev6s in the four communities. Predominant
life forms are provided for each species according to the classification of
Raunkiaer (1934). Ch= Chamaephyte, E= epiphyte, G= geophyte, H=
hemicryptophyte, L= lithophyte, Ph= phanerophyte, Th= therophyte,
a= mean constancy (%), b=- life form.
Species in shrub layer (E2)
Vanillosmopsis erythropappa Schult. Bip.
Leandra aurea (Cham.) Cogn.
Vellozia kolbekii Alves
Lepidaploa ruJogrisea (St. Hil.) H. Robins.
Aspilia sp.
Croton gnidiaceus Baill.
Eupatorium barbacense Hier.
Rapania andina Mez
Hyptisfruticosa Salzm,
Stryphnodendron adstringens (Mart,) Coville
Baccharis calvescens DC.
Chionolaena cf. latifolia Bak,
Chamaechrista brachypoda Benth,
flex amara (Veil,) Loes.
Byrsonima arctostaphylloides Nied.
Cephea ericoides Cham. & Schltd.
Byrsonima basiloba Adr, Juss.
Myrcia mutabilis DC.
Dasyphyllum macrocephala (Bak.) Cabr.
Comotia sertularia (DC.) Triana
Chamaechrista sp.
Aloraia myriadenia (Schult. Bip.) Bak.
Hyptis reticulata Mart. ex Benth.
Ditassa sp.
Vochysia thyrsoidea Pohl
Clusia arrudea E & Tdana
Miconia theaezans (Bonpl.) Cogn.
Peixotoa tomentosa Adr. Juss.
Miconia ligustroides (DC.) Naud.
Gomidezia gaudichaudiana Berg.
Hyptis complicata St. Hil. ex Bentb.
llex integerrima (Veil.) Reiss.
Myrcia suaveolens Camb.
Paliavana lasiantha Wirth.
Erythroxylum suberosum Mart.
Jacaranda paucifoliata St. HiL
Chaetostoma armature (Spreng.) Cogn.
Gaylussacia brasiliensis (Spreng.) Meissn.
Baccharis sp.
Miconia peppericarpa DC,
ab
48 Ph
47 Ph
35 Ph
23 Ph
23 Ph
16 Ph
16 Ph
15 Ph
15 Ph
11 Ph
11 Ph
10 Ph
9 Ph
8 Ph
7 Ph
6 Ph
6 Ph
6 Ph
6 Ph
5 Ph
5 Ph
5 Ph
4 Pb
4 Ph
4 Ph
4 Pit
3 Ph
3 Ph
3 Ph
2 Ph
2 Ph
2 Ph
2 Ph
2 Ph
2 Ph
2 Ph
1 Ph
1 Ph
1 Ph
1 Ph
Family
Asteraceae
Melastomataceae
Velloziaceae
Asteraceae
Asteraceae
Euphorbiaceae
Asteraceae
Myrsinaceae
Lamiaceae
Mimosaceae
Asteraceae
Asteraceae
Caesafpiniaceae
AqMfoliaceae
Malpighiaceae
Lythraceae
Matpighiaceae
Myrtaceae
Asteraceae
MeIastomataceae
Caesalpiniaceae
Asteraceae
Lamiaceae
Asclepiadaceae
Vochysiaceae
Clusiaceae
MeIastomataceae
Malpighiaceae
Melastomataceae
Myrtaceae
Lamiaceae
Aquifotiaceae
Myrtaceae
Gesneriaceae
Erythroxylaceae
Bignoniaceae
Melastomataceae
Ericaceae
Asteraceae
Melastomataceae
129
Table 2. Continued.
Species in shrub layer (E2)
ab
Family
Podocarpus lamberti Klotzsch
Chamaechrista cathartica Mart.
Lippia lupulina Chain. & Schlecht.
Peixotoa catarinensis C. Anderson
1illandsia stricta Soland vat, stricta
?~llandsia tenuifolia L.
Tacoyenaformosa K. Schum.
Usnea el, rubicunda Stilt.
Austroplenckia populnea Reiss.
Bulbophyllum ipanemensis Hoelme
Croton antisyphiliticus Mart.
Peixotoa sp.
Psittacanthus robustus Mart.
(epiphytic parasite on Vochysia thyrsoidea
1 Ph
l Ph
1 Ph
1 Ph
1E
1E
1 Ph
1E
l Ph
1E
1 Ph
1 Ph
1E
Podocarpaceae
Caesalpiniaceae
Verbenaceae
Malpighiaceae
Bromeliaceae
Bromeliaceae
Rubiaceae
Usneaceae
Celastraceae
Orchidaceae
Euphorbiaceae
Malpighiaceae
Loranthaceae
Species in ground layer (Et)
Melinis minutiflora P. Beaav,
Leandra aurea (Chain.) Cogn.
Loudetiopsis chrysothrix (Nees,) J. Felir
Cuphea ericoides Chain. & Schltd.
Lagenocarpus rigidus Nees
Bulbostylis lagoensis Boeck.
Andropogon leucostachyus H.B.K.
Borreria brachystemonoides Chain, & Schltd,
Vellozia crinita Goeth. & Henr.
Arthrocereus melanurus (Schum.) Braun et al.
Rhynchospora globosa R. & S.
Vellozia kolbekii Alves
Alomia myriadenia (Schult, Bip.) Bak.
Vellozia crassicaulis Mart, ex Schult.
Laelia mantiqueirae Pabst
Aylthonia tomentosa (Mart,) Menezes
Vanillosmopsis erythropappa Schult. Bip,
Doryopteris ornithopus (Mett.) J.Srnith
Senecio adamantinus Bong.
Euphorbia coecorum Mart,
Polypodium lepidopteris (Langsd. & Fisch.) Kze.
Portulaca mucronata Link,
Eupatorium barbacense Hier.
Splecklinia rupestris (Lind.) E Barros
Dipladenia gentianoides Z. Br.
Aspilia sp,
m a n y s p e c i e s o f Orchidaceae, a n d s o m e Bromeliaceae
a n d Cactaceae, a n d w h i c h are d e n s e l y c o v e r e d w i t h
encrusting lichens. The most intense flowering occurs
from January to March, but individual plants flower
66 H
59 Ph
54 H
50 Ch
50 H
42 H
40 H
37 Ch
35 Ch
33 Ch
31 H
30 Ph
29 Ch
29 Ph
29 L
28 L
27 Ph
24 Ch
19 Ch
17 G
16 ChlLIE
15 Ch
15 Ph
15 L
14 G
12 Ph
Poaceae
Melastomataceae
Poaceae
Lythraceae
Cyperaceae
Cyperaceae
Poaceae
Rubiaceae
Velloziaceae
Cactaceae
Cyperaceae
Velloziaceae
Asteraceae
Velloziaceae
Orchidaceae
Velloziaceae
Asteraceae
PoIypodiaceae
Asteraceae
Euphorbiaceae
Polypodiaceae
Portulacaceae
Asteraceae
Orchidaceae
Apocynaceae
Asteraceae
d u r i n g t h e w h o l e year. F u r t h e r field s t u d i e s a r e n e c e s sary for a n a t t e m p t at d e f i n i n g t h e d i s t r i b u t i o n o f this
species, as well as m a n y s i m i l a r t a x a v i c a r i o u s w i t h
it o n n e a r b y m o u n t a i n r a n g e s , a n d e v e n as f a r as t h e
130
Table 2. Continued.
Species in ground layer (El)
ab
Croton gnidiaceus Baili.
Xyrius asperula Kunth
Peperioma decora Dahlst. vat. decora
Klotzschia brasiliensis Cham.
Marcetia taxifolia (St. Hil.) DC.
Cuphea thymoides Chain. & Schltd.
Syngonanthus niveus (Bong.) Ruhl.
Xyris bahiana Malme
Cryptanthus schwackeanus Mez.
Sida cf. rhombifolia L.
Rhynchospora consanguinea Boeck.
Stachytarpheta seUowiana Schau.
Aechmea nudicaulis (L.) Griseb.
Dyckia argentea Mez
Ditassa sp.
Chamaechrista sp.
Borreria sp.
Bulbophyllum ipanemensis Hoehne
Gomphrena agrestris Mart.
Polygala paniculata L.
Comolia sertularia (DC.) Triana
Syngonanthus gracilis (Koern.) Ruhl.
Vigna sp.
Spigelia heliotropoides Guim. & Font.
Xyris rupicola Kunth
Aristolochia gracilis Ducht.
Tillandsia gardneri Lindl.
Phyllanthus niruri L.
Oncidium blanchetii Rchb. f.
Senna bicapsularis (L.) Roxb.
Xyris hymenachne Mart.
Rapania andina Mez
Vernonia linearifolia Gatdn.
Bulbostylis paradoxa (Spreng.) Clarke
Anemia villosa Willd.
Anacheilium vespum (VEIL) Dressler sp. agg.
Elaphoglossum sp.
cf. Briza sp.
Anthurium sellowianum Kunth
Hyptis complicata (St. Hil.) ex Benth.
outcrops on the Pai IMcio hill in Bahia.
Vellozia kolbekii was found in three localities,
roughly 60 km apart. The best studied locality of these
is the S~o Jos6 range in which several large populations
occur (Fig. 3). It grows on unevenly eroded quartzite
outcrops with or without a layer of fine sand and grav-
12 Ph
11 H
11 L
10 G
10 Ph
9 Ch
9 Th
9H
8L
8 Ch
8 Ch
8 Ph
8L
7L
7 Ch
7 Ph
7 Ch
7L
6 Ch
6 Ch
6 Ph
6 Th
5H
5 Ch
5H
5H
5L
5 Ch
4 Ch
4 Ph
4H
4 Ph
4 Ph
4H
4 Ch
4L
3L
3 Ch
3L
3 Ph
Family
Euphorbiaceae
Xyridaceae
Piperaceae
Apiaceae
Melastomataceae
Lythraceae
Eriocaulaceae
Xyridaceae
Bromeliaceae
Malvaceae
Cyperaceae
Verbenaceae
Bromeliaceae
Bromeliaceae
Asclepiadaceae
Caesalpiniaceae
Rubiaceae
Orchidaceae
Amaranthaceae
P olygalaceae
Melastomataceae
Eriocaulaceae
Fabaceae
Loganiaceae
Xyridaceae
A ristolochiaceae
Bromeliaceae
Euphorbiaceae
Orchidaceae
Caesalpiniaceae
Xyridaceae
Myrsinaceae
Asteraceae
Cyperaceae
Schizeaceae
Orchidaceae
Aspidiaceae
Poaceae
Araceae
Lamiaceae
el, (usually on bare rock and without any apparent
preference for the cracks and ledges in it). The second
locality is west of the city of S~o Jo~o Del Rei, in the
Lenheiro range. Populations here are smaller and more
isolated, partly due to human exploitation (mining and
overgrazing), and in part to the more heterogenous soil
131
Table 2. Continued.
Species in ground layer (El)
ab
Family
Stryphnodendron adstringens (Mart,) Coville
Chaetostoma luteum Cogn.
Hyptis conferta Pohl
Microlicia cinerea Cogn.
Cyperus cf. cyperinus (Vahl) Suringar
Eremanthus speciosus Bak.
Dyckia sp.
Sauvagesia rubiginosa St. Hil.
Pfaffia helychrisoides (Moq.) Kuntze
Miconia ligustroides (DC.) Naud.
Lepidaploa rufogrisea (St. Hil.) H. Robins
Anemia elegans Pohl.
Dasyphyllum brasiliensis (Spreng.) Cabr.
Lycnophora passerina (Mart. ex D.C.) Gardn.
Chamaechrista rotundifolia Pers.
Hyptisfruticosa Salzm.
Trimeziajuncifolia (Klatt.) Benth. & Hook. f.
Erythroxylum suberosum St. Hil.
Spigelia scabra Cham. & Schltd.
Lagenocarpus polyphyllus Kuntze
Gaylussacia montana (Pohl) Sleumer
Peperomia subrubrispica C. DC.
Gomidezia a~nis (Camb.) Legr.
Leucothose crassifolia (Pohl.) DC.
Clusia arrudea PI. & Triana
3 Ph
3 Ch
3 Ph
3 Ch
3H
Mimosaceae
Melastomataceae
Lamiaceae
Melastomataceae
Cyperaceae
Asteraceae
Bromeliaceae
Ochnaceae
Amaranthaceae
Melastomataceae
Asteraceae
Schizeaceae
Asteraceae
Asteraceae
Caesalpiniaceae
Lamiaceae
lridaceae
Erythroxyllaceae
Loganiaceae
Cyperaceae
Ericaceae
Piperaceae
Myrtaceae
Ericaceae
Clusiaceae
3H
3L
3 Ch
3 Ch
3 Ph
3 Ph
3L
2 Ph
2 Ph
2 Ch
2 Ph
2G
2 Ph
2 Ch
2 Ch
2 Ph
2L
2 Ph
2 Ph
2 Ph
Species with 1% constancy only (Ground layer): Achyrocline albicans Griseb.
[Ch], Aechraea bromeliifolia (Rudge) Baker [El, Baccharis calvescens DC. [Phi,
Bulbophyllum bidentatum (B. aodr.) Cogn. [L], Bulbostylis sp. [Ch], Byrsonima basiloba Adr. Juss. [Phi, Camaridium rigidum B, Rodr, [L], Carex sp.
[Ch], Chamaechrista brachypoda Benth. [Ph], Chamaechrista cathartica Mart.
[Phi, Commelina agraria Kunth [Ch], Coccocypselum erythrocephalum Chain.
& Schltd. [Ch], Gaylussacia ridelii Meissn. [Phi, Glaziovanthus curumbensis (Phil.) Macleen [HI, Gomphrena officinalis Mart. [Ch], Hatiora aff. salicornioides (Haw.) Br. & R. ILl, Hippeastrum of. equestre (Ait.) Herb. [G],
Kalanchoe brasiliensis Camb. [Ch/L], Leiothrix proh'fera (Bong.) Ruhl. [Th],
Maxillaria acicularis Herb. [L], Miconia cf. sellowiana Naud. [Phi, Miconia
theaezans (Bompl.) Cong. [Phi, Microlicia isophylla DC. [Ch], Microlicia spec.
[Ch], Ditassa sp. II [Ch], Peixotoa catarinensis C. Anderson [Phi, Peixotoa
tomentosa Adr. Juss. [Ph], Rumex sp. [Th], Poaceae I [Ch], Poaceae II [Cb].
c o m p o s i t i o n o f this range. T h e densest stands of V.
k o l b e k i i were f o u n d in the third locality, in the Ouro
G r o s s o range. This p o p u l a t i o n forms thickets on the
southern slopes o f l o w - l y i n g quartzite outcrops which
face the Carrancas range s o m e 20 k m yonder. It c a n be
reached from the B a r b a c e n a - L a v r a s road b y p a r k i n g
at the 100 k m m a r k e r b r i d g e over the Rio G r a n d e and
h i k i n g some 1200 m south.
132
LIFE FORM S P E C T R U M
~Y
SP~C
LIFE FORM S P E C T R U M
CONStANt-CORRECTED
I ~
TH (2.3Z)
L (1 1.5X)
TH (1oIZ)
L (10,1Z)
CH (23.0X)
3.8x)
H (I 8.5~)
O (3.4x)
E (1.4x)
E (4.ox)
G (2.9X)
Ph (47.1X)
Ph (42.~)
F i g . 2.
(left) Life form spectrum of the stands in Table 2, based on floristic data. (right) The previous life form spectrum (corrected by constancy values to better illustrate the vegetational aspect). Ch=Chamaephyte, E=epiphyte, G=geophyte,
H=hemicryptophyte, L=lithophyte, Ph=phanerophyte, Th=therophyte.
Fig. 3. Stand of Vellozia kolbekii in the S~o Jos6 range.
Vellozia crassicaulis was observed in dense stands
on quartzite outcrops of the S~o Jos6 range, especially
on the north-facing slopes at higher altitudes. This
species has been collected more frequently and in a
wider distribution range (Smith & Ayensu 1976) in
the states of Minas Gerais, Goias and Mato Grosso.
However, it had not been previously recorded for the
S~o Jos6 range.
133
Fig. 4. Table mountain with campo rupestre in the Sao Jos6 range - Aerial Photograph approx. 1:30.000.
Vellozia crinita, curiously, was known only from
the type specimen until the date of the revision (Smith
& Ayensu 1976). Since 1988 the occurrence of V. crinita was a commonly accepted fact to us in the S~o
Jos6 range, and in the same year stands were also
found in the vicinity of Itutinga. This species grows
in white sands, forming a network of small creeping
caudex-mounds, which apparently grow at a very slow
rate. The type specimen was collected in the S~o Jos6
range itself (Glaziou 16,388). Smith & Ayensu (1976)
expressed doubt as to wether Glaziou's locality was
not S~o Joao Del Rei (Lenheiro range), but this resulted from the renaming of what was then called Villa de
S~o Jos6 d'el Rey, and is now known as Tiradentes.
The adjacent mountain range preserved its old name
according to the nearby town, still being known as Serra S~o Jos6. Nevertheless the species was also found in
the Lenheiro range, occurring in several of our relev6s.
Eugenia langsdorfii is apparently endemic to the
region between Lavras and the S~o Jos6 range. The
species was rarely collected and seems to be restricted
to a small number of table-mountains. E. langsdorfii
grows on white sands in campo rupestre formations
that have periodic natural fires. Scree mixed with white
sand seems to be a favorable combination of substrates,
with gravel size from 3 to 6 cm in diameter. This species
was seldom found in relev6s. Eugenia langsdorfii was
found growing mostly in the sparse shrub layer of open
stands (Table 3). This stand grew on a cliff slope,
covering 20% of the surface, the rest being exposed
bedrock. The soil was only a white sand layer with a
maximum depth of 5 cm.
For Sarcoglottis cogniauxiana, Hoehne (1945) provides a full description, but the illustration bears certain discrepancies which indicate that it had been made
from a herbarium specimen. This species was already
known by Cogniaux (1893-1906), who provided a color plate in an unpublished part of his 'Icon. Orch.
Bresil'. Hoehne's diagnosis of the live plant (Hoehne
1945:329) fits our field observations perfectly, there
being no doubt as to the identity of this endemic
species. The distribution cited is the city S~o Jo~o d'el
Rei in Minas Gerais. This town, is located at the eastern base of the Serra do Lenheiro, where we collected a
specimen on November 1st, 1989. The new locality for
this species is the range called Serra de S~o Jos6, east
of Tiradentes. In both ranges the species grows in the
bleached sands which frequently include a high content
134
Table 3. S p e c i e s in s t a n d in w h i c h Sarcoglottis cogniauxiana (a) a n d Eugenia
langsdorfii (b) w e r e r e c o r d e d in t h e S~o Jos~ r a n g e . A s i m p l e c o m b i n e d s c a l e
o f c o v e r a n d a b u n d a n c e is u s e d to i n d i c a t e t h e i r s i g n i f i c a n c e in the s t u d i e d
stands, D = d o m i n a n t s p e c i e s , + = s p e c i e s w i t h m e d i u m c o v e r v a l u e s . R =
s p e c i e s w i t h l o w c o v e r v a l u e s or r a r e s p e c i e s ,
Shrub layer (E2)
a
b
Family
Vellozia kolbekii Alves
Leandra aurea (Chain.) Cogn.
Aspilia sp.
Vanillosmopxis eo,thropappa Schutt. Bip.
Hyptis lantan(~dia Poit.
Camaechrista brachypoda Benth.
Byrsonima arctostaphylloides Nied.
Chaetostoma armature (Spreng.) Cogn.
D
R
+
R
R
R
Velloziaceae
Melastomataceae
msteraceae
Asteraceae
Lamiaceae
Caesafpiniaceae
Matpighiaceae
Melo.vtomataceae
D
-
+
-
R
-
R
-
+
-
Ground layer (E I )
Sarcoglottis cogniauxiana (B. Rodr.) Schltr,
Eugenia langdsorfii Berg
Bulbostylis capillaris (L.) Clarke
l.xJudetiopsis chrysothrix (Nees) J. Felir
Lagenocarpus rigidus (Kunth.) Nees
Metinis rainutiflora H.B.K.
Cuphea ericoides Chain, & Schl.
Leandra aurea (Chain.) Cogn.
Vanillosmopsis erythropappa Sehult. Bip.
Laelia mantiqueirae Pabst
Vellozia ~dbela'i R.J.V. Alves
Vellozia crassicaulis Mart.
Arthrocereus melwzurus (Schum.) Braun et al.
Eupamrium barbacenae Hier.
Andropogon tener Kunth
Chamaechrista sp.
Stenorrhynct~r lanceolatus (Aubl.) L.C. Rich.
Buchnera lavandutaceae (:ham. & Schl.
Doryopreris ornithopus (Mett.) J. Smith
Sauvagesia rubiginosa St. Hit.
Senecio sp.
Polypodium lepidopteris (Langsd. & Fisch,) Kz¢.
Portulaca mucronata Lindl.
Cryptanthus schwackeanus Mez
Rhynchospora globosa R. & S.
Xyris bahiana Malme
Microlicia isophylla DC. vat. stenophylla Cogn.
Lepidaploa rufogrisea (St. Hil,) H. Robins
Klotz.~chia brasiliensis Cham.
Xyris asperula Kunth
R
-
-
R
D
+
D
R
+
D
+
R
+
R
+
R
+
R
R
R
-
D
-
D
+
-
+
-
+
-
R
-
R
--
R
-
R
-
R
-
R
R
-
R
--
R
-
D
-
+
-
R
-
R
--
R
--
R
-
Shrub layer (E2)
Ground layer (Et)
20
40
5
35
Moss layer (Eo)
50
40
Cover (%)
Orchidaceae
Myrlaceae
Cyperaceae
Poaceae
Cyperaceae
Poaceae
Lythraceae
Melastomataceae
Asteraceae
Orchidaceae
Velloziaceae
Velloziaceae
Cactaceae
Asteraceae
Poaceae
Caesalpiniaceae
Orchidaceae
Scrophutariaceae
Potypodiaceae
Ochnaceae
Asteraceae
Polypodiaceae
Portulacaceae
Bromeliaceae
C3peraceae
Xyridaceae
Melastomataceae
Asteraceae
Apiaceae
Xyridaceae
135
of milky-quartz gravel. Stands with this species consist
of a relatively continuous herbaceous cover composed
of species of Lagenocarpus, Bulbostylis, Xyris, and
Andropogon. Sparsely scattered woody species do not
create a true layer here (Table 3). The sand layer is
about 30 cm deep, directly on a solid quartzite basement. All flowering individuals observed were leafless.
Though the presence of leaves at anthesis is used as a
taxonomic character by Pabst & Dungs (1975, 1977),
it has limited systematic value. Many Spiranthinae
flourish maintaining their leaves when they grow in
stands with a dense shrub or tree cover, whereas the
same species bloom leafless on more exposed sites. We
observed these conditions for Stenorrhynchus lanceolatus (Aubl.) L.C.Rich, Eltroplectris triloba (Lindl.)
Pabst, and numerous other species.
Considering the present desolate state in which the
Lenheiro range, the occurrence of Sarcoglottis cogniauxiana in the S~o Jose range is relevant for the survival of this rare endemic. Populations are very sparse
even in its natural stands. A moss and lichen layer with
10% cover (50% on rocks) was present.
Croton gnidiaceus is another endemic species of the
Sao Jose range. It is closely related to C. timandroides,
which occurs endemically in the Serra do Cip6. It was
not found in nearby ranges. Croton gnidiaceus occurs
mainly in stands with Vellozia kolbekii, where it has a
17% constancy. It occurs in at least 10 relevEs as an
additional species.
Discussion
Campos rupestres and tepuis topographically act as
quartzite and sandstone islands emerging from a sea of
unrelated substrates such as laterite (Fig. 4). In Brazil,
the term 'mar de morros' is frequently used to describe
the rugged cerrado landscape that surrounds the campo
rupestre mountain ranges. Mainly thanks to this insulax effect, endemic species play an important role in
the composition of campo rupestre floras. Many campo rupestre species are only known from holotypes
in herbaria. This is mainly due to their small areas
of distribution and insufficient collecting. This is well
known about many species of the families Cactaceae,
Cyperaceae, Eriocaulaceae, Euphorbiaceae, Lamiaceae, Melastomataceae, Myrtaceae, Orchidaceae,
Velloziaceae, etc. A basic technical insufficiency of
most distribution surveys published so far is that they
fail to distinguish between non-occurring and unfound
species, which are both registered as nill. Thus white
spots on distribution maps can have two meanings.
According to Burman (1991) endemic species make up
about 30% of the Espinhaqo range flora. Most of those
species are actually restricted to isolated mountains or
smaller ranges which make part of the Espinha~o complex. Among the most representative campo rupestre
families, Burman (1991) reveals species of Velloziaceae, Xyridaceae, and many Eriocaulaceae, and also
that some species of Vellozia are resinous and have
been used as locomotive fuel, Curvelo-Diamantina
railway. This is why Vellozia spp. are known in Bahia
as 'Candomba', a word derived from the Tupi-Guarani
indigenous words language. A large Vellozia, according to Burman (1991), can take up to 100 years to reach
'adult' stage. On a field trip to the Ouro Branco range
with Johann Becker in 1990, we came across specimens of VeUozia sp. over 4 m high, and estimated the
age of individuals of V incurvata, with shorter stature,
at over 500 years.
Sarcoglottis caudata, Liparis beckeri, Pelexia
phaUocallosa, Eugenia langsdorfii, and Croton gnidiaceus are strict endemics of the Sao Jose range.
Sarcoglottis cogniauxiana, Leiothrix prolifera, and
Selaginellafragillima only occur in the Serra SAo Jose
and adjacent Lenheiro range. Vellozia virgata is a mysterious species collected by Glaziou in the SAo Jose
range in 1889. It is apparently known only from the
type specimen and from an uncited collection on Pico
Itabira do Campo, about 120 km north (Smith & Ayensu 1976:51).
Some preliminary studies on the distribution patterns of certain taxa throughout the campos rupestres
(Giulietti & Pirani 1988; Harley & Simmons 1988;
Barros 1990) have been published. Despite the present
limitations of our knowledge on this subject, they clearly demonstrate unequal distribution tendencies within
some of the main taxa (usually families). Most species
of the Velloziaceae are confined to smaller ranges, and
a few, like Vellozia dasypus Seub. (Harley & Simmons 1988:100) have disjunct distributions, occurring
in the campo rupestre and in the restinga (sandy coastal
strand vegetation) north of Salvador. The same author
mentions that Mandevilla moricandiana (DC.) Woods.
of the Apocynaceae has also been found in restinga and campo rupestre, and our own collections in
the Sao Jose range and in the Maricd restinga in Rio
de Janeiro confirm this. Other species like Bonnetia
stricta, Marcetia taxifolia, Couma rigida, Evolvulus
jacobinus and Anthurium affine (Harley & Simmons
1986, 1988) share this disjunct distribution. Giulietti
& Pirani (1988) believe these species to be indigenous
136
to the Espinhaqo chain and secondary in the restingas.
The question of how their diaspores reached places
so remote still remains. Not much is presently known
about disjunct distribution patterns for campo rupestre
species. Beach strand vegetation is known to be vicarious around the world, and some species of these communities are more widely distributed (Kolbek & Alves
1993). The fact that restinga vegetation occurs in an
extremely humid coastal climate suggests that campos
rupestres may not be as arid as certain authors claim
(see further).
Harley & Simmons (1986:9) suggests that high
endemicity in certain campos rupestres 'is probably
due to speciation as a response to local, not necessarily present-day, conditions, and partly due to reliction and extinction, following range contraction of formerly more widespread species as a result of climatic
changes'. Giulietti & Pirani (1988:47) further claim
that species which occur disjunctly in the Espinhaqo
chain and in the serras of Goi~ts (which have similar
geological, physical and climatic features), 'provide
evidence of former epochs when there were major links
between the floras of these regions'. The high number
of endemic species which are vicarious from range to
range indubitably testifies links, but with the present
state of knowledge we can only speculate about their
specific nature.
According to Ramos (1986), between 1650--950
million years ago, a lacustrine (shallow sea or lake)
environment existed in the area of the S~o Jos6 range.
Due to the presence of ripple marks in quartzites from
the Espinha~o chain ranges, we may suppose their formation conditions to have been similar. The tectonics
which raised the campo rupestre ranges from among
latosol surroundings supposedly occurred between
950-650 million years ago, during the last geotectonic cycle. Latosols, which are older, have apparently
been separating the outcrop ranges since then. This
mainly edaphic contrast is responsible for the potential
isolation barriers between individual stands of campo
rupestre.
On a broad scale the greatest climatic differences
are found between the three main campo rupestre
chains. The Espinhaqo chain within the zone with
annual rainfall above 1250 mm; the Chapada Diamantina, with less than 1000 mm (but the N and S
sides of this complex have profoundly distinct rainfall
patterns: the south side near Rio de Contas is much
drier than the more northern Palmeiras and Lencois
vicinity); and the serras of Goi~is with over 1500 mm.
Nimer & Brand~o (1989:13) state that 'the plant asso-
ciations of the cerrados are apparently constituted of an
ecological climax linked to both climatic and edaphic
factors'. They present a series of maps with a broader
zonation of climatic factors, but the S~o Jost, Ouro
Branco and Ouro Preto ranges lie south, beyond their
proposed 'cerrado region'. In truth, the typical cerrado
zone extends through Lavras as far south as Pirassununga in the state of Sao Paulo. Despite this, we have
placed annual rainfall zones on one map with lithosolic soils in order to provide an approximate notion
of their possible influence on the formation of campo rupestre vegetation (Alves 1992a). When isolated
mountains and ranges (such as campo rupestre serras)
rise from relatively flat terrain, they frequently provoke
condensation of rain from the passing cloud cover. On
relatively clear days the few existent clouds only condense when they pass over the summits of the tall
peaks. This precipitation excess is unaccounted for by
nearby meteorological stations. At first sight the campo
rupestre areas may thus seem more arid than they really
are, and available meteorological data, even from nearby stations, may be misleading. An exception seems
to be the station of S~o Jo~o Del Rei - - in a campo
rupestre at 991 m s.m. in the Lenheiro range, with an
average annual rainfall of 1467.4 mm. As Harley &
Simmons (1986) agree, high nocturnal drops in temperature cause dew condensation which compensates
for part of the hydric deficiency. According to Nimer
& Brand~o (1989: fig. 11), the states of Minas Gerais
and Bahia annually have from 5 to 10 months of hydric
deficiency (from 5 to 7 along the Espinhaqo chain and
adjacent land).
Based on the abundance of Cactaceae, some
authors like Siqueira (1988) have speculated that the
area now comprising campo rupestre vegetation was
more arid in the past, mainly due to studies from the
Amazon region. The numerous similar species of Cactaceae in the region are found in disjunct areas, as
is also the case of many Orchidaceae, Melastomataceae, Eriocaulaceae and Velloziaceae. Thus some
researchers attribute to campos rupestres the role of
refugia for xerophytic species after the invasion of a
moister climate. Harley & Simmons (1988:113)recognize the need of further fossil evidence to support this
and states that 'Apart from requiring a more specialised
substrate, usually associated with impervious rocks,
the climatic regime which suite them [campo rupestre
species] while distinctly seasonal, is cooler and more
humid, the aridity tempered with rain and dew from
the atmosphere, suggesting marked diurnal changes
in temperature'. These climatic observations generally
137
agree our field data. Even in a generally more arid environment, these mountains were probably moister than
their surroundings. They further suggest that the campo
rupestre mountain ranges could have acted as refugia
during adverse periods. We believe that the confinement of xerophytic species to these mountain ranges
(and their relative absence from surrounding terrain) is
due mainly to edaphic conditions. The lithosolic nature
of their soils could hardly have supported the suggested
Quaternary forest refugia, as most non-campo rupestre
plant species would not survive the harsh environmental conditions.
The development of saxicolous plants ancestral to
those found presently in campos rupestres can only
have begun after the Silurean, when some plants had
definitely become adapted to terrestrial conditions.
(The Magnoliopsida only appeared during the Jurassic.) We believe most endemic campo rupestre species
have probably developed as recently as the Pleistocene
(Fig. 5). Hammen (1974) supposes that three cool dry
periods should have occurred, approximately between
20,000-13,000, 11,000-9,500, and 3,500-2,800 years
ago, but not much is known about local conditions
in Brazil of that era. The abundance and considerable depth of laterites indicates that they are usually
much older than the Pleistocene (Smol~ov~i 1982).
This should also be valid in areas adjacent to campos rupestres. Latosols such as those surrounding the
S~o Jos6 range have been formed by the action of
humid tropical intemperism, and this opposes the pastdrought theory. This same intemperism (by differentially eroding quartzite outcrops) has formed the sand
and gravel beds atop table mountains and at their bases.
These are characteristic soils for some campo rupestre
vegetation types. Hence the edaphic contrast between
campo rupestre and surrounding terrain has apparently
existed for a long period.
Many succulent herbs, mainly orchids and cacti, grow both epiphytically and lithophytically. Epiphytism is usually understood as a strategy linked primarily to illumination conditions of tree crowns as
contrasted with by those of the forest understory. The
same principle probably applies to lithophytes, though
the environment is usually even dryer and substrate
temperatures become higher than on trees. Due to fast
runoff in both cases, water absorption by the plants
is more dependent on duration of rain or dew than on
total rainfall. The effect of nutrient poverty of campo rupestre soils (usually bleached sands) is almost
analogous to aluminium content in laterites, and to
conditions caused by high runoff on tree bark. In the
EVENT
E ~ D E M ~ c CAMPO
F~R~T MAQNO~OP~D~
YEARS A G O
x I0 ~
0 "1
t
135--180 t
F~T~T~T~-~ST~=
400~40
t
~=~N~.OO~~O~
T~:-~
950--650
t
Fig. 5. Illustrative chronogram of main events which were a
prerequisite to the advent of endemic campo rupestre species.
above cases, though due to distinct causes, availability
of nutrients to plants is limited. We agree with Barros
(1990), in that part of the present campo rupestre lithophytes may have originated from epiphytes of nearby
cerrados and gallery forests.
Many campo rupestre plant species thrive well in
artificial conditions which strongly differ from those
in their present natural habitat. Orchids, bromeliads
and some cacti grown in constantly humid greenhouses are examples of plants which develop into stronger,
more robust individuals when grown in a greenhouse.
Though campo rupestre plants are highly tolerant to
long drought and thermal oscillations with extreme
minima and maxima in their natural habitat, these
conditions are an environmental stress factor and not
a requirement of the species. They grow in campos
rupestres thanks to their unique morpho-physiological
adaptations (like the CAM metabolism), and usually
fail to occur in the surrounding vegetation (like cerrado) either due to stronger competition from other
species or possibly due to their inability to thrive on
latossol, due to high aluminium content, for example.
Of the grasses, Diandrostachya (Loudetiopsis)
chrysothrix is probably the most typical campo
rupestre species. The barbed glumes indicate a possible epizoochoric dispersal in addition to anemochory,
and this may help explain the relatively broad distribution of this species. The same may be valid for
the sedge Lagenocarpus rigidus, which is widely dispersed on most campos rupestres. Dispersal barriers
such as geographic isolation of one campo rupestre
from another may have accelerated speciation in situ
and resulted in a higher rate of endemism. This seems
138
to be supported by the fact that most Myrtaceae (usually endozoochoric) have a wider distribution throughout
campos rupestres than families in which other dispersal
mechanisms predominate. A more detailed correlation
of dispersal strategies should shed light on the causes of campo rupestre dispersal patterns. Presently the
main efforts should, in our opinion, be directed toward
enhancement of floristic knowledge which can then
serve as a base for distribution surveys.
Conclusions
Based on the above discussed aspects, we concluded that most known endemic species in the campos
rupestres so far studied have probably originated locally from c o m m o n ancestral species. The inability to
grow on the much older latosolic soils which surround
the table mountains indicates that they are not relicts of
previously more dispersed populations (Alves 1992a).
Evidence of the relative ages of these substrate types
is suggested by the presence of small lateritic hardpans and deposits with cerrado plant species on top of
many table mountains. Furthermore, the distribution
of vicarious species on nearby table mountains also
supports the in situ speciation, as does the occurrence
of several very related species on the same table mountain, for ex. Bulbophyllum ipanemensis, B. teresensis,
B. weddellii, B. spp. aff. in the S~o Jos6 range (Alves
1991).
Furthermore, the available moisture on these table
mountains is more abundant than in the surrounding
cerrados, due to orographic condensations and frequent
mist. This apparently refutes previous theories which
stated that the campo rupestre species are relicts of
more arid climates.
Life on the table mountains is edaphically and otherwise so isolated from the surrounding cerrado, that
one can not deduce any significant climatic changes
for this region as was attempted by other authors.
The insular status of table mountains has endowed
the campos rupestres with many endemic species.
The articulate geomorphology of the campo rupestre
ranges provides isolation barriers, which prevent the
migration of certain species between the ranges or
even between individual mountains of the same range.
Mosaic distribution of soil types contributes to this isolation. Populations of many endemic campo rupestre
species are thus restricted to extremely small areas.
Another factor which contributes to the restricted
dispersal of these species is their slow metabolism
due to nutrient-poor substrates, in lithophytic species
enhanced by extreme substrate temperature oscillations. These species are evidently more easily endangered than those with broad distribution.
Based on our field observations from the campos
rupestres, the mentioned species should be considered endangered. Knowledge of the vegetation and site
characteristics in which they grow is the first prerequisite for the successful conservation of these species.
Many other endemic plant species are likely to become
endangered in the near future. Unfortunately, knowledge about isolated species has seldom helped in their
conservation in Brazil. Seeds have been collected from
some of the treated species for attempted propagation
and were distributed to numerous growers which have
not yet reported their results.
Acknowledgements
The authors thank two referees for constructive criticism and literature references.
References
Alves, R. J. V. 1991. Field guide to the orchids of the Serra
de S,~o Jos6. Guia de campo das orqufdeas da Serra de
S~o Jos6. Tropicaleaf, 148 pp., Praha.
Alves, R. J. V. 1992a. The flora and vegetation of the Serra de
Siio Jos6 in Minas Gerais, Brazil. Thesis, 114 pp. [Botan.
Inst. Czechoslovak Academy of Sciences, Pruhonice].
Alves, R. J. V. 1992b. Sarcoglottis caudata (Orchidaceae)
and Velloziakolbekii (Velloziaceae), two new species from
Minas Gerais, Brazil. Novon, St. Louis 2: 299-301.
Alves, R. J. V. & Kolbek, J. 1993. Penumbral rock and sand
communicaties in campo rupestre sites in Brazil. Journ.
Veget. Sci., Uppsala 4: 357-366.
Barros, E 1990. Diversidade taxonOmica e distribuic~o
geogrfifica das Orchidaceae Brasileiras. Acta Bot. Brasil.
4: 177-187.
Burman, A. 1991. Saving Brazil's savannas. New Scientist,
London, 129: 30-34.
Cogniaux, A. 1893-1906. Orchidaceae. In: Martius' Flora
Brasiliensis, Vol. 3, Tom. 4---6.
Donselaar, J. van. 1965. An ecological and phytogeographic
study of northern Surinam savannas. Wentia 14:1-163.
Giulietti, A. M. & Pirani, J. R. 1988. Patterns of geographic
distribution of some plant species from the Espinha~o
range, Minas GerMs and Bahia, Brazil. In: Heyer, W.
A. & Vanzolini, P. E. eds., Proceedings of a workshop
on neotropical distribution patterns, pp. 39-69, Rio de
Janeiro, Acad. Bras. CiSncias.
Hammen, Th. van der & al. 1974. The Pleistocene changes of
vegetation and climate in tropical South America. Journ.
139
of Biogeography 1: 3-26.
Harley, R. M. & Simmons, N. A. 1986. Florula of Mucuge.
227 pp., Royal Bot. Gardens, Kew, London.
Harley, R. M. & Simmons, N. A. 1988. Evolution and distribution of Eriope and its relatives in Brazil. In: Heyer,
W. A. & Vanzolini, P. E. eds., Proceedings of a workshop
on neotropical distribution patterns, pp. 71-120, Rio de
Janeiro, Acad. Bras. Ci~ncias.
Hoehne, E C. 1945. Flora brasilica Vol. XII (II): 311-330,
tab. 180 (1), Sao Paulo.
Kolbek, J. & Alves, R. J. V. 1993. Some vicariating plant
communities in Brazil, Malaysia and Singapore. Vegetatio, Dordrecht, Boston, London, 109: 15-27.
K0ppen, W. 1936. Das geographische System der Klimate.
Vol. 1 (C). In: KOppen, W. & Geiger, R. eds. Handbuch
der Klimatologie. Gebr. Borntraeger, Berlin.
Nimer, E. & Brando, A. M. P. M. 1989. Balan~o hfdrico e clima da regi~o dos Cerrados. Fundaq~o Brasil. de Geogr~if.
e Estatfst. (IBGE), 162 pp., Rio de Janeiro.
Pabst, G. E J. & Dungs, E 1975, 1977. Orchidaceae
brasilienses. Vol. 1, 408 pp., Vol. 2, 418 pp., Brucke
Verlag, Hildesheim.
Ramos, R. R. C. 1986. Sintese geol6gica da Serra de S~o
Jos6 (Tiradentes - MG). ms. [depon. by R. Alves]
Raunkiaer, C. 1934. The life forms of plants and statistical
plant geography. Being the collected papers of C. Raunkiaer. Clarendon Press, Oxford.
Silveira, A. A. da. 1931. Floralia Montium. Vol. 2, pp. 322339, Imprensa Oficial de Minas Gerais, Belo Horizonte.
Siqueira, J. C. da. 1988. Curso de adapta~6es morfol6gicas
nos vegetais, ms. [annot. by R. Alves during the course]
Smith, L. B. & Ayensu, E. S. 1976. A revision of the American Velloziaceae. In: Smithsonian Contr. Bot. 30, 172 pp.,
Smithsonian Inst., Washington.
Smolfkov~i, L. 1982. Pedologie I, & II. St~it. Pedag. Nakl.,
Praha, 294 pp.