( PDF ) Estrutura temporal e espacial de comunidades de anuros em riachos na mata de RPPN Serra do Caraça (Catas Altas, Minas Gerais)

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Lilian Gomes Afonso

ESTRUTURA TEMPORAL E ESPACIAL DE COMUNIDADES DE

ANUROS EM RIACHOS DE MATA NA RPPN SERRA DO CARAÇA

(CATAS ALTAS, MINAS GERAIS)

Orientadora: Dra. Paula Cabral Eterovick

Dissertação apresentada ao Programa

de Pós-Graduação em Zoologia de

Vertebrados da Pontifícia Universidade

Católica de Minas Gerais como parte

dos requisitos necessários à obtenção

do título de mestre em Zoologia de

Vertebrados

Belo Horizonte

2005

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ÍNDICE

Agradecimentos ……………………………………………………….......…… 4

Introdução geral ……………………………………………………….......…… 6

Bibliografia …………………………………………………………..…….10

Capítulo 1

– Spatial and temporal distribution of anuran amphibians in streams at

the RPPN Serra do Caraça, southeastern Brazil........................................................15

Resumo ……………………………………………….……………....16

Abstract ................................................................................................ 17

Introduction ...............................................................................................18

Study site ................................................................................................20

Methods ...............................................................................................22

Results ...............................................................................................24

Discussion ................................................................................................29

Acknowledgements ................................................................................................34

References ................................................................................................35

Capítulo 2

– Microhabitat choice and partitioning by anurans in forest streams in

southeastern Brazil ………………………………………………………….…....41

Resumo ...................................................................................................42

Abstract .................................................................................................43

Introduction .................................................................................................44

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Study site ..................................................................................................45

Methods ...................................................................................................47

Results ....................................................................................................51

Discussion ...................................................................................................55

Acknowledgements ..................................................................................................59

References ..................................................................................................60

Appendix ...................................................................................................64

Conclusões gerais ...................................................................................................65

Agradecimentos

Um agradecimento especial aos meus adoráveis pais e ao meu irmão que sempre me

apoiaram em tudo que precisei e em tudo que quis fazer. Muito obrigada pelos momentos

de carinho e pela alegria com as minhas vitórias!!!

A minha orientadora Paula Cabral Eterovick pela dedicação, carinho, incentivo,

amizade e pelos momentos divertidos que passamos no campo. Obrigada de coração!!!

A inesquecível Luciana Barreto Nascimento por ter me ensinando tanto sobre os

“sapinhos” e pelo carinho com que sempre me tratou.

A Katia e Milena pela ótima companhia no campo e pelas constantes brincadeiras o

que tornou o trabalho muito mais divertido. Adorei conhecer vocês.

Aos amigos do Laboratório de Ecologia Evolutiva de Anfíbios e Répteis:

Arquimedes, Camilinha, Carlos, Izabela e Paulinho pela ajuda nos trabalhos de campo e

pela diversão garantida. Valeu!!!

Aos amigos que fiz no Setor de Herpetologia do Museu de Ciências Naturais da

PUC/MG: Emiliane (Mimi), Pedro, Filipe, Rafael (Piu-Piu), Bruno, Breno, Conrado,

Daniel, Mauro, Alexandre, Débora e Laura.

Ao pessoal da RPPN Serra do Caraça que sempre nos receberam e trataram com

tanto carinho: Padre Célio, as meninas da recepção, as cozinheiras pela maravilhosa

comida, a bióloga Consuelo Paganini por ter facilitado a realização do trabalho e em

especial ao Daniel pelas conversas nas noites mais frias tomando um chá e comendo

pipoca.

Ao Gustavo pelas constantes conversas e ajuda dedicada. Obrigada pela paciência,

pelo companheirismo e pelo incentivo de sempre o que contribuiu muito para o meu

crescimento profissional e pessoal. Muito obrigada!

Aos meus grandes amigos Tati, Marcílio, Luciana, Cassius e Fernanda por serem

pessoas tão especiais e verdadeiras.

Ao Rafael pelo incentivo e amizade.

Ao Joaquim (Quincas) pela confecção dos mapas.

Ao Fundo de Incentivo a Pesquisa (Fip) da Pontifícia Universidade Católica de

Minas Gerais pelo auxílio financeiro nos trabalhos de campo.

Ao Ibama pela licença concedida de nº 128/2004 para trabalhar na RPPN Serra do

Caraça.

Introdução geral

Comunidades são agrupamentos de espécies moldados por interações bióticas

(Pianka 1973) que coexistem no espaço e no tempo (Begon et al. 1996). O principal

objetivo de estudos de ecologia de comunidades é identificar como os fatores abióticos e

bióticos determinam a distribuição e abundância das espécies (Norton 1991).

A coexistência de espécies em uma taxocenose é possibilitada, dentre outros fatores,

pela partição de recursos disponíveis no ambiente (Blair 1961, Duellman e Pyles 1983,

Aichinger 1987, Cardoso et al. 1989, Haddad e Sazima 1992, Pombal 1997, Eterovick e

Sazima 2000, Eterovick e Barros 2003), que é determinada tanto pelos fatores ecológicos

quanto históricos, uma vez que espécies relacionadas filogeneticamente costumam

apresentar os mesmos nichos ecológicos (Cadle e Greene 1993). Duellman (1989) sugere

ainda que para explicar o padrão observado na partilha de recursos deve-se levar em

consideração, além desses fatores, a própria história do ambiente. A existência ou a

aparente falta de padrões na estrutura das comunidades podem refletir condições climáticas,

geológicas ou outras forças que atuaram no passado e que não agem mais nos dias atuais

(Ricklefs 1987).

A partilha de recursos pode ser influenciada pelas preferências das espécies (Wisheu

1998) em relação a alimentação, uso do espaço e época de atividade (Pianka 1973), e

resulta de necessidades fisiológicas dos organismos e interações bióticas dentro do

ecossistema (Zweimüller 1995).

A segregação das espécies nas comunidades pode ocorrer em função da estrutura da

vegetação, da durabilidade dos riachos (temporários ou permanentes) e da movimentação

da água (lótico ou lêntico) (Bernarde e Anjos 1999), a escolha destes locais de reprodução

pelas espécies de anuros está relacionada com adaptações morfológicas, fisiológicas e

comportamentais (Crump 1971, Pough et al. 1977, Cardoso et al. 1989). Além dessas

diferenças no ambiente para reprodução (Rossa-Feres e Jim 1994), há diferenças nos sítios

(Duellman 1967, Cardoso et al. 1989), na temporada e no turno de vocalização (Cardoso e

Haddad 1992, Rossa-Feres e Jim 1994, Pombal 1997) que também podem determinar a

partilha de recursos. A variedade de modos reprodutivos tem implicações diretas na

diversidade de espécies ocupando uma determinada área e na utilização dos recursos

ambientais (Crump 1982). Diferenças na utilização desses recursos podem reduzir a

competição e permitir que uma maior variedade de espécies consiga coexistir (MacArthur

1972).

A coexistência entre as espécies é possível não só por elas apresentarem padrões

distintos quanto à ocupação ambiental, mas também porque demonstram distribuição

estacional diferenciada (Duellman 1978). Heatwole (1982) indica que, para anfíbios, o

padrão sazonal parece ser mais importante que o espacial no processo de isolamento

reprodutivo.

As variáveis ambientais precipitação, temperatura (Toft e Duellman 1979) e nível

dos corpos d’água influenciam o comportamento dos anuros (Heyer et al. 1994). A época

do ano e a duração do período de atividade das espécies são determinadas principalmente

pela temperatura nas regiões temperadas e pela precipitação nas regiões tropicais e sub-

tropicais (Duellman e Trueb 1994), mas deve-se considerar a partilha temporal como um

mecanismo secundário de isolamento reprodutivo porque, em geral, as espécies

neotropicais apresentam grande sobreposição na estação chuvosa e não hibridizam (Blair

1961), desta forma o espaço acústico poderia ser o fator de maior importância como

determinante deste isolamento (Pombal 1997, Bernarde e Anjos 1999).

Diversos registros de declínios levaram à hipótese de que os anfíbios sofrem com

maior intensidade do que outros grupos de vertebrados os efeitos das mudanças ambientais

impostas pelos homens (Beebee 1996). Há possibilidade de que o desaparecimento de

populações de anuros reflita degradação do ambiente, e este fenômeno parece estar

ocorrendo em escala mundial (Vitt et al. 1990, Lips 1998, Houlanhan et al. 2000).

Entretanto faltam evidências sobre a verdadeira causa de muitos declínios, principalmente

pela falta de conhecimento sobre a ecologia das espécies, sobretudo na região tropical

(Beebee 1996).

A grande diversidade de ambientes existentes no estado de Minas Gerais, aliada a

um panorama neotropical, possibilitam a ocorrência de uma alta diversidade de anfíbios,

ultrapassando 200 espécies, o que representa cerca de 1/3 do total registrado para o país

(Costa et al. 1998, SBH 2005).

Estudos abordando partilha de recursos em comunidades de anuros na região

sudeste do Brasil incluem os trabalhos de Cardoso et al. (1989), Cardoso e Haddad (1992),

Nascimento et al. (1994), Rossa-Feres e Jim (1994), Pombal (1997), Feio et al. (1998),

Eterovick e Sazima (2000), Bertoluci e Rodrigues (2002a, 2002b), Eterovick e Barros

(2003). Heyer et al. (1988) indicam a necessidade de estudos sobre a anurofauna nesta

região não só pela diversidade de ecossistemas encontrados, mas também devido à

descaracterização ambiental que a região vem sofrendo, decorrente de eventos naturais ou

provocados pela ação humana. A elaboração de estratégias de conservação depende de uma

boa base teórica, ou as medidas tomadas podem ser ineficazes (Beebee 1996).

Este estudo foi realizado com o objetivo de verificar aspectos da estrutura espacial e

temporal em comunidades de anuros na RPPN Serra do Caraça (Catas Altas, MG). No

capítulo 1, a distribuição das espécies pelos riachos foi relacionada com o volume de cada

riacho e a distribuição temporal relacionada com fatores climáticos (temperatura e

pluviosidade). O capítulo 2 aborda o uso espacial com base na diversidade de

microambientes e seu uso pelos anuros.

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214pp.

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habitats de vocalização em uma taxocenose de anuros (Amphibia) da Mata Atlântica

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ecological structure of neotropical snake assemblages, pp.281-293. In: Ricklefs, R.E.

and Schluter, D. (eds). Historical and geographical determinats of community

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comunidades de anfíbios (Anura) no sudeste do Brasil. Revista Brasileira de Biologia

49:241-249.

Cardoso, A. J. and C. F. B. Haddad. 1992. Diversidade e turno de vocalizações de anuros

em comunidade neotropical. Acta Zoologica Lilloana 41:93-105.

Costa, C. M. R., G. Herrmann, C. S. Martins, L. V. Lins, and I. R. Lamas (org.). 1998.

Biodiversidade em Minas Gerais: um atlas para sua conservação. Fundação

Biodiversitas, Belo Horizonte, MG.

Crump, M. L. 1971. Quantitative analysis of the neotropical herpetofauna. Occasional

Papers of the Museum of Natural History 3:1-62.

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Duellman, W. E. 1967. Courtship isolating mechanisms in Costa Rican hylid frogs.

Herpetologica 23:169-183.

Duellman, W. E. 1978. The biology of an equatorial herpetofauna in Amazon Ecuador.

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communities. Copeia 1983:639-649.

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Springer-Verlag, New York.

Duellman, W. E. and L. Trueb. 1994. Biology of amphibians. Mcgraw-Hill, New york,

670pp.

Eterovick, P. C. and I. Sazima. 2000. Structure of an anuran community in a montane

meadow in southeastern Brazil: effects of seasonality, habitat and predation.

Amphibia-Reptilia 21:439-461.

Eterovick, P. C. and I. S. Barros. 2003. Niche occupancy in south-eastern Brazilian tadpole

communities in montane-meadow streams. Journal of Tropical Ecology 19:1-10.

Feio, R. N., U. M. L. Braga, H. Wiederhecker, and P. S. Santos. 1998. Anfíbios anuros do

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Biologia 57:583-594.

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Peru: a preliminary analysis of community structure. Herpetologica 35:71-77.

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of decay. BioScience 40:418-418.

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CAPÍTULO 1

Spatial and temporal distribution of anuran amphibians in streams

at the RPPN Serra do Caraça, southeastern Brazil

Resumo

A comunidade de anuros da RPPN Serra do Caraça, localizada no município de

Catas Altas (MG), foi estudada no período de agosto de 2003 a outubro de 2004 em oito

riachos permanentes de mata. Foram registradas 19 espécies de anuros pertencentes a

quatro famílias: Bufonidae (10.53%), Centrolenidae (5.26%), Hylidae (63.16%) e

Leptodactylidae (21.05%). Houve uma relação negativa significativa entre o número de

espécies presentes e o volume dos riachos. Não houve uma relação entre os fatores

abióticos (precipitação e temperatura) e a diversidade de espécies por mês e a diversidade

de espécies vocalizando, mas os anuros apresentaram diferenças quanto à distribuição

temporal. Das 19 espécies encontradas, 12 apresentaram atividade de vocalização e para 10

espécies foram encontrados indícios de atividade reprodutiva como fêmeas ovadas, pares

em amplexos, desovas, girinos e jovens recém metamorfoseados. O tamanho dos riachos

parece ser um importante fator determinando a riqueza de espécies de anuros local, a

relativa estabilidade climática dos riachos de mata favorecem as espécies de anuros com

período reprodutivo longo bem como o aumento do período reprodutivo de espécies mais

flexíveis.

Palavras chaves: Anfíbios anuros, distribuição temporal, fatores abióticos.

Abstract

Anuran communities were studied at eight permanent forest streams located in the

Reserva Particular do Patrimônio Natural (RPPN) Serra do Caraça, municipality of Catas

Altas, Minas Gerais state, southeastern Brazil, from August 2003 to October 2004. A total

of 19 anuran species was recorded in four families: Bufonidae (10.53%), Centrolenidae

(5.26%), Hylidae (63.16%), and Leptodactylidae (21.05%). Number of species present in

the streams was negatively related to stream volume. Rainfall and mean monthly

temperatures were not related to anuran species diversity or diversity of species with calling

males per month, though species differed in their temporal distributions. From the 19

species recorded, 12 exhibited calling activities during the study period and 10 were

assumed to have reproduced based on records of gravid females, amplexed pairs, egg

clutches, tadpoles, or post metamorphic froglets, considered as indicatives of reproduction.

Stream size seems to be an important factor determining local anuran species richness,

while the relatively stable climatic conditions of forested sites seems to favor anuran

species with long breeding periods as well as the increase of breeding periods of more

flexible species.

Key Words: Anura, temporal distribution, abiotic factors

Introduction

The co-existence among populations of different species at a given site is

possible due to specific behavior and interspecific interactions that influence social

organization, spatial and temporal distribution (MacNally, 1979), contributing to a higher

local species diversity. Competition, predation, and factors independent of biotic

interactions, such as specific requirements, were considered as the main forces shaping

anuran communities by Toft (1985).

The Theory of Island Biogeography predicts the number of species to increase with

area and decrease with isolation level of an island (MacArthur and Wilson, 1967), what

may happen, for instance, because larger areas may include a larger variety of habitat types

and resources (Williams, 1964). Zimmerman and Bierregaard (1986) found species-area

relationships to be of little importance in anuran communities at Central Amazon, the

availability of suitable reproductive sites being the most important factor determining most

species distribution. Considering size variation within a given type of reproductive site,

Heyer et al. (1975) hypothesized tadpole species richness to be higher at ponds of

intermediate size, due to a trade-off between pond permanency and predation pressures.

Environmental heterogeneity is important to determine the number of species that

can use a given habitat (Cardoso et al., 1989), so that higher species richness can be

expected in an area with more microhabitats and ecological niches (MacArthur, 1968). In

anurans, different reproductive modes may occur among sympatric species (Duellman,

1989) and aid to resource partitioning. Shared resources may include calling sites,

oviposition sites, acoustic space, annual and daily calling periods (Crump, 1971; Hödl,

1977; Cardoso and Haddad, 1992; Pombal, 1997). During the larval stage, anurans may

differ in habitats and microhabitats used food type and size, daily and annual activity

periods (Wild, 1996). The diversity of reproductive modes directly influences species

diversity and patterns of resource use (Crump, 1982). When partition of resources related to

reproduction fail or do not exist, species hybridization may take place (Haddad et al., 1990;

Haddad et al., 1994; Pombal, 1997).

In temperate regions, temperature is the main abiotic factor controlling anuran

reproductive activities, while rainfall assumes a greater importance in tropical regions

(Duellman and Trueb, 1994). Anuran communities occurring at sites with low annual

humidity variations include several species that reproduce continuously or sporadically

throughout the year (Crump, 1974; Duellman, 1978; Wiest, 1982). At seasonal neotropical

sites, the occurrence of two well defined seasons, a dry and a wet one, is expected to

promote some variation regarding anuran species temporal distribution.

Studies on anuran communities are scarce in Brazil once we consider the great

amphibian richness in the country (775 species; SBH, 2005) and are badly needed for

conservation purposes (Eterovick et al., 2005). Knowledge on abiotic factors that influence

the structure of anuran communities may be important to understand how species can keep

co-existing and how human influence may disturb their assemblages. Such knowledge is

badly needed once several amphibian populations are suspected to be declining in Brazil

(Eterovick et al., 2005), as well as many other countries (Lips, 1998; Lips et al., 2003;

2004; Young et al., 2001; 2004).

Attempting to improve the knowledge on neotropical amphibian community

organization, we aimed to (1) determine the species composition of anuran communities

occurring at eight streams at the RPPN Serra do Caraça, (2) test whether local species

richness is influenced by stream volume, (3) test whether abiotic factors such as rainfall and

temperature influence the temporal distribution of species activities, and (4) look for

patterns of seasonal variations in community composition.

Study site

The Reserva Particular do Patrimônio Natural (RPPN) Serra do Caraça is located in

the municipality of Catas Altas (20º 05’S, 43º 29’W), Minas Gerais state, southeastern

Brazil. The reserve includes 10187.89 ha in the southern portion of the Espinhaço mountain

range, between 850 and 2070 m above sea level (Fig. 1). The region is formed by the

orographic systems of Minas Gerais and Bahia states (Derby 1966), representing a contact

zone between the Cerrado and Atlantic Forest biomes in its southern portion and a

transition zone between both biomes in its northern portion (Giulietti and Pirani 1988,

Giulietti et al. 1997).

The region has two seasons, a dry from April to September and a wet, from October

to March (Fig. 2).

Figure 1. Location of the RPPN Serra do Caraça in Minas Gerais state,

southeastern Brazil.

Figure 2. Mean monthly rainfall (solid line), maximum and minimum temperatures

(dotted lines) at the RPPN Serra do Caraça, southeastern Brazil, from August 2003

to October 2004.

Para Belo Horizonte

Para BR-381

P ara Mariana

P ara A lvinóp olis

A lvinó po lis

R io Piracicaba

São Gonçalo do Rio Abaixo

O uro Preto

R io Acima

Itabirito

M a riana

20º00'

43 º30 '

43 º15 '

C aeté

Ba rã o de Cocais

Sa nta Bárbara

C ata s Altas

0 5 10km

0 150km

Month

Maximum and minimum temperature

(ºC)

100

120

140

160

180

Rainfall (mm)

Methods

The inventory of anuran species in the studied streams was conducted through

monthly three-day samplings from August 2003 to October 2004. Anuran species were

searched for during the day (diurnal frogs and tadpoles) and at night (nocturnal species;

from sunset to about 11:00 pm). Eight permanent forest streams with varied widths and

water volumes were sampled (Fig. 3) throughout 150 m sections marked along their

courses.

Data on maximum and minimum temperatures were obtained from the

Meteorological Station of João Monlevade municipality (Minas Gerais state) located 47.5

km from the study site. Air and water temperatures and rainfall were measured in the field

with a thermometer (to the nearest 0.5ºC) and a rain gauge, respectively.

Adult anurans were located through visual search or auditory inspection for their

calls. Gravid females, amplexed pairs, egg clutches, tadpoles, and post metamorphic

froglets were considered as indicatives of the occurrence of reproduction at the site.

Species that could not be identified in the field had some individuals collected and

fixed following Heyer et al. (1994), for posterior identification. Specimens were deposited

in the herpetological collection of the Museu de Ciências Naturais of the Pontifícia

Universidade Católica de Minas Gerais.

Figure 3. Location of the eight sampled streams at the RPPN Serra do

Caraça (Catas Altas municipality, Minas Gerais state, southeastern Brazil).

To estimate monthly species diversity (H) we used Shannon's diversity index

(Pielou 1975):

H = - ∑ pi log

where pi represents the proportion of individuals of species “i” recorded per month,

in relation to total number of individuals recorded in the month considered.

Stream volume was estimated multiplying the length of the sampled section (150 m)

by mean stream width and depth. Mean stream width was calculated based on ten

measurements (taken every 15 m in the sampled section) and mean stream depth was

calculated based on 75 measurements (taken every 2 m in the sampled section, at varied

distances from the right margin: 1/6, 1/3, 1/2, 2/3, and 5/6 stream width at the measured

point). The number of anuran species present and the number of species calling in each

stream were related to stream volume using adjustment curves (Zar 1999). Data normality

was tested for through residual analyses.

To evaluate the relationships among mean air and water temperatures, monthly

rainfall and species diversity per month, as well as diversity of species with calling males

per month, we used multiple linear regressions (Zar 1999). All the statistical tests were

conducted using the software BioEstat (BioEstat 2003).

Results

During the study period, we recorded 19 anuran species in the families Bufonidae

(10.53%), Centrolenidae (5.26%), Hylidae (63.16%), and Leptodactylidae (21.05%) at the

RPPN Serra do Caraça (Table 1). Species distribution was not uniform among streams,

Stream 5 (see Fig. 3) being the one with the greatest species richness (n = 9) and Stream 6

sheltering only Hylodes uai (Table 1).

Anuran species richness was negatively related to stream volume (R

= 0.760, F =

23.166, p < 0.004, Fig. 3A). Residuals of the relationship between species richness and

stream volume showed that data had normal distribution (p = 0.668). By the other side, the

residuals of the relationship between species with calling males and stream volume

indicated that data did not have normal distribution (p = 0.010), maybe due to the lower

sample size, so it was not possible to analyse these data. Therefore, a tendency of increase

in the number of species with calling males with the decrease of stream volume could be

noticed (Fig. 5), as it happened with total number of species.

Table 1. Distribution of 19 anuran species in eight forest streams (S1 - S8) and estimated volume of sampled

stream sections at the RPPN Serra do Caraça, southeastern Brazil.

Species

Bufonidae

Bufo pombali

Baldissera, Caramaschi & Haddad,

2004

Bufo rubescens

Lutz,1925

Centrolenidae

Hyalinobatrachium

cf.

eurygnathum

Hylidae

Hyla albopunctata

Spix, 1824

Hyla

sp.

(gr.

circumdata

)

Hyla faber

Wied-Neuwied, 1821

Hyla martinsi

Bokerman, 1964

Hyla minuta

Peters,1872

Hyla nanuzae

Bokermann & Sazima, 1973

Hyla polytaenia

Cope, 1868

Phyllomedusa burmeisteri

Boulenger, 1882

Scinax luizotavioi

(Caramaschi &

Kisteumacher, 1989)

Scinax machadoi

(Bokermann & Sazima, 1973)

Scinax

aff.

Perereca

Scinax

sp. (gr.

ruber

)

Leptodactylidae

Crossodactylus

sp.

Hylodes uai

Nascimento, Pombal & Haddad, 2001

Physalaemus

aff.

olfersii

Proceratophrys boiei

(Wied-Neuwied, 1824)

Species richness

Estimated volume of sampled section (m

)

47.08

17.27

118.44

19.37

72.18

235.63

104.02

283.66

Species diversity was not related to monthly rainfall or mean air and water

temperatures (R

= 0.077, F

3,11

= 1.3887, p = 0.298). Diversity of species with calling

males was not related to these climatic parameters either (R

= 0.1862, F

3,11

= 2.0679, p =

0.162).

Figure 4. Relationship between estimated volume of stream sampled

sections (m

) and anuran species richness at the RPPN Serra do Caraça,

southeastern Brazil.

Figure 5. Relationship between estimated volume of stream sampled

sections (m

) and number of anuran species with calling males at the

RPPN Serra do Caraça, southeastern Brazil.

From the 19 anuran species recorded at the studied streams, 12 were observed in

calling activities (Table 2). Some species showed prolonged calling periods, such as Hyla

minuta, H. nanuzae, Scinax luizotavioi and Crossodactylus sp.. For these species, calling

males were recorded year-round. Other species were opportunistic, being active in periods

with suitable climatic conditions throughout the year, such as Bufo pombali, Hyla faber, H.

martinsi, and H. polytaenia, which chose the hottest and wettest period; Hylodes uai, which

was active by the end of the rainy season and the onset of the dry season, and

Proceratophrys boiei, which called with the first rains of the year (Table 2). Data obtained

for Phyllomedusa burmeisteri and Hyalinobatrachium cf. eurygnathum were not enough to

determine specific activity periods due to small sample size.

Although emission of mating calls may be considered as an indicative of

reproduction by some authors, the occurrence of calling activities does not necessarily

mean that the species reproduced or will actually reproduce (Cardoso and Haddad, 1992).

Thus, we preferred to be conservative and not to consider calling males as an indicative of a

species reproduction. We then detected reproductive activities for 10 species: Bufo

pombali, Hyla sp. (gr. circumdata), H. faber, H. martinsi, H. nanuzae, Scinax machadoi,

Scinax sp. (gr. ruber), S. luizotavioi, Crossodactylus sp. and Hylodes uai (Table 2).

Inferences could not be made on the temporal distribution of reproductive activities

of Bufo pombali, Hyla sp. (gr. circumdata), H. faber, Scinax sp. (gr. ruber) and Hylodes uai

due to the small number of individuals recorded for these species.

Table 2. Activities and life stages recorded for the anuran species at the RPPN Serra do Caraça, southeastern

Brazil, from August 2003 to October 2004: (

•

) silent individuals; (M) calling males; (F) gravid females; (a)

amplexed pairs; (*) egg clutch;

(T) tadpoles, and (fr) post metamorphic froglet.

Species

Aug

Sep

Oct

Nov

Dec

Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

Sep

Oct

Bufo pombali

••

B. rubescens

••

Hyalinobatrachium

cf. eurygnathum

Hyla albopunctata

••

Hyla sp. (gr.

circumdata)

••

Hyla faber

H. martinsi

••

MFT

••

H. minuta

H. nanuzae

••

Mfr

H. polytaenia

••

Phyllomedusa

burmeisteri

Scinax aff.

perereca

••

S. machadoi

••

Scinax sp. (gr.

ruber)

S. luizotavioi

MFfr

Crossodactylus sp.

MFT

••

MFT

Hylodes uai

Physallaemus aff.

olfersii

••

Proceratophrys

boiei

Discussion

Density of vegetation cover along stream margins constitute an important factor

influencing choice of reproductive sites by anurans (Werner and Glennemeier, 1999). The

greatest proportion of hylids recorded in the streams may be related to the highest diversity

of calling sites available for this group, since the presence of all vegetation strata provides

several microhabitats to be explored by these climbing treefrogs. The presence of adhesive

discs at hylid fingertips adapts species of this family to explore the vegetation vertically

(Cardoso et al., 1989), besides being able to explore also other microhabitats such as rocks

and leaf litter, as other frogs do.

The differential use of sampled streams by anuran species reflects selection of

breeding habitats, known to occur in this group (Collins and Wilbur, 1979; Gascon, 1991).

Stream 5 has a large backwater that function as a permanent pond and sheltered both

species typical of forest streams and species that reproduce in open habitats such as Hyla

minuta, Hyla polytaenia and Phyllomedusa burmeisteri (see Cardoso et al., 1989). The

remaining streams were relatively uniform throughout the sampled sections and bordered

by all vegetation strata, varying in size among them, though.

Variation of habitat types, interspecific interactions, disturbances, colonization

processes, local, regional and continental selection and evolution processes may all inspire

models proposed to understand stream communities (Ricklefs and Schluter, 1993). Larger

fragments are supposed to shelther greater habitat diversity and are, thus, expected to

shelther greater species diversity (Lack, 1976). Alternatively, larger fragments may suffer

less species extinctions and more colonization events, resulting in a higher species richness

(MacArthur and Wilson, 1967). In the studied streams, the negative relationship between

stream sampled section estimated volume and anuran species richness stresses the influence

of habitat variability on species distribution, since species seem to choose the most suitable

breeding habitats along a stream size gradient, most species preferring smaller streams. The

same pattern was recorded by Eterovick (2003) in streams at the Serra do Cipó, a site close

to the RPPN Serra do Caraça, in the southern portion of the Espinhaço mountain range.

Both works, though, point to the hypothesis that Island Biogeography Theory does not

apply to anuran species in streams.

Zimmerman and Simberloff (1996) stressed that the evolution of neotropical

anurans favored species that breed in lenthic water bodies, contrary to the pattern observed

at southeastern Asia, because ancestral lineages that evolved in these two continents had

adaptations to lenthic and lotic aquatic habitats, respectively. Parris and McCarthy (1999)

found anuran assemblages to be richer in larger streams in Australia. By the other side,

anuran species in the RPPN Serra do Caraça may prefer to breed in small sections of

streams, which are washed by strong currents just during the rainfall peaks, since these

species have few adaptations to live in strong currents during their larval stage, as it also

happens at the Serra do Cipó (Eterovick, 2003). We suppose that living downstream, in

larger sections with larger water volume, would imply in a greater demand on tadpoles for

adaptations to swim against the current, attach themselves to substrates and search for

shelters in shallow microhabitats. Alternatively, tadpoles lacking adaptations to life in

strong currents might have more opportunities to escape the occasional relatively strong

water flows that wash small streams, that is, stream sections closer to the source.

Anuran annual breeding period and duration of breeding activities are related to

seasonal climatic variations in temperature and rainfall (Toft and Duellman, 1979). Species

that occur in permanent shaded water bodies, with high humidity during most of the year,

usually show a long reproductive period (Rossa-Feres and Jim, 1994). The lack of

association between climatic variables (rainfall and temperature) and monthly anuran

species diversity and between climatic variables and diversity of species with calling males

may be due to local habitat conditions at the RPPN Serra do Caraça. The preserved forest

vegetation at stream margins and stream permanence may contribute to maintain air

humidity and temperature relatively stable and predictable for anuran species. Colwell

(1974) had already noticed forest habitats to be more stable and predictable than open

habitats.

Tadpoles of Scinax machadoi were recorded in all sampling months, indicating

continuous reproduction and/or long development. Nevertheless, the number of adult

individuals located was relatively low, maybe due to the species small size, cryptic

coloration, and low, irregular mating call (Bokermann and Sazima, 1973), making it

difficult to locate. In Stream 8, a single gravid female was recorded within the sampling

section, on July 2004. Besides Scinax machadoi, only tadpoles of Hyla martinsi and

Hylodes uai were recorded in this stream. There is a waterfall upstream next to the sampled

section, and it is possible that adults of these species reproduce upstream to this waterfall,

at smaller sections of the stream, and egg clutches and/or tadpoles are carried downstream

to the sampled section.

Crossodactylus sp. showed reproductive activities year-round, as reported for

Crossodactylus sp. at the Parque Estadual Mata dos Godoy (Paraná state, south Brazil;

Bernarde and Anjos, 1999) and Crossodactylus bokermanni at the Serra do Cipó (Minas

Gerais state, southeastern Brazil) (Eterovick and Sazima, 2004). As other species in the

subfamily Hylodinae (Leptodactylidae), the species of Crossodactylus occurring at the

RPPN Serra do Caraça is diurnal; males call close to or on the soil, at moist microhabitats

where they may reduce water loss (Cardoso and Martins, 1987; Cardoso and Haddad,

1992).

For the species that did not show strong indicatives of reproduction but mating

calls, it was not possible to describe a temporal distribution pattern for breeding activities,

because males' calling period may be longer than the actual specific breeding period

(Wiest, 1982; Donnelly and Guyer, 1994).

The species showing the greatest plasticity in stream occupancy were those

presenting the most indicatives of reproduction (gravid females, egg clutches, tadpoles, and

post metamorphic froglets), such as Hyla martinsi, H. nanuzae, Scinax luizotavioi, S.

machadoi, Crossodactylus sp., and Hylodes uai, which were observed almost year-round.

Hyla martinsi had abundance peaks at the hottest and most humid months, but its tadpoles

were recorded in all months, what may be due to continuous reproduction and/or long

tadpole development. Hyla nanuzae had a long breeding period with an activity peak during

the rainy season, its breeding period being longer than the one recorded at the Serra do

Cipó (Eterovick and Sazima, 2004), a more markedly seasonal and open habitat. Scinax

luizotavioi was recorded in almost all sampling months, with an activity peak during the

dry season. Differences in reproductive periods had already been interpreted as a potential

mechanism to avoid interspecific competition (Bertoluci and Rodrigues, 2002).

Nevertheless, climatic factors and physiological adaptations acquired during species

evolution may play a more important role in determining breeding periods of anurans, since

even populations of the same species may show variations in breeding pattern at different

sites, subject to different climatic conditions, as noticed here for Hyla nanuzae. Besides,

31.6% of the anuran species recorded in forest streams at the RPPN Serra do Caraça

showed indicatives of reproduction or reproductive activities year-round, contrasting with

only 11.6% (18.5% considering only species that reproduce in streams or associated to

them) of the anuran species of the Serra do Cipó, a less stable, open habitat (Eterovick,

2003; Eterovick and Sazima, 2004).

Species typical of forest habitats are probably more specialized and have

reproductive modes with more restrictive needs (see Duellman and Trueb, 1994) being

potentially more sensitive to habitat changes. The RPPN Serra do Caraça is located in the

domains of the Espinhaço mountain range, where many Brazilian endemic genera and local

endemic species occur (Costa et al., 1998). The Espinhaço is an important area for

amphibian conservation in the state of Minas Gerais and its surroundings are suffering

strong human impacts caused by mining activities and tourism. Once species spatial and

temporal distribution patterns are known, departures from these patterns may be considered

as indicatives of environmental disturbances, aiding to species conservation and

management.

Acknowledgments

We are grateful to Arquimedes D. M. Ferreira, Camila R. Rievers, Carlos Augusto

N. Ventura, Izabela M. Barata and Paulo Henrique C. de Souza for help during field work,

to Joaquim A. de Souza for making the maps, to Luciana B. Nascimento for help in species

identification, to Luciana B. Nascimento and Márcio Martins for suggestions in the

manuscript, to Consuelo Paganini for permit and logistics to work at the RPPN Serra do

Caraça, to the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis

(Ibama) for collecting permit (128/2004), and to the Fundo de Incentivo a Pesquisa (FIP) of

the Pontifícia Universidade Católica de Minas Gerais for financial support.

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CAPÍTULO 2

Microhabitat choice and partitioning by anurans in forest streams

in southeastern Brazil

Resumo

A utilização do nicho espacial pelos anuros adultos foi estudada em oito riachos de

mata na RPPN Serra do Caraça localizada no município de Catas Altas (Minas Gerais). Os

microambientes avaliados foram classificados em 18 tipos baseados nos substratos, na

distância e na altura da água. Um total de 440 anuros de 19 espécies apresentaram grande

seletividade na utilização desses microambientes. Espécies com nichos mais amplos (mais

generalistas) não ocuparam um maior número de riachos do que as espécies mais

especialistas, nem os riachos com uma maior riqueza de espécies apresentaram espécies

com valores mais estreitos de nicho. As espécies apresentaram variados níveis de

sobreposição na utilização dos microambientes. O padrão de distribuição observado neste

estudo sugere que a competição não é um importante fator influenciando a estrutura

espacial das comunidades de anuros de riachos permanentes de mata.

Palavras-chaves: Anfíbios anuros, distribuição espacial, utilização de microambientes,

largura de nicho, plasticidade comportamental.

Abstract

The use of niche spatial dimension by anuran amphibians was studied in eight forest

streams in the RPPN Serra do Caraça, Catas Altas municipality, Minas Gerais state,

southeastern Brazil. Microhabitats were sampled and classified in 18 types based on

substrate and height above ground/water. A total of 440 individual anurans of 19 species

was recorded using these types of microhabitats. Anurans showed selectivity in

microhabitat use. Species with broader niches (generalists) did not occur in more streams

than species with narrower niches (specialists), and streams with higher species richness

did not shelter more specialists. Species showed variable levels of superposition in

microhabitat use. The distribution patterns observed in the studied anuran assemblages

suggest that competition is not an important factor influencing the spatial structure of these

assemblages in permanent forest streams.

Key words: Anuran amphibians, spatial distribution, microhabitat use, niche breadth,

behavioral plasticity

Introduction

Species co-existence in an assemblage is possible due to partition of available

resources (Blair 1961, Duellman and Pyles 1983, Aichinger 1987, Cardoso et al. 1989,

Haddad and Sazima 1992, Rossa-Feres and Jim 1994, Pombal 1997, Eterovick and Sazima

2000, Eterovick and Barros 2003), which are distributed in three main niche dimensions:

time, space, and food (Pianka 1973). The use of such resources is a compromise between

physiological needs of organisms and biotic interactions among them within the ecosystem

(Zweimüller 1995).

Differences in resource use may reduce competition and make the co-existence of a

higher number of species possible (MacArthur 1972). Competition intensity between

species may be related to the level of overlap in use of a critical resource (MacArthur and

Levins 1967). When use of a resource result in competition, species may diverge in order to

avoid it, reducing overlap in resource use (Schoener 1982). According to Pianka (1973), a

species niche is the set of resources it uses, and species under competition pressure are

expected to narrow their niches or tolerate greater niche overlap in richer assemblages.

In general, resource partitioning by amphibians is related to several specific needs

(Crump 1971) and differences in reproductive modes (Duellman 1989). The highest the

diversity of reproductive modes in an assemblage, the highest the number of species

expected to be able to co-exist, maybe due to a more efficient pattern of resource

partitioning (Crump 1982).

Habitat partitioning represents the occupancy of the spatial dimension of species

niches (Pianka 1973) and it may be the most important niche dimension to be partitioned by

adult anurans (Toft 1985). Variable and heterogeneous habitats favor an increase in species

richness, since a higher combination of microhabitat types and ecological niches is

available (MacArthur 1968). The choice of specific microhabitats within this habitat mosaic

is related to morphological, physiological and behavioral adaptations of species (Crump

1971, Pough et al. 1977, Cardoso et al. 1989). Species with broader niches are expected to

be more widespread may tolerate a larger variety of habitat conditions (Gaston et al. 1997,

Pyron 1999). Besides, species closely related phylogenetically tend to be associated to the

same or similar ecological niches, and in such instances historical factors are more

important than recent ecological ones in determining species distribution (Inger 1969).

Studies on microhabitat use by anurans are scarce (Eterovick and Fernandes 2001,

Eterovick and Barros 2003), nevertheless anuran reproductive sites may be studied as well

limited ecosystems where spatial niche can be characterized and quantified (Eterovick and

Barros 2003) making studies on spatial organization of anuran assemblages feasible.

Considering the diversity of microhabitats used by adult anurans as a measurement of their

niche breadth (Pianka 1973), we aimed to test whether (1) anurans select actively their

microhabitats, (2) species with broader niches (generalists) occur in a higher number of

streams, (3) species occurring in richer assemblages have narrower niches, and (4) species

partition microhabitats.

Study site

The Reserva Particular do Patrimônio Natural Serra do Caraça is located at Catas

Altas municipality (20º 05’S; 43º 29’W), Minas Gerais state, southeastern Brazil. The

reserve encompasses 10 187.89 ha in the southern portion of the Espinhaço mountain

range, from 850 to 2070 m above sea level (Fig. 1). The region is formed by the orographic

P ara Belo Horizonte

P ara BR-381

P ara Mariana

P ara Alvin ópolis

A lvinó po lis

R io Piracicaba

S ão Gonçalo do Rio Abaixo

O uro Preto

R io Acima

Itabirito

M ariana

20º00'

43º30'

43º15'

C aeté

Ba rã o de Cocais

Sa nta Bárbara

C ata s Altas

0 5 10km

0 150km

systems of Minas Gerais and Bahia states (Derby 1966), representing a contact zone

between the Cerrado and Atlantic Forest biomes in its southern portion and a transition

zone between both biomes in its northern portion (Giulietti and Pirani 1988, Giulietti

et al

1997).

The region has two seasons, a dry from April to September and a wet, from October

to March.

Figure 1. Location of the RPPN Serra do Caraça, Minas Gerais state,

southeastern Brazil.

Methods

The work was conducted during three-day monthly field trips from August 2003 to

October 2004, when eight permanent forest streams were regularly sampled (Fig. 2). Each

month, 150 m sections marked, one at each stream, were inspected in search for anurans

through visual and auditory searching procedures. For each individual located, we recorded

substrate used and height from the ground.

Specimens not identified in the field were preserved according to Heyer et al.

(1994) for posterior identification and then deposited in the herpetological collection of the

Museu de Ciências Naturais of the Pontifícia Universidade Católica de Minas Gerais.

Figure 2. Location of the eight sampled streams at the RPPN Serra do Caraça,

southeastern Brazil.

Microhabitat selection

Microhabitat availability was quantified using a new method proposed herein. Five

pictures of the marginal habitat were taken for each stream, within the marked 150 m

sampling section. The pictures were taken at 15, 45, 75, 105, and 135 m from the beginning

of the section. The margin (right or left) to be photographed was randomly assigned at the

first point, and then the margins were alternated at each following point. To standardize

picture size, a metric tape was extended at the photographed point and the width of each

picture corresponded to 3 m. The bottom of each picture was positioned where stream

water contacted stream margin at the middle point. All the pictures were taken with the

same camera and by the same person, without flash.

An uniform 15 x 21 line grid was superposed to each picture (Fig. 3) and

microhabitats occurring at line intersections were recorded at three height classes (0-70 cm,

>70-140 cm, and >140 cm). As the pictures were taken in a perpendicular position in

relation to the photographed area, height from the ground (measured to characterize

microhabitats used by recorded frogs) could be then assigned to the height classes used in

the pictures (Fig. 3). Microhabitats were classified into 18 types resulting from the

combination of the three height classes and seven substrate types: green leaves (including

ferns, bromeliads, grasses), brown leaves, branches (including roots, fallen branches,

lianas), rocks, leaf litter, bare soil (including sand, mud and river banks), and water (Table

1). Microhabitats of leaf litter above 140 cm and of water above 70 cm were not recorded

and were so eliminated from the analyses.

Absolute numbers recorded for availability and use of microhabitat types were

compared through Chi-square tests (Zar 1999), assuming that a random distribution of

anurans throughout the streams (no microhabitat selection) would result in proportional

values of use and availability. A significant difference between observed and expected

values would so indicate microhabitat selection by anurans at the studied streams.

>140 cm

> 70-140 cm

0-70cm

Figure 3.

Picture taken at the first point (15 m) of Stream 3, with the 15 x 21 line

grid superposed to quantify available microhabitats in three height classes at the

RPPN Serra do Caraça, southeastern Brazil. Each height class encompasses five

horizontal grid lines.

Niche breadth

Niche breadth was estimated for each anuran species using Simpson's diversity

formula (Pianka 1973):

D = 1 /

∑

where Pi represents the proportion microhabitat "i" was used by the species

considered in relation to the total number of microhabitat use records for this species.

First, the diversity of microhabitats used by each species was estimated using data

from all streams where it occurred (A) and the diversity of available microhabitats was also

estimated for the same set of streams used by the species considered (S). Then, the diversity

of microhabitats used by each species was estimated separately for each stream where it

occurred (A'), and the diversity of available microhabitats was estimated for each stream

(S'). The A index was estimated for species with more than nine records (n = 7 species) and

the A' index was estimated for species with more than seven records (n = 6 species) in a

given stream.

A conservative estimate of niche breadth was given by A/S, since species occurring

in streams with greater microhabitat diversity could appear to have greater microhabitat use

diversity if they were randomly distributed in the habitat. So we tried to minimize the effect

of habitat heterogeneity on species niche breadths in order to compare them. We assumed

that higher A/S values would indicate species with greater plasticity in microhabitat use,

suggesting a generalist behavior, and we tested whether such species would occur in a

greater number of streams using linear regressions (Zar 1999). We considered the number

of streams where a species was recorded as the dependent variable and the species niche

breadth as the independent variable.

We also hypothesized that the number of species occupying a stream did would

influence on niche breadth of the species present, as assumed by Pianka (1973). We then

related niche breadth of species occurring in each stream (as the dependent variable) to

stream species richness (as the independent variable) using linear regressions (Zar 1999).

Statistical analyses were conducted in the software BioEstat (BioEstat 2003).

Niche overlap

To estimate niche overlap between anuran species regarding microhabitat use, we

used the formula proposed by Pianka (1973):

= __∑ P

√ ∑P

∑P

where P

and P

are the proportional uses of microhabitat "i" by species "j" and "k"

respectively. We used this index only for species occurring in the same stream.

Results

A total of 440 individual anurans from 19 species (Appendix 1) was observed using

16 out of the 18 recorded microhabitats. They used branches, bare soil and green leaves in

heights of 0-70 cm in proportions greater than expected (X

= 928.56, p < 0.001, Table 1).

None of the species used leaf litter or bare soil at heights of >70-140 cm (Table 1).

The high number of records obtained for Scinax luizotavioi, Hyla nanuzae and

Crossodactylus sp. made the conduction of specific analyses of microhabitat use possible,

and all these species showed microhabitat preferences. Scinax luizotavioi used

preferentially branches at heights of 0-70 cm (X

= 274.38, p< 0.001). Hyla nanuzae used

preferentially rocks at heights of 0-70cm (X

= 215.18, p< 0.001) and Crossodactylus sp.

used preferentially bare soil at heights of 0-70 cm (X

= 3418.7, p < 0.001).

Table 1. Microhabitats available in the eight studied streams and used by

19 anuran species at the RPPN Serra do Caraça, southeastern Brazil.

Microhabitats

Available

Used

Expected

Green leaves, 0-70 cm

1675

61.10

Green leaves, >70-140 cm

2102

76.7

Green leaves,

140 cm

1985

72.43

Brown leaves, 0-70 cm

332

12.10

Brown leaves, >70-140 cm

459

16.75

Brown leaves,

140 cm

332

12.10

Branch, 0-70 cm

1081

109

39.43

Branch, >70-140 cm

1325

48.35

Branch,

140 cm

1710

62.4

Rock, 0-70 cm

274

Rock, >70-140 cm

1.75

Rock,

140 cm

0.15

Leaf litter, 0-70 cm

Leaf litter, >70-140 cm

0.84

Bare soil, 0-70 cm

383

Bare soil, >70-140 cm

151

5.50

Bare soil,

140 cm

1.3

Water, 0-70 cm

2.1

Total

12058

440

Niche breadth

Species with broader niches (generalists), that is, those with higher A/S values, did

not occupy more streams than species with narrow niches (R

= -18.33%, p = 0.795, Table

2).

Table 2. Number of streams occupied and diversity of microhabitats used by seven anuran species

and diversity of available microhabitats in the set of streams used by them in the RPPN Serra do

Caraça, southeastern Brazil.

Species (n)

Number of

streams occupied

Diversity in

microhabitat use

(A)

Diversity of

available

microhabitats

(S)

A/S

Hyla

sp. (gr. c

ircumdata

)

(9)

3.24

8.45

0.38

Hyla martinsi

(19)

4.69

7.54

0.62

Hyla minuta

(13)

2.60

6.30

0.41

Hyla nanuzae

(104)

6.72

7.77

0.87

Hyla polytaenia

(12)

4.00

6.30

0.63

Scinax luizotavioi

(123)

2.99

7.62

0.40

Crossodactylus

sp.

(104)

2.62

7.89

0.33

The number of species occupying a stream did not influence on niche breadth of the

species present (A’/S’, Table 3) (R

= 4.95%, p = 0.237).

Table 3. Diversity of microhabitats used by six anuran species, diversity of microhabitat availability

in local streams and estimated niche breadth for species in particular streams (A'/S') at the RPPN

Serra do Caraça, southeastern Brazil. Streams are numbered like in Figure 2.

Species (number of

streams used)

Streams used

(number of

records)

Diversity in

microhabitat use (A’)

Diversity of

available

microhabitats

(S’)

A’/S’

Hyla martinsi

(4)

3 (8)

2.13

8.46

0.25

4 (7)

3.77

6.54

0.58

Hyla minuta

(1)

5 (13)

2.60

6.30

0.41

Hyla nanuzae

(4)

2 (12)

6.55

7.66

0.85

4 (32)

5.51

6.54

0.84

5 (55)

4.84

6.30

0.77

Hyla polytaenia

(1)

5 (12)

4.00

6.30

0.63

Scinax luizotavioi

(5)

2 (33)

3.96

7.66

0.52

4 (76)

2.63

6.54

0.36

5 (9)

2.45

6.30

0.39

Crossodactylus

sp. (3)

3 (78)

2.29

8.46

0.27

7 (43)

2.92

6.43

0.45

Niche overlap

Species had variable values of spatial niche overlap, and even species with great

superposition in microhabitat use could also superposition in their temporal distribution

(Afonso and Eterovick, unpubl. data).

Hyla nanuzae and S. luizotavioi (O

= 0.668) co-occurred on August 2003, March, April,

September, and October 2004 in Stream 2.

Hyla nanuzae and S. luizotavioi (O

= 0.635) co-occurred on August and September 2003,

from March to June and from August to September 2004 in Stream 4.

Hyla nanuzae and S. luizotavioi (O

= 0.529) co-occurred on March, May, August and

September 2004 in Stream 5.

Hyla nanuzae and H. polytaenia (O

= 0.373) co-occurred on August and October 2003 and

December and March 2004 in Stream 5.

Hyla nanuzae and H. minuta (O

= 0.511) co-occurred on August and September 2003 and

on March, May, August and September 2004 in Stream 5.

Scinax luizotavioi and H. polytaenia (O

= 0.754) co-occurred on March and September

2004 in Stream 5.

Scinax luizotavioi and H. minuta (O

= 0.950) co-occurred on March, May, August and

September 2004 in Stream 5.

Hyla minuta and H. polytaenia (O

= 0.682) co-occurred on August and October 2003 and

March and September 2004 in Stream 5.

Discussion

Environmental complexity, species niche breadth, niche overlap and behavioral

plasticity are all factors that may influence community structure (Inger and Colwell, 1977;

Cardoso et al., 1989). Environmental complexity is important to determine the number of

species that can exploit a given habitat (Cardoso et al., 1989). In forests, the complexity is

represented, in part, by the presence of all vegetation strata, creating a tridimensional space

with many microhabitat types. The use of all such space may favor the reduction of

competition among congeneric species (Meserve, 1977).

Spatial distribution is related to morphological (Cardoso et al., 1989), physiological

(Pough et al., 1977) and behavioral adaptations associated to anuran reproductive modes

(Crump, 1971). The anuran species occurring at the RPPN Serra do Caraça showed

selectivity in microhabitat use, branches at heights between 0 and 70 cm being the preferred

microhabitats. The high number of hylids present in the study site can help explain the

preference for microhabitats on the vegetation, as the presence of adhesive discs at hylid

fingertips turn species of this family able to explore the vegetation vertically (Cardoso et

al., 1989). Besides, these treefrogs can also use rocks and leaf litter as substrates as other

frogs do. This may contribute to a large niche breadth in species of this family. In fact, the

Leptodactylid Crossodactylus sp. had niches narrower than most Hylids studied (see Tables

2 and 3). Physiological differences in tolerance to water loss may also influence on

microhabitat choice (Pough et al., 1977). Species preference for microhabitats at heights

from 0 to 70 cm may be due to a higher humidity expected to occur close to the ground

(Cardoso and Martins, 1987; Cardoso and Haddad, 1992).

Scinax luizotavioi and Hyla nanuzae followed the pattern of spatial distribution

recorded for hylids at other sites (see Pombal, 1997; Eterovick and Sazima, 2004). These

species preferred to use branches and rocks respectively, both at heights from 0 to 70 cm.

Crossodactylus sp. preferred to use bare soil at heights of 0-70 cm. Since this species is

diurnal, the frogs call from the ground or close to it, at microhabitats that provide more

protection against water loss due to high humidity (Cardoso and Martins, 1987; Cardoso

and Haddad, 1992). As the remaining species recorded are nocturnal, Crossodactylus sp. is

not supposed to compete for space with them, so that the narrow niche recorded for this

species may be due to specific behavior and physiologic tolerances other than competitive

interactions with other anuran species.

According to Pianka (1973), species occurring in streams with higher species

richness would be expected to have narrower niches or greater niche overlap if subjected to

competition for the spatial niche dimension. Though, values of species niche breadths were

not related to species richness in streams at the RPPN Serra do Caraça. This may indicate

that the available niche space is not completely occupied, and competition is not strong

enough to influence community structure making species narrow their niches (Pianka,

1973). A similar pattern was recorded for tadpoles at montane meadow streams at Serra do

Cipó, southeastern Brazil (Eterovick and Barros, 2003).

The streams studied at Serra do Caraça are permanent and do not undergo abrupt

changes, being relatively stable if compared to temporary streams, as the ones studied by

Eterovick and Barros (2003) at Serra do Cipó. Habitat stability could provide suitable

conditions for species with narrow niches, and allow species to specialize in microhabitat

use (Donohue et al., 2001). Besides, forest habitats are considered more stable and

predictable than open habitats (sensu Colwell, 1974). Future studies addressing niche

breadth of anuran species in less stable and open habitats will be useful to assess the role of

environmental stability in shaping anuran assemblage structure.

Species pairs with higher values of niche overlap regarding microhabitat use may

show less overlap in other niche dimensions, such as food and time, in order to avoid

interspecific competition (Pianka, 1973). According to Toft (1985), the spatial niche

dimension is more important than food and time to be partitioned by anurans, since the

trophic niche is closely related to microhabitats used by the species (Inger and Colwell,

1977). At the study site, many species with spatial niche superposition also showed overlap

in period of occurrence, reinforcing the little importance of competition in structuring local

anuran assemblages.

Scinax luizotavioi and H. minuta were the species with the highest value of niche

overlap (O

= 0.950). Although these species used the same microhabitats, they were

distributed throughout the stream in a way that S. luizotavioi was more frequent at stream

sections with more closed canopy and H. minuta was more frequent at open sections around

large backwaters. Scinax luizotavioi was also observed calling in a lake surrounded by

herbaceous and shrubby vegetation at Serra do Caraça by Caramaschi and Kisteumacher

(1989). Hyla minuta can also use puddles and swamps besides stream backwaters

(Eterovick and Sazima, 2004), occurring also in ponds at the RPPN Serra do Caraça (K.

Kopp and P. C. Eterovick, unpubl. data). In spite of being able to occupy different types of

water bodies, both Scinax luizotavioi and Hyla minuta had low values of niche breadth if

compared with other co-occurring hylids (see Tables 2 and 3). These species may occupy

habitats opportunistically but have an expected spatial distribution within them, regarding

microhabitats used. Microhabitat use may be more likely related to specific behavior than

to any kind of niche separation caused by competition, since there is a great availability of

the preferred microhabitats in the set of habitats used by the species. By the other side,

habitat occupancy may be related to differential migrating and colonization abilities of

species, so that species niches were not related to number of streams occupied.

The observed variable levels of niche overlap between species pairs indicate that

they differ in resource use although selective pressures may not be strong enough to lead to

a complete species differentiation in microhabitat use, as also noticed by Eterovick and

Barros (2003) for tadpole assemblages at Serra do Cipó, southeastern Brazil. Zimmerman

and Simberloff (1996) showed that anuran community structure, regarding habitat type

used for reproduction and development, is determined mainly by phylogenetic constraints

of species colonizing each site instead of environmental or competitive pressures. These

authors suggest that competition might assume a greater importance in a finer spatial scale,

but here we show that competition does not seem to have a great interference in

microhabitat use by adult anurans, at least in permanent streams.

The patterns of spatial distribution and microhabitat use of anuran assemblages in

the RPPN Serra do Caraça indicate that competition may not have an important influence

on their structure. Species may show temporal and spatial overlap within a given habitat

(stream), or use the same microhabitats in a set of habitats (streams and ponds), even side

by side or scattered throughout the water body. Although species show patterns of

microhabitat preferences, microhabitats seem to be abundant enough to allow coexistence

without restrictions in specific preferences caused by competition. The role of habitat

stability in shaping species spatial niche is still little explored. Studies on anuran

assemblages from intermittent streams and sites with open vegetation, employing the new

method proposed here, will aid to the knowledge on how habitat stability and predictability

influence species niche breadth.

Acknowledgments

We are grateful to Arquimedes D. M. Ferreira, Camila R. Rievers, Carlos A. N.

Ventura, Fernanda C. Zaidan, Izabela M. Barata and Paulo Henrique C. de Souza for help

during field work, to Joaquim A. de Souza for making the maps, to Luciana B. Nascimento

for help during species identification, to Luciana B. Nascimento and Márcio Martins for

helpful suggestions in the manuscript, to Consuelo Paganini and the RPPN Serra do Caraça

staff for permits and logistics, to the Instituto Brasileiro do Meio Ambiente e dos Recursos

Naturais Renováveis (Ibama) for collecting permit (128/2004), and to the Programa de

Incentivo à Pesquisa (FIP) of the Universidade Católica de Minas Gerais for financial

support.

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