Content uploaded by Leandro Oliveira Drummond
Author content
All content in this area was uploaded by Leandro Oliveira Drummond on Feb 16, 2018
Content may be subject to copyright.
1
Impact of re on anurans of rupestrian grasslands
Available at http://www.salamandra-journal.com
© 2018 Deutsche Gesellscha für Herpetologie und Terrarienkunde e.V. (DGHT), Mannheim, Germany
SALAMANDRA 54(1) 1–10 15 February 2018 ISSN 0036–3375
Impact of re on anurans of rupestrian grasslands (campos rupestres):
a case study in the Serra do Espinhaço, Brazil
L O D,, F R M M R S P
1) Universidade Federal de Ouro Preto, Pós-Graduação em Ecologia de Biomas Tropicais. Campos Morro do Cruzeiro, s/n, Bauxita,
CEP 35400-000, Ouro Preto, MG, Brazil
2) Universidade Federal do Rio de Janeiro, Departamento de Ecologia, Laboratório de Vertebrados. CP 68020, Ilha do Fundão.
CEP 21941-901, Rio de Janeiro, RJ, Brazil
Corresponding author: L O D, e-mail: barrocolod@hotmail.com
Manuscript received: 25 September 2016
Accepted: 25 April 2017 by E L
Abstract. e rupestrian grasslands of the Serra do Espinhaço (Espinhaço Mountain Range) are mainly a savanna vegeta-
tion complex with a high degree of anuran endemism. Although this re-prone vegetation is frequently burned by natural
and anthropogenic res, there is no information about how populations of the anurans of this ecosystem respond to such
an impact. Aiming to evaluate the eect of re on the anuran composition of a typical rupestrian grasslands environment,
a high-elevation temporary pond of about m² (Lagoa Seca) in Parque Estadual do Itacolomi was monitored during
three dierent one-year time periods: Pre-re (PrF), immediately Post-re (PoF) and Seven Years Post-re (PoF). Surveys
took place every two weeks throughout each study period. An increase in anuran species richness was found immediately
aer the re event. e species present during the periods when the vegetation was in advanced stages of regeneration
(PrF and PoF) were not eliminated by the re event. Additionally, ve species were recorded at low densities exclusively
in the PoF period. e factors that may provide re resistance to anuran of rupestrian grasslands and the implications of
the results for re management plans, a conservation measure previously treated as a taboo by many Brazilian conserva-
tion managers, are discussed.
Key words. Amphibians, altitudinal grasslands, conservation, re eect, rocky elds, savanna, Espinhaço Mountain Range.
Introduction
Fire is recognized as an important factor in the forma-
tion of savanna and grassland landscapes (H
M , M et al. ). In fact, according to
C (), natural re is an ecological factor that
can determine the structure of an entire ecosystem, main-
ly through selecting ecophysiological, morpho-anatomical
and physiognomical-structural characteristics of the ora.
e historical relationship between re and highly re-re-
sistant plant species is one of the factors responsible for the
structural and taxonomic diversication in savannas, like
those of the Cerrado morphoclimatic domain (S et
al. ).
Despite the importance of re in shaping natural envi-
ronments, its impact on anurans remains poorly known
(C et al. , C L , W-
T et al. ), and most of the existing information
deals with observations in temperate regions (e.g. M-
et al. , M et al. , S F
, H P , G et al. ). Fire
may change population dynamics of anurans both directly,
by causing the death of individuals, and indirectly, through
alteration of habitat (G ). Fire can signi-
cantly alter an environment by altering the humidity and
temperature of the soil, the structure of the vegetation, the
depth of the leaf litter, the rate of soil erosion and the hy-
droperiod of aquatic habitats (C et al. , S
F ).
Studies evaluating the eects of re on Brazilian fauna
are scarce, particularly for anurans (F et al. ).
is is surprising since Brazil harbors the richest anuran
fauna in the world (S et al. ) and possesses
several biomes adapted to dierent re regimes. Tropi-
cal forests in the Amazon and Atlantic Forest morphocli-
matic domains, for example, have evolved under a low to
nearly nonexistent re regime (H et al. ). In
fact, P P () and R et al. () found
re to have negative eects on diet and population density
of frogs associated with bromeliads of coastal sandbanks
(restingas) of the Atlantic Forest morphoclimatic domain.
On the other hand, M et al. () found no eects
of re on the pattern of co-occurrence of anuran species
in the only study carried out to date in the re-prone sa-
2
L O D et al.
vanna formations of the Cerrado morphoclimatic domain.
It seems clear that, as far as anurans are concerned, much
needs to be understod regarding the eects of re on lo-
cal fauna. is understanding is particularly important for
properly designing and implementing conservation and
management plans, such as the use of prescribed-re or
re prevention and suppression measures.
Rupestrian grasslands (Campos rupestres in Portu-
guese) are vegetation complexes that occur above m
in elevation throughout the Serra do Espinhaço (Espin-
haço Mountain Range) in central Minas Gerais State to
northern Bahia State, and sparsely throughout some oth-
er mountainous areas of central Brazil (A et al. ).
is diverse and re-prone mountainous mosaic of vege-
tation encompasses phytophysiognomies from grasslands
to shrublands on shallow soils of quartzitic-sandstone and
iron-ore with numerous rocky outcrops (G P-
, G et al. , S et al. ).
Both the ora and fauna of rupestrian grasslands are struc-
turally very similar to that of the Cerrado, but with some
inuence from the Atlantic Forest and Caatinga, and some
of the highest rates of endemism among phytophysiogno-
mies in Brazil (G P , H ).
Although rupestrian grasslands are frequently burned by
natural and anthropogenic res, there have been no stud-
ies on the eect of re on its highly endemic anuran fauna
(L et al. ).
e present study evaluates the eect of re on the an-
uran composition of a typical rupestrian grasslands envi-
ronment in the state of Minas Gerais in southeastern Bra-
zil. Sampling eorts targeted an isolated temporary pond
and surveyed its anuran fauna before, aer, and seven years
aer a re event.
Materials and methods
e study took place in Parque Estadual do Itacolo-
mi (PEIT), a conservation unit encompassing an area of
ha in the municipalities of Mariana and Ouro Preto,
Minas Gerais, Brazil (Fig. ). e park is in the transition
zone between the Atlantic Forest and Cerrado morphocli-
matic domains in the southern limit of the Serra do Es-
pinhaço. e vegetation of the approximately lowest
elevations of the conservation unit is semideciduous sea-
sonal rainforest, while the remaining higher areas, usu-
Figure 1. Geographic location of Parque Estadual do Itacolomi (shaded area) and the study site (Lagoa Seca, black dot), in the mu-
nicipalities of Mariana and Ouro Preto, Minas Gerais State, Brazil.
3
Impact of re on anurans of rupestrian grasslands
ally above m, contain the complex of phytophysio-
gnomies that comprise rupestrian grasslands (C et al.
, P S ).
According to the Köppen classication, the study site has
a mesothermic climate with dry winters and hot, rainy sum-
mers (Cwb; K et al. ). e elevation varies from
m to m, the average annual rainfall is mm and
is concentrated from November to March, while the average
annual temperature is °C, with a maximum of °C and
minimum of °C (C et al. ). e study site, Lagoa
Seca, is a temporary pond of about m² and maximum
depth of cm when completely full, located at an elevation
of m (°’” N, °’”W; WGS ) near Pico do
Itacolomi, the highest point in the park. Lagoa Seca is sit-
uated among typical rupestrian grasslands vegetation with
abundant rocky outcrops (Fig. ), and contains species of
macrophytes (E-S’ et al. ), with a pre-
dominance of the emergent species Juncus microcephalus.
Fire events occur frequently in the vicinity of PEIT,
but mainly towards the end of dry seasons. Most of these
res have both accidental or intentional anthropic origin,
such as to remove native vegetation in order to increase
and improve pasture areas (F et al. ). Recently,
the development of re prevention and control programs
has dramatically reduced the number of re events within
PEIT (F et al. ). Nonetheless, in early October
, a large anthropogenic re burned almost the entire
area of rupestrian grassland vegetation of PEIT. e re
burnt all macrophytes and much of the herbaceous and
shrubby vegetation of the area surrounding Lagoa Seca.
Visits to Lagoa Seca were made every two weeks during
three distinct one-year periods, for a total of seventy-two
visits ( each year; Fig. ): (i) Pre-re (PrF) – between the
months of October and September , when there
had not been a re event recorded at Lagoa Seca or its sur-
roundings for at least years; (ii) Post-re (PoF) – Octo-
ber to October , immediately aer the re event;
and (iii) Seven Years Post-re (PoF) – November to
October , aer complete regeneration of the burned
vegetation.
Anurans were surveyed by direct search guided by male
breeding activity and vocalization. During each visit, the
Figure 2. Studied temporary pond, Lagoa Seca, during four dierent periods: (A) Before the re event (February 2006); (B) just aer
the re event (October 2007); (C) One year aer the re event (October 2008); (D) Seven years aer the re event (December 2014).
4
L O D et al.
pond, as well as the marginal vegetation to meters from
the high-water mark of the pond, were inspected. Indi-
viduals of all species of anurans active between : and
: h were recorded.
Air temperature was measured with a mercury ther-
mometer at the beginning and end of each survey. Daily
rainfall data was provided by the environmental control
area of the company Novelis do Brasil LTDA. for the PrF
and PoF periods, and from Centro Nacional de Monito-
ramento e Alerta de Desastres Naturais for the PoF peri-
od. Variation in temperature and rainfall among the three
study periods are presented in Figure .
Voucher specimens were killed with xylocaine, xed
with formalin, preserved in alcohol and deposited
in the Coleção Herpetológica of the Laboratório de Zoolo-
gia dos Vertebrados (LZV) of the Universidade Federal de
Ouro Preto (Appendix I).
For all analyses, species presence/absence data for each
eld day were used. To assess the stability of community
composition among the studied periods, species were clas-
sied according to their proportion of occurrence among
eld days for each study period: constant = observed on
more than of the eld days; occasional = –; and
rare = less than . Sampling eciency was evaluated us-
ing species accumulation curves produced by the program
EstimateS version .. (C ).
To test for dierences in species composition of the
anuran community among three study periods a PER-
MANOVA (Permutational Multivariate Analysis of Vari-
ance) was performed. PERMDISP was used to test for ho-
mogeneity of multivariate dispersion between each peri-
od, since PERMANOVA has the implicit assumption that
dispersion is roughly constant across groups. PERMDISP
results can also be useful for determining whether with-
in-period temporal variation in assemblage structure dif-
fered among study periods (i.e. there were greater seasonal
uctuation in species composition in one period than in
others?) (A W ). Both analyses were
made using the Vegan package (O et al. ) in
the Renvironment (R Core Team ) with a signicance
level of ..
Results
A total of een species of anurans were recorded over the
three study periods. e greatest species richness was re-
corded in the Post-re period (PoF = spp.), followed by
the Pre-re period (PrF = spp.) and the Seven Years Post-
re period (PrF = spp.). Five species were exclusively re-
corded in PoF, each being recorded during a single eld day:
Leptodacylus cunicularius, L. furnarius, L. fuscus, Rhinella
crucifer, and Scinax fuscovarius. All of these exclusive PoF
species were represented by only a single individual, except
for Scinax fuscovarius, which was represented by two. Ad-
ditionally, all these exclusive PoF species were recorded per-
forming reproductive activity, except by Rhinella crucifer.
Two species, Dendropsophus minutus and Physalaemus cu-
vieri, were present only in the PrF and PoF periods, having
seemingly disappeared by the PoF period (Table ).
Sampling eciency (i.e. the potential of not encounter-
ing a new species) diered among the three study periods as
indicated by species accumulation curves. e curve for the
PoF period stabilized on the th day of sampling, while the
curve for the PrF period stabilized on the nd day of sam-
pling. e curve of the PoF period failed to stabilize, and
was continuing to increase through the last day of sampling,
indicating that new species could be encountered with ad-
ditional sampling eort during this period (Fig. ).
During the PrF period, four rare and ve occasional
species were recorded (Table ). Aer the re, the number
of rare species increased to nine. Most of these rare spe-
cies were new records ( spp.), but the frequency of Ischno-
cnema juipoca, previously considered common, decreased
drastically enough for it to become rare. At PoF, there
Figure 3. Annual variation of temperature and rainfall in the
pre-re (PrF), post-re (PoF), and seven-year post-re (7PoF)
periods.
5
Impact of re on anurans of rupestrian grasslands
was an increase in constant species, such as S. curicica and
L.latrans. e species S. squalirostris, L. jolyi and P. eryth-
ros maintained their frequency of occurrence throughout
all three study periods (Table ).
e anuran species composition of Lagoa Seca dif-
fered slightly, but signicantly, among study periods (PER-
MANOVA, R²=.; F,=. p=.). is dierence oc-
curred between the periods with the highest (PoF) and the
lowest (PoF) species richness (R²=,; F,=.; p<.);
PrF not diering from the other two periods. Additional-
ly, there were no dierences in intra-annual seasonal var-
iation in species composition among the study periods
(PERMDISP, F,=.; p=.).
Discussion
When evaluating the impacts of human activities on nat-
ural environments, it is essential to dierentiate naturally
occurring uctuations in species richness and abundance
from those resulting from the human activities (P-
et al. , P W ). Unfortu-
nately, long-term studies identifying patterns in popula-
tion uctuations are virtually absent in Brazil (S
S ). Although long-term monitoring has not
been performed at the Lagoa Seca, the fact that no spe-
cies was eliminated from the study area, and that there was
temporary settlements of new species aer the re strong-
ly suggests that anurans of rupestrian grasslands possess
some resistance to isolated re events.
However, one thing that must be considered is the sim-
plied environment that resulted from re, which may
have facilitated the visual detection of anurans. If so, this
could possibly explain the increase in species richness in
the PoF period. Nonetheless, most species and individuals
were recorded by acoustic signals, and new species contin-
ued to be recorded even at the end of the PoF period, when
the vegetation was already well regenerated. Furthermore,
Table 1. Frequency of occurrence of each species recorded at Lagoa Seca in the three study periods and their classication according
to this frequency.
Species
Frequency Classication
Pre–re Post–re 7 Post–re Pre–re Post–re 7 Post re
Ischnocnema juipoca 38% 4% 38% occasional rare occasional
Dendropsophus minutus 17% 38% – rare occasional –
Pithecopus ayeaye 21% 21% 25% rare rare occasional
Scinax curicica 42% 54% 63% occasional constant constant
Scinax squalirostris 38% 38% 29% occasional occasional occasional
Scinax rogerioi 21% 33% 13% rare occasional rare
Scinax fuscovarius – 4% – – rare –
Leptodactylus latrans 46% 38% 75% occasional occasional occasional
Leptodactylus jolyi 29% 25% 38% occasional occasional occasional
Leptodactylus furnarius – 4% – – rare –
Leptodactylus fuscus – 4% – – rare –
Leptodactylus cunicularius – 4% – – rare –
Physalaemus cuvieri 13% 21% – rare rare –
Physalaemus erythros 8% 8% 4% rare rare rare
Rhinella crucifer – 4% – – rare –
Figure 4. Species accumulation curves for the three study periods.
6
L O D et al.
higher species richness in the PoF period can hardly be ex-
plained by climatic factors, since the greatest richness was
recorded exactly during the period of lowest total rainfall
and average temperature (Fig. ), which are usually associ-
ated with lower amphibian activity (P J. , T-
et al. ).
An increase or maintenance of species richness aer iso-
lated re events seem to be common among animals from
the savanna formations of the Cerrado morphoclimatic do-
main. Such eects have been recorded for several groups,
including small mammals (B et al. , V
), birds (C A , R et al. ),
lizards (A et al. , C et al. ), snakes (S-
), termites ( S et al. ), and ground-
dwelling ants(N , F et al. , N et al.
). We can conclude from this that, overall, the fauna of
the Cerrado is adapted to the natural frequent re regime
that has shaped this domain for millennia. Several authors
have pointed that savanna formations with a dominance of
grasses, like rupestrian grasslands, evolved under a more
severe re regime (S J F , M
), and thus these formations can be expected to pos-
sess a fauna adapted to survive these re events as well.
Resistance of amphibian populations to re events may
be related to their dependence on humid environments.
Species in regions with marked seasonal rainfall tend to
restrict their activity to rainy periods (P J. ,
Tet al. , Pet al. ). is restriction in
temporal distribution is even greater in environments with
a predominance of temporary water bodies, such as in the
present study (Aet al., A , A
F , Bet al. , Aet al.
). erefore, during periods when res are more in-
tense and frequent, which usually corresponds to the end
of the dry season (M et al. ), anurans are usu-
ally protected by being hidden in overwintering shelters
such as burrows (N et al. ), ant and termite
mounds (M et al. ), and rocky crevices and
bromeliads of the abundant rocky outcrops present in the
rupestrian grasslands (e.g. P et al. , N
C, ).
e presence of ve species in low densities and fre-
quencies only during the period when the environment
was markedly modied, even with this period being dri-
er and less warm than the PrF, suggests that re may have
facilitated the immigration of species to the area. In fact,
re events can lead to benecial environmental changes for
some anuran species. Loss of vegetation and the resulting
lower evapotranspiration, for example, can lead to an el-
evation of the water table, the creation of small ponds and
the increase in volume of pre-existing ponds (P et
al. ). Furthermore, nutrient load resulting from lixi-
viation of ashes leads to increased productivity in water
bodies (S H ), and the increase in the
radiation at soil level and liberation of previously immobi-
lized mineral nutrients resulting from incineration of the
inert dry phytomass, leads to increased productivity in ter-
restrial systems (C , M et al. ).
So, species that can tolerate the increased exposure and the
simplied environment arising from re can benet from
their occurrence.
Another explanation for the increase in diversity aer
re events is the rapid change in vegetation structure that
occurs mainly during the initial stages of succession (B-
et al. , S et al. ). e vegetation struc-
ture at Lagoa Seca had dramatically changed into, and con-
tinuously beyond, the PoF period (Fig. ) is continu-
ous change in vegetation structure can potentially explain
the occurrence of new species even in the last month of
this period. Furthermore, the rapidly changing vegetation
structure immediately aer the re may explain why PoF
period was the only one in which the species accumulation
curve did not reach an asymptote, suggesting that more
species could be recorded with additional sampling eort.
Most of the species found exclusively during the PoF pe-
riod do indeed possess some resistance to environmental
alterations and are known to occur in extremely simplied
anthropogenic environments (A et al. , C
et al. , E S , S et al. ).
is resistance may be a result of a set of behavioral, mor-
phological, and physiological adaptations. For example,
the tadpoles of Scinax fuscovarius and Leptodactylus fus-
Table 2. Species encountered in each sampling event throughout the three study periods. Shaded columns represent sampling events
that resulted in no anuran records.
7
Impact of re on anurans of rupestrian grasslands
cus can tolerate high water temperatures (S N
) and, consequently, low oxygen levels, a situation that
can occur in small ponds in environments with low veg-
etation cover. E S () state that the
same can occur with tadpoles of L. cunicularius, L. fur-
narius and P. cuvieri. e burrowing capacity of species of
Leptodactylus from the L. fuscus group (L. fuscus, L. cuni-
cularius, L. furnarius and L. jolyi) likely provides resistance
since during re the temperature at cm below the soil sur-
face varies as little as °C (M et al. ). Further-
more, these species have foam nests, which are considered
adaptations for seasonal environments with unpredictable
rainfall because they prevent the dehydration of the eggs
(H ), in addition to providing a microenviron-
ment with higher thermal stability (D , D
G ).
Conversely, I. juipoca was recorded with lower constan-
cy and abundance (personal observation) in the PoF pe-
riod, and was probably the most negatively aected spe-
cies in the studied environment. According P et al.
() aquatic amphibians are more resistant to re events
than amphibians whose adults spend some time on dry
land. Ischnocnema juipoca has direct development and
uses bunch grasses as shelter, and vocalization and egg
deposition sites (E S , G
F ). us, this species may be susceptible to re-
moval of this microenvironment by re.
Currently, there is a global perception that re manage-
ment is important for the conservation of re-prone en-
vironments (F et al. ). Long periods of re
suppression can lead to dry biomass accumulation result-
ing in wildres of greater intensities that eventually aect
more sensitive phytophysiognomies that are usually pro-
tected from re, like those associated with rock outcrops
and riverine forests (N C , R
F , S et al. ). In the case of PEIT,
the success of the re suppression methods employed, in
the form of re brigades and environmental education
programs, have resulted in a great reduction of re events
when compared to the surroundings (F et al. ).
But this complete suppression could result in massive re
events, such as those of the years and , which
burned and of the reserve, respectively, impact-
ing less re-adapted phytophysiognomies, such as Semide-
ciduous forest (F et al. ). e use of prescribed
res as management tools in rupestrian grasslands can lead
to an increase in regional diversity by promoting a mosa-
ic of vegetation types and re regimes. However, deciding
whether to use a specic prescribed re regime is a com-
plex and dynamic process that must consider temporal, bi-
otic, abiotic, cultural, social, economic and historical fac-
tors (Fet al.).
Anuran sensitivity to re disturbance probably varies
among life stages, among populations of the same species
in dierent geographic regions and, certainly, among spe-
cies that evolved in dierent re regimes (P et al.
). In the case of anurans of rupestrian grasslands, the
present study recorded high tolerance to isolated res at the
study site, which is apparently associated with the timing
of the re event (dry season) and the presence of protected
wintering shelters like rock outcrops, burrows and termite
mounds. Although this study suggest that re management
can be a good conservation measure for rupestrian grass-
lands, data for this ecosystem are still too limited, and re-
searches in other areas and with other taxonomic groups
are needed to clarify questions regarding the ideal extent,
timing and frequency for this type of management.
Acknowledgements
We are grateful to all who helped us during the eldwork, and
especially B. A, B. Y. P. I, and S. D. R. We thank
R. N. F, L. B. N, Y. A, P. C. E
and C. A. C. B for the critical reading of earlier versions of
this work, and E. W for translation and careful revision this
manuscript. We thank the sta of Parque Estadual do Itacolo-
mi for the infrastructure and helpfulness. LOD and FRM thank
FAPEMIG and CAPES, respectively, for research grants. Collec-
tion of voucher specimens was performed with licenses from the
required environmental agencies (ICMBIO - and -,
IEF-MG / and /) and approval by the Committee
for Ethics in Research with Animals of the Universidade Federal
de Ouro Preto (CEUA /).
References
A, P. A., H. W J. P. P J. (): Anuran
temporal occupancy in a temporary pond from the Atlantic
Rain Forest, south-eastern Brazil. – Herpetological Journal,
: –.
A, L., A. K, M. V. S D. B (): Rhinel-
la crucifer. e IUCN Red List of reatened Species. – Avail-
able at: http://www.iucnredlist.org/details//.
A, M. J. D. C. I. W (): PERMANOVA,
ANOSIM, and the Mantel test in the face of heterogeneous
dispersions: What null hypothesis are you testing? – Ecologi-
cal Monographs, : –.
A, A. F. B., E. M. M. C, R. F. O, K. F, M.
F. S O. R. P J. (): Efeito de queimadas na fau-
na de lagartos do Distrito Federal. – pp. – in: M,
H. S., C. H. S B. F. S. D (eds): Impactos de queimadas
em áreas de Cerrado e Restinga. – Departamento de Ecologia,
Universidade de Brasilia.
A, C. (): Reproductive activity patterns of anurans in
two dierent altitudinal sites within the Brazilian Caatinga. –
Revista Brasileira de Zoologia, : –.
A, C., C. X. C M. A. G. C (): Anuran
assemblages in Castro Forest ponds (Sergipe state, Brazil):
Comparative structure and Calling activity patterns. – Herpe-
tological Journal, : –.
A, R. W. A. V. L. F (): Riqueza e densidade de
vocalizações de anuros (Amphibia) em uma área urbana de
Corumbá, Mato Grosso do Sul, Brasil. – Revista Brasileira de
Zoologia, : –.
B, C. A, R. J. S, M. C K M. M
(): Amphibians of an open Cerrado fragment in south-
eastern Brazil. – Biota Neotropica, : –.
8
L O D et al.
B, D. C., A. R. T. P, E. M. V R. P. B. H
(): Post-re succession of small mammals in the Cerrado
of central Brazil. – Biodiversity & Conservation, : –.
C, M. D., T. B. W D. J. R (): Prescribed re ef-
fects on structure in uneven-aged stands of loblolly and short-
leaf pines. –Wildlife Society Bulletin, : –.
C, P. D. G. C. L (): Eects of re and cattle
grazing on amphibians and lizards in northeastern Argentina
(Humid Chaco). – European Journal of Wildlife Research, :
–.
C, R. B. M. A. S. A (): Eect of re on sa-
vanna birds in central Brazil. – Ornitología neotropical, : –
.
C, G., L. B. N, D. S J. L ():
Leptodactylus furnarius. e IUCN Red List of reatened
Species. – Available at: www.iucnredlist.org/details//.
C, R. K. (): EstimateS: Statistical estimation of species
richness and shared species from samples. Version .
C, J. M., P. T. G B. R. A (): Pat-
terns of distribution, relative abundance, and microhabitat use
of anurans in a boreal landscape inuenced by re and timber
harvest. – Ecoscience, : –.
C, T. S., C. C. P T. W (): Bromeliaceae Juss.
nos campos rupestres do Parque Estadual do Itacolomi, Minas
Gerais, Brasil. – Rodriguésia, : –.
C, B. M., D. L. P, M. C. M. V G. R. C
(): Direct and short-term eects of re on lizard assem-
blages from a neotropical savana hotspot. – Journal of Herpe-
tology, : –.
C, L. M. (): Fire in the ecology of the Brazilian Cer-
rado. –pp – in: Goldammer, J. G. (ed.): Fire in the tropi-
cal biota: Ecological processes and global challenges. Ecologi-
cal Studies series. – Springer-Verlag, Berlin.
C, L. M. (): O conceito de bioma. – Acta Botanica
Brasilica, : –.
D S, O., L. B. A, V. M. T, L. P. P
R. R. J (): Eects of re on termite generic richness
in a savanna-like ecosystem (‘Cerrado’) of central Brazil. – So-
ciobiology, : –.
D, D. S. R. D. G (): ermal aspects of an-
uran foam nests. – Journal of Herpetology, : –.
D, J. R. (): Functions of the foam-nesting leptodactylid
Physalaemus pustulosus. – Herpetological Journal, : –.
E-S’, E. M., L. F R. A. M ():
Ecossistemas lacustres montanos: biodiversidade e grau de
vulnerabilidade à ação antrópica. – MG Biota, : –.
E, P. C. I. S (): Structure of an anuran
community in a montane meadow in southeastern Brazil: ef-
fects of seasonality, habitat, and predation. – Amphibia-Rep-
tilia, : –.
E, P. C. I. S (): Anfíbios da Serra do Cipó,
Minas Gerais – Brasil. – Editora PUC Minas, pp.
F, J. E. C., K. T. R, M. C. R, C. M. J, H.
F, A. C. O. N, A. A. C, F. A. M, J.
M. S A. K. M (): Fire in Rupestrian Grass-
lands: plant response and management. – pp – in:
F G. W. (ed.): Ecology and Conservation of Moun-
taintop grasslands in Brazil. – Springer International Publish-
ing, New York.
F T. L. M., C. B, M. P. B H. L. V-
(): Revisão dos efeitos do fogo sobre a fauna de for-
mações savânicas do Brasil. – Oecologia Australis, : –.
F, T. L. M., R. I. C H. L. V (): Efei-
to do fogo sobre a riqueza e abundância de formigas em área
de Cerrado no Brasil Central. – Biológico, : –.
F, M. A. G., M. G. P. L M. C. T. B. M ():
Análise multitemporal das mudanças no uso e ocupação do
Parque Estadual do Itacolomi (MG) através de técnicas de ge-
oprocessamento. – Revista Escola de Minas, : –
G A. A. K. G. F (): Reproduction and habi-
tat of ten Brazilian frogs (Anura). – Contemporary Herpetol-
ogy, : –.
G, A. M. J. R. P (): Patterns of geographic
distribution of some plant species from the Espinhaço Range,
Minas Gerais and Bahia, Brazil. – pp. – in: V, P.
E. W. R. H (eds): Proceedings of a workshop on Neo-
tropical distribution patterns. – Academia Brasileira de Ciên-
cias, Rio de Janeiro.
G, A. M., J. R. P R. M. H (): Espinhaço
Range region, eastern Brazil. – pp.– in: D, S. D.,
V.H. H, O. H-MB, J. V-L
A. C. H (eds): Centers of plant diversity: a guide and
strategy for their conservation, v. . e Americas. – World
Conservation Union, Cambridge.
G, R. E. (): Fire and aquatic ecosystems in forest-
ed biomes of North America. – Transactions of the American
Fisheries Society, : –.
G, R., D. A. B, G. A. G, K. J. F-
N. B. P (): Opposing responses to ecologi-
cal gradients structure amphibian and reptile communities
across a temperate grassland-savanna-forest landscape. – Bio-
diversity Conservation, : –.
H, J., R. M W. F (): Fire, ecosystems, and
people: a preliminary assessment of re as a global conserva-
tion issue. – e George Wright Forum, : –.
H W. R. (): e Adaptive Ecology of the Species Groups
of the Genus Leptodactylus (Amphibia, Leptodactylidae). –
Evolution, : –.
H, W. R. (): A new genus and species of frog from Bahia,
Brazil (Amphibia: Anura: Leptodactylidae) with comments on
the zoogeography of Brazilian campos rupestres. – Proceed-
ings of the Biological Society of Washington, :–.
H, W. A. A. G. M (): e Role of Fire in
Population Dynamics of Woody Plants. – pp. –. in: O-
, P. S. R. J. M (eds): e Cerrados of Brazil –
Ecology and Natural History of a Neotropical Savanna. – Co-
lumbia University Press, New York.
H, B. R. D. S. P (): Amphibian responses to
wildre in the western United States: Emerging patterns from
short-term studies. – Fire Ecology, : –.
K, M., J. G, C B, B. R F. R ():
World Map of the Köppen-Geiger climate classication updat-
ed. – Meteorologische Zeitschri, : –.
L, F. S. F., F. A. J P. C. E (): Status do con-
hecimento, endemismo e conservação de anfíbios anuros da Ser-
ra do Espinhaço, Brasil. – Revista Megadiversidade, : –.
M, D. B., C. K. D, S. A. J J. G. P ():
Amphibians and re in longleaf pine ecosystems: Response to
Schurbon and Fauth. – Conservation Biology, : –.
9
Impact of re on anurans of rupestrian grasslands
M, H. S., M. M. C. B A. C. M A. C.
(): e re factor. – pp. – in: O, P. S. R. J
M (eds): e Cerrados of Brazil – Ecology and Natu-
ral History of a Neotropical Savanna. – Columbia University
Press, New York.
M, A. C., H. S. M, I. D. O. D B. F. D. D
(): Soil and air temperatures during prescribed Cerrado
res in Central Brazil. – Journal of Tropical Ecology, : –.
M, H. S., M. N. S, W. N. N F. S. A ():
Fires in the Cerrado, the Brazilian savanna. – pp. –
in: C, M. A. (ed.): Tropical Fire Ecology: Climate
Change, Land Use, and Ecosystem Dynamics, vol. . – Spring-
er-Verlag, Berlin, Heidelberg.
M, A. R., L. G. C R. P. B (): Queimadas
podem alterar as assembleias de anuros? O caso das veredas na
Estação Ecológica Serra Geral do Tocantis. – Revista de Biolo-
gia Neotropical, : –.
M, A. G. (): Proteção contra o fogo e seu efeito na
distribuição e composição de espécies de cinco sionomias
de Cerrado. – pp. – in: M, H. S., C.H. S
B.F.S. D (eds): Impactos de queimadas em áreas de Cer-
rado e Restinga. – Departamento de Ecologia, Universidade
de Brasilia.
M, L. A., D. B. F, H. L. R. S N. J. S. S J.
(): A preliminary list of the herpetofauna from termite
mounds of the Cerrado in the upper Tocantins River valley. –
Papeis Avulsos de Zoologia, : –.
M, K. R., S. B. C S. H. S ():
Eects of Prescribed Fire on Herpetofauna in Bottomland
Hardwood Forests. – Southeastern Naturalist, : –.
N, M. A. (): Efeito do fogo na população de formigas
(Hymenoptera-Formicidae) em cerrado do Distrito Federal.
– pp. – in: Anais do Simpósio Impacto das Queimadas
sobre os Ecossistemas e Mudanças Globais. º Congresso de
Ecologia do Brasil. Brasília, DF.
N S. P. S. A. A. C (): Campo rupestre recém-
queimado na Chapada Diamantina, Bahia, Brasil: plantas de
rebrota e sementes, com espécies endêmicas na rocha. – Acta
Botanica Brasilica, : –.
N, F. S., T. C. L, M. C. A, A. C. R G. W. F-
(): Ant Community in Burned and Unburned Sites
in Campos Rupestres ecosystem. – Sociobiology, : –.
N, F., D. C. R-F F. L (): Burrow-
ing behavior of Dermatonotus muelleri (Anura, Microhylidae)
with reference to the origin of the burrowing behavior of An-
ura. – Journal of Ethology, : –.
O, J., F. G. B, R. K, P. L, P. R. M-
, R. B. O’, G. L. S, P. S, M. H. H. S-
H. W (): Vegan: Community ecology. – Av-
aliable online at: http://CRAN.R-project.org/package=vegan.
P, M. G. C. O. G. P (): Decline in a Population of
the treefrog Phyllodytes luteolus aer re. – Herpetological Re-
view, : –.
P, G. H. C. S (): Comunidade arbórea de uma
mancha orestal permanentemente alagada e de sua vegetação
adjacente em Ouro Preto-MG, Brasil. – Ciência orestal, :
–.
P, J. H., D. E. S, R. D. S, J. P. C,
L. J. V J. W. G (): Declining amphibian popu-
lations: the problem of separating human impacts from natu-
ral uctuations. – Science, : –.
P, J. H. K. H. M. W (): Putting declining
amphibians populations in perspective: Natural uctuations
and human impacts. – Herpetologica, : –.
P, D. S., R. B. B, E. J. H, C. A. P P. S. C
(): Fire and amphibians in North America. – Forest Ecol-
ogy and Management, : –.
P J., J. P. (): Distribuição espacial e temporal de an-
uros (Amphibia) em uma poça permanente na Serra de Paran-
apiacaba, sudeste do Brasil. – Revista Brasileira de Biologia,
: –.
P C. P. A., M. U C. F. B. H ():
Breeding activity patterns, reproductive modes, and habitat
use by anurans (Amphibia) in a seasonal environment in the
Pantanal, Brazil. – Amphibia-Reptilia, : –.
P, A., J. P. P J I. S (): A new species
of Scinax (Anura: Hylidae) from rocky montane elds of the
Serra do Cipó, Southeastern Brazil. – Zootaxa, : –.
R Core Team (): R: A language and environment for statisti-
cal computing. R Foundation for Statistical Computing, Vi-
enna, Austria. – Available at: www.r-project.org.
R, M. G., C. Z. F M. M. D (): e inuence
of re on the assemblage structure of foraging birds in grass-
lands of the Serra da Canastra National Park, Brazil. – Anais
da Academia Brasileira de Ciências, : –.
R, M. C. J. E. C. F (): Uma abordagem
histórica do fogo no Parque Nacional da Serra do Cipó, Minas
Gerais, Brasil. – Biodiversidade Brasileira : –
R C. F. D., C. V. A, V. A. M D. V
(): Eects of a re on a population of treefrogs (Scinax cf.
alter, Lutz) in a restinga habitat in southern Brazil. – Brazilian
journal of biology, : –.
S J, J. J. M. R. F (): Changes in tree density and
species composition in a protected Trachypogon Savanna pro-
tected for years. – Acta Oecologica, : –.
S, R. J. (): História natural e ecologia das serpentes de
Cerrado da região de Itirapina. – PhD esis, Universidade
Estadual de Campinas, Campinas, SP, pp.
S, C. E. G. R., G. R. C, H. G. C, D. M. A-
, J. A. N, R. W. A, P. M. S. R, E. I.
F F, A. F. S. P, P. C. B A. V.
N (): e physical environment of Rupestrian Grass-
lands (Campos Rupestres) in Brazil: geological, geomorpho-
logical and pedological characteristics, and interplays. – pp
– in: F, G. W. (ed.): Ecology and Conservation
of Mountaintop grasslands in Brazil. – Springer International
Publishing, New York.
S, A. J. R. N (): Tolerance to high temperatures
in tadpoles of Leptodactylus fuscus e Hyla fuscovaria in tem-
porary ponds (Amphibia, Leptodactylidae, Hylidae). – Zoolo-
gischer Anzeiger, : –.
S, I. B., M. B. S, I. B. F T. T
(): Fogo e artesanato de capim-dourado no Jalapão – usos
tradicionais e consequências ecológicas. – Biodiversidade Bra-
sileira, : –.
S, J. M. J. E. F (): Eects of prescribed burn-
ing on amphibian diversity in a southeastern U.S. National
Forest. – Conservation biology, : –.
10
L O D et al.
S J. M. J. E. F (): Fire as friend and foe of
amphibians: A reply. – Conservation Biology, : –.
S, M. V., U. C, C. A. G. C, T. G, C. F.
B. H, P. C. A. G, B. V. M. B J. A. L-
(): Brazilian amphibians: list of species. – Herpetolo-
gia Brasileira, : –.
S, D. L. M. V. S (): Conservação de anfíbios
no Brasil. – Megadiversidade, : –.
S, M. F., R. G, L. P. Q, C. S, R. T.
P C. E. H (): Recent assembly of the
Cerrado, a neotropical plant diversity hotspot, by in situ ev-
olution of adaptations to re. – Proceedings of the National
Academy of Sciences of the United States of America, :
–.
S, J. J., M. H. A. O. S M. I. S. L (): Twenty
years of post-re plant succession in a “cerrado”, São Carlos,
SP, Brazil. – Brazilian Journal of Biology, : –.
S, C. N. F. R. H (): Phosphorus and nitrogen
dynamics in streams during a wildre. – Journal of the North
American Benthological Society, : –
S, J. L. M. M., J. S. T V. L. F (): Diet of
Leptodactylus fuscus (Amphibia: Anura: Leptodactylidae) in
the Pantanal of Miranda river, Brazil. – Biota Neotropica, :
–.
T, L. F., J. Z, C. F. B. H (): Distribuição es-
pecial e temporal de uma comunidade de anfíbios anuros do
município de Rio Claro, São Paulo, Brasil. – Holos Environ-
ment, : –.
V, E. M. (): Small mammal communities and re in the
Brazilian Cerrado. – Journal of Zoology, : –.
W-T, E., M. M, J. H, R. F. V, E.
W, N. P J. C. A (): Frog communi-
ties in re-disturbed forests of the Peruvian Amazon. – Her-
petological Bulletin, : –.
Appendix I
Voucher specimens
Dendropsophus minutus: LZVA; Ischnocnema juipoca:
LZV–A, A, A, A, A; Leptodactylus la-
trans: LZVA; Leptodactylus cunicularius: LZVA; Lep-
todactylus jolyi: LZVA; Physalaemus cuvieri: LZVA,
A; Physalaemus erythros: LZVA, A; Rhinella cru-
cifer: LZVA; Scinax curicica: LZVA, –A (juve-
nile), A; Scinax fuscovarius: LZVA; Scinax rogerioi: LZ-
VA, –A (juvenile), –A; Scinax squalirostris:
LZV–A.
