CUNHA MS, 2011 - RI UFBA - Universidade Federal da Bahia

Maria Silva Cunha
SELEÇÃO DE SÍTIO DE VOCALIZAÇÃO PELO ANFÍBIO
BROMELÍGENO Phyllodytes melanomystax
(ANURA, HYLIDAE)
Programa de Pós-Graduação em Ecologia e Biomonitoramento
Universidade Federal da Bahia
Salvador, 2011
i
Salvador, 2011
UNIVERSIDADE FEDERAL DA BAHIA
INSTITUTO DE BIOLOGIA
PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA E
BIOMONITORAMENTO
SELEÇÃO DE SÍTIO DE VOCALIZAÇÃO PELO ANFÍBIO
BROMELÍGENO Phyllodytes melanomystax (ANURA, HYLIDAE)
Maria Silva Cunha
Dissertação apresentada ao Programa
de Pós-Graduação em Ecologia e
Biomonitoramento do Instituto de
Biologia da Universidade Federal da
Bahia, sob orientação do Prof. Dr.
Marcelo Felgueiras Napoli, como prérequisito para a obtenção do título de
Mestre
em
Ecologia
e
Biomonitoramento.
Salvador
2011
ii
Ficha Catalográfica
Cunha, Maria Silva.
Seleção de sítio de vocalização pelo anfíbio bromelígeno Phyllodytes melanomystax (Anura,
Hylidae) / Maria Silva Cunha. - 2011.
69 f. : il.
Orientador: Prof. Dr. Marcelo Felgueiras Napoli.
Dissertação (mestrado) - Universidade Federal da Bahia, Instituto de Biologia, Salvador, 2011.
1. Anfíbio. 2. Perereca. 3. Bromélia. 4. Ecologia. I. Napoli, Marcelo Felgueiras.
II. Universidade Federal da Bahia. Instituto de Biologia. III. Título.
CDD - 597.8
CDU - 597.8
iii
Maria Silva Cunha
Seleção de sítio de vocalização pelo anfíbio bromelígeno Phyllodytes
melanomystax (Anura, Hylidae)
Dissertação apresentada ao Programa de Pós-Graduação em
Ecologia e
Biomonitoramentto do Instituto de Biologia da Universidade Federal da Bahia como
partes dos requisitos necessários para a obtenção do título de Mestre em Ecologia e
Biomonitoramento.
Aprovada por:
Prof. Dr. Marcelo Felgueiras Napoli
Orientador
Prof.ª Dr.ª Flora Acuña Juncá
Universidade Estadual de Feira de Santana
Prof. Dr. Mirco Solé
Universidade Estadual de Santa Cruz
iv
Dedicatória
À minha mamãe, sempre!
v
Epígrafe
(...) de qualquer forma, eu gostaria de saber
se alguma vez aparecerei em histórias e
canções (...), quero dizer, ser posta em
palavras, sabe, contadas ao pé da lareira ou
lida de um grande livro grosso com letras
douradas, anos e anos depois. E as pessoas
dirão “Vamos ouvir a história de Maria e
dos Phyllodytes”! E elas dirão “Essa é uma
das minhas preferidas”.
J. R. R. Tolkien, O senhor dos anéis
(adaptado).
vi
Agradecimentos
Ao meu bom Deus, que me guarda a cada segundo, ilumina e protege os meus
passos por onde quer que eu passe. A ti, Senhor, toda a glória.
À, minha mamãe, Adenita, por ser esta figura única na minha vida, que tantas
vezes esqueceu-se de si para me proporcionar o melhor e que faz de tudo pela filhota
aqui. Ao meu pai, Antônio (in memorian), sou grata por ajudar tanto na formação do
que eu sou hoje, mesmo estando ausente. Às minhas tias “Anas” e ao meu tio/pai
Adelson, por mais uma vez acompanharem e apoiarem as minhas decisões e pela boa
educação que sempre me deram. Hoje compreendo a importância de vocês apagarem
toda a palavra quando eu errava apenas a última letra no dever de casa do primário! Aos
meus avós, às minhas primas Brunna e Mariana e ao meu afilhado Bruno, obrigada
por existirem na minha vida.
À Mariza, Marcely e toda sua família, por terem me acolhido em Salvador
como se eu fosse um deles, pela confiança e cuidado que só na minha própria família eu
encontraria. Muito obrigada!
Ao meu namorado lindo, Élton, por ser tão fofo! Por ser sempre uma companhia
maravilhosa, pelo carinho e por cuidar tão bem de mim. E a toda a família Milanês, em
especial à minha sogra Ozelita.
Ao meu orientador, Marcelo, pela oportunidade, confiança e experiência
passada. Obrigada por me ensinar tanto sobre o curioso mundo dos sapos e por ser um
exemplo de dedicação à ciência.
Ao Programa de Pós-Graduação em Ecologia e Biomonitoramento, por me
mostrar o que é Ecologia de verdade. Obrigada a cada professor que contribuiu tão
fortemente para minha formação profissional e que, através de suas disciplinas,
colaborou para a qualidade deste trabalho. E à Jussara, que facilitou a minha vida
burocrática na pós-graduação.
À Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB), que me
proporcionou a bolsa de mestrado durante os meus dois anos de curso.
vii
Ao Sr. Alberto Bolzico, por ter permitido a realização da coleta de dados na
área da Fazenda Praia do Forte. Ao Samuel, por ajudar alguns procedimentos logísticos
do campo e pela disponibilidade em cooperar conosco. E ao Seu Anísio! Que nos
conduziu tão bem pelas areias escaldantes da restinga de Praia do Forte e que, no final,
já estava até coletando os Phyllodytes conosco!
Aos meus super ajudantes de campo, que se revezaram durante as semanas de
coleta com toda a boa vontade do mundo! Obrigada a Rafa, Júnior, Lucas, Vanessa
Bonfim (VaiNessa!), Joice Ruggeri, Manu, Joice Herrera, Daniele, Jucilene,
Ariane, Thiago Filadelfo e Thaís (Kuen).
A Rafael e Fila pelas fotos maravilhosas e a Lucas pela ótima ilustração da
bromélia.
Aos meus super amigos da “Liga da UESC”, Euvaldo Júnior, Marlla (sem
alça) e Camila “Pitty”, por tornarem meus dias na UFBA mais familiares, por assim
dizer. Agradeço ao Júnior por me transmitir o vírus da herpetologia, à Marlla por ser tão
“Marlla” e à Pitty por ter se transformado de uma simples colega da graduação a uma
das minhas melhores amigas. Ao amigo Gilson Ximenes, por ser um exemplo de
professor e de pessoa, pela sua humildade e simplicidade e por não nos abandonar,
mesmo nos intitulando de “pragas”! E aos meus demais amigos que, mesmo não
estando presentes no meu dia-a-dia, torceram muito para que desse tudo certo. Amo
muito vocês!
Aos meus colegas da turma 2009.1 do PPGEcoBio, pelas tantas risadas e pelas
contribuições ao meu trabalho.
Agradeço imensamente ao povo do Laboratório de Taxonomia e História
Natural de Anfíbios (AMPHIBIA), por terem me recebido da melhor forma possível!
Eu que cheguei meio tímida e que aos poucos fui me deixando levar por essas pessoas
maravilhosas! São essas figuras pitorescas e tão especiais: Ariane Xavier (Aribio – a
alça), Thaís Dória (Kuen), Deise Cruz (“Valeu Neymar”!), Patrícia Fonseca (Pati –
Amuu!), Emanuela Petersen (Manuuuu!), Milena Camardelli (“Se eu pudesse eu
matava Mil, Mil Mil, ê iê!), Rafael Abreu (que gosta de biscoito de morango e faz
biscuit...), Joice Ruggeri (Cota), Lucas Menezes (Loucas), Laís Encarnação (Lai),
viii
Euvaldo Jr. (Juninho da Baêa, pai!), Joice Herrera (Joicebunda), Tamiris, (Têimiris)
e aos novatos Camila e Robson. E não posso esquecer do nosso mais ilustre anexo,
Tiago Porto (Tiko). Não dá para contar quantas resenhas surgiram, de quantas idiotices
de Rafa nós rimos, de quantas alucinações de Kuen, Pati e/ou Manu nós tivemos crises
de gargalhadas, mas dá pra saber que vocês foram essenciais nestes dois anos de
convivência.
E, finalmente, aos Phyllodytes (tão fofinhos), que permitiram que eu conhecesse
um pedacinho do curioso mundo em que vivem.
ix
Sumário
Texto para divulgação
1
Introdução Geral
2
Referências
8
Figura 1
13
Figura 2
14
Artigo. Revista Journal of Animal Ecology
15
Título do Artigo: Calling site selection by the bromeliad-dwelling treefrog 16
Phyllodytes
melanomystax (Amphibia: Anura: Hylidae) in a coastal sand
dune habitat
Summary
17
Introduction
19
Material and Methods
Study area
22
Research Design and Field Methods
22
Data Analysis
25
Results
Microhabitat variables and natural history notes
27
Statistical analyses
28
Discussion
29
Acknowledgements
34
References
35
Figure captions
40
Figure 1
41
Figure 2
42
Figure 3
43
Table 1
44
Table 2
45
Table 3
46
x
Table 4
47
Regras para publicação no Journal of Animal Ecology
48
xi
Texto De Divulgação
Bromélias-tanque são plantas capazes de acumular água da chuva dentro de suas
rosetas. Tal capacidade permite a formação de pequenos corpos d‟água conhecidos como
fitotelmos. Esse micro-hábitat é usado por uma grande variedade de vertebrados e
invertebrados. Além disso, algumas espécies chegam a passam todo o seu ciclo de vida dentro
das bromélias, como as atuais onze espécies de pererecas do gênero Phyllodytes.
É sabido que anfíbios anuros, que utilizam as bromélias-tanque, as selecionam de forma
não aleatória. Entretanto, os fatores ambientais que direcionam essa seleção ainda não estão
claros. Na presente dissertação, foram investigadas as variáveis associadas à seleção de
bromélias
por machos vocalizantes do anuro bromelígeno Phyllodytes melanomystax.
Ademais, foram feitas observações acerca da história natural dessa espécie e um experimento de
marcação e recaptura.
O estudo foi conduzido em um ambiente de restinga arbóreo-arbustiva, localizada no
município de Mata de São João, litoral norte do estado da Bahia, Brasil. Duzentas e duas
bromélias terrestres foram amostradas, 101 com e 101 sem machos vocalizantes de P.
melanomystax. Foram medidas nove variáveis ambientais que, de acordo com a literatura,
possivelmente influenciam a seleção de bromélias por anuros. Os dados foram analisados
através da análise de regressão logística múltipla e do teste de Wald.
Foi encontrada uma relação significativa entre a presença/ausência de machos de P.
melanomystax e duas das variáveis medidas: quantidade de detrito acumulado no tanque da
bromélia e número de bromélias em um raio de 2m. O experimento de marcação e recaptura
indicou que os machos possuem alta fidelidade ao sítio de vocalização. As observações de
história natural sugeriram que as bromélias escolhidas para vocalização são também utilizadas
para reprodução, oviposição e crescimento dos girinos.
A partir dos resultados, entendemos que P. melanomystax segue um dos padrões
já descritos para alguns invertebrados (aranhas e opiliões) que utilizam as bromélias-tanque.
Para esses animais já foi demonstrado que o detrito acumulado pela bromélia os impede de
utilizar o tanque de modo eficiente. Ao conjugarmos as observações de história natural ao fato
de que P. melanomystax parece evitar bromélias que estão isoladas espacialmente, assumimos
que a área de vida dos machos é restrita, e que o número de bromélias com potencial de serem
usadas pode ser uma variável importante na escolha dos machos pelas fêmeas.
1
1
Introdução Geral
2
Na história de vida de espécies que habitam locais sob condições variáveis, um
3
dos processos decisivos para sobrevivência e sucesso reprodutivo dos indivíduos é a
4
seleção de hábitat (Huey 1991, Rudolf & Rödel 2005, Brown et al. 2008a, Lin et al.
5
2008). As características do hábitat selecionado influenciam desde disponibilidade de
6
alimento e vulnerabilidade do adulto ao predador, até condições do hábitat para o
7
desenvolvimento e sobrevivência da prole (Resetarits & Wilbur 1989, Romero &
8
Vasconcellos-Neto 2005, Rudolf & Rödel 2005). Os indivíduos são capazes de avaliar
9
previamente o hábitat em questão e tal avaliação é mais crítica durante o período
10
reprodutivo, pois a prole geralmente é menos tolerante a condições físico-químicas
11
extremas e normalmente é incapaz de mudar para outro local caso o ambiente não
12
apresente condições favoráveis à sobrevivência (Huey 1991, Rudolf & Rödel 2005). As
13
características do hábitat que influenciam tal processo de seleção dependerão, entre
14
outros fatores, do tipo de hábitat utilizado e das necessidades intrínsecas a cada espécie,
15
as quais estão associadas aos seus aspectos reprodutivos, ecológicos e comportamentais.
16
Entre os anfíbios anuros, características do hábitat que parecem influenciar fortemente a
17
seleção de tais locais durante o período reprodutivo são temperatura e pH da água, além
18
de presença de predadores e densidade de coespecíficos (Bursik 1988, Resetarits &
19
Wilbur 1989, Gascon 1992, Oliveira & Navas 2004, Brown et al. 2008a,b, Lin et al.
20
2008). Entretanto, anfíbios anuros que habitam regiões tropicais apresentam um grande
21
número de modos reprodutivos, o que leva ao uso de micro-hábitats diversos por estes
22
animais (Haddad & Prado 2005) e, por conseguinte, pode levar a mudanças nas
23
características associadas à seleção do hábitat.
24
Anfíbios anuros que habitam fitotelmos enfrentam riscos e situações incomuns a
25
outros hábitats. O termo fitotelmo (do grego phytos = planta, telm = poça) foi designado
2
1
em 1928 pelo alemão Ludwig Varga, que estudava a fauna aquática associada a plantas
2
carnívoras e é definido como corpos d‟água acumulados em plantas ou partes de plantas
3
(Kitching 2000). Entre os exemplos mais comuns de fitotelmos estão água acumulada
4
em bromélias-tanque, colmos de bambu, cavidades de árvores e brácteas florais
5
(Kitching 2001, Lehtinen et al. 2004). Anuros que habitam fitotelmos têm que lidar
6
frequentemente com situações como a exposição à dessecação, a imprevisível
7
disponibilidade de alimento e baixas concentrações de oxigênio, sendo tais situações
8
mais críticas para o indivíduo em estágio larval (Lehtinen et al. 2004). Anuros
9
habitantes de fitotelmos apresentam uma série de estratégias comportamentais que lhes
10
permitem sobreviver nestes ambientes, como oofagia e cuidado parental (Schiesari et al.
11
2003, Lehtinen et al. 2004, Brown et al. 2008 a,b), além de outras fisiológicas, como
12
redução do aparato branquial para minimizar a perda de oxigênio para o meio (Lanoo et
13
al. 1987).
14
Entre os tipos de fitotelmo supracitados, as bromélias são conhecidas como
15
plantas-chave em ambientes tropicais onde, em muitas situações, representam o único
16
reservatório de água disponível no ambiente (Neill 1951). Devido à sua alta
17
adaptabilidade, a família Bromeliaceae, atualmente composta por mais de 2800
18
espécies, se distribuiu amplamente nos diversos ecossistemas do Novo Mundo, sob uma
19
grande variedade de formas e tamanhos (Smith & Downs 1979). O micro-hábitat
20
formado pelas bromélias-tanque, aquelas cuja estrutura permite o armazenamento de
21
água da chuva, é utilizado por muitos grupos de animais (Neill 1951, Laessle 1961,
22
Armbruster et al. 2002) e até mesmo por outras plantas que utilizam tal ambiente para a
23
germinação de suas sementes (Sampaio et al. 2005). A relação entre as bromélias e sua
24
fauna associada possui graus de dependência entre animal e planta, podendo esta
25
relação ser espécie-específica, como entre a aranha Psecas chapoda Peckham &
3
1
Peckham, 1894 e Bromelia balansae Mez, 1891 (Romero & Vasconcelos-Neto 2005) e
2
entre a perereca dourada de Trinidad Phytotriades auratus (Boulenger, 1917) e a
3
bromélia-tanque Glomeropitcairnia erectiflora Mez, 1905 (Jowers et al. 2008).
4
Sob o propósito de investigar a relação entre os anfíbios anuros e as bromélias
5
da Mata Atlântica, Peixoto (1995) estudou os tipos de associação entre anuros e
6
bromélias neste ecossistema, fornecendo definições que nortearam os trabalhos
7
subsequentes que versaram sobre anuros em bromélias no Brasil. De acordo com o
8
autor, os anuros associados às bromélias podem ser classificados em:
9
1) Bromelícolas – espécies que utilizam as bromélias como refúgio, mas que se
10
reproduzem em outros locais, não havendo dependência do anuro para com a
11
bromélia. Os bromelícolas podem ainda ser divididos em (1) eventuais,
12
quando a espécie é encontrada frequentemente em outros ambientes e (2)
13
habituais, quando, apesar de se reproduzir em outros locais, a espécie é mais
14
frequentemente encontrada em bromélias.
15
2) Bromelígenas – espécies cujo ciclo reprodutivo é dependente do ambiente
16
proporcionado pelas bromélias. Quanto ao tipo de desenvolvimento larvar, as
17
espécies foram categorizadas em espécies de desenvolvimento direto e
18
espécies de fase larvar livre.
19
Dentre as espécies bromelígenas que ocorrem no Brasil, as mais conhecidas são
20
as espécies do grupo de Scinax perpusillus (sensu Peixoto 1987) [S. alcatraz (Lutz,
21
1973); S. atratus (Peixoto, 1989); S. littoreus (Peixoto, 1988); S. melloi (Peixoto, 1989);
22
S. perpusillus (Lutz & Lutz, 1939); S. v-signatus (Lutz, 1968); S. peixotoi Brasileiro
23
Haddad, Sawaya & Martins, 2007; S. faivovichi Brasileiro, Oyamaguchi & Haddad,
24
2007; S. tupinamba Silva & Alves-Silva, 2008; S. belloni Faivovich, Gasparini &
25
Haddad, 2010], as espécies do gênero Flectonotus [F. fissilis (Miranda-Ribeiro, 1920);
4
1
F. fitzgeraldi (Parker, 1934); F. goeldii (Boulenger, 1895); F. ohausi (Wandolleck,
2
1907); F. pygmaeus (Boettger, 1893)], Gastrotheca fissipes (Boulenger, 1888),
3
Crossodactylodes izecksohni Peixoto, 1983 e todas as espécies do gênero Phyllodytes
4
Wagler, 1830 (Peixoto 1995, Caramaschi et al. 2004, Silva & Britto-Pereira 2006,
5
Alves-Silva & Silva 2009).
6
O gênero Phyllodytes é composto por pequenas pererecas bromelígenas com
7
fase larvar livre, distribuídas em diferentes fisionomias da Mata Atlântica. São onze as
8
espécies atualmente descritas de Phyllodytes: P. acuminatus Bokermann, 1966; P.
9
brevirostris Peixoto & Cruz, 1988; P. edelmoi Peixoto, Caramaschi & Freire, 2003; P.
10
gyrinaethes Peixoto, Caramaschi & Freire, 2003; P. kautskyi Peixoto & Cruz, 1988; P.
11
luteolus (Wied-Neuwied, 1824); P. maculosus Cruz, Feio & Cardoso, 2007; P.
12
melanomystax Caramaschi, Silva & Britto-Pereira, 1992; P. punctatus Caramaschi &
13
Peixoto, 2004; P. tuberculosus Bokermann, 1966 e P. wuchereri (Peters, 1873). As
14
espécies de Phyllodytes apresentam como principais características a presença de
15
odontóides bastante evidentes e o ciclo de vida altamente relacionado às bromélias
16
(Caramaschi et al. 2004).
17
Pouco se sabe sobre ecologia e comportamento das espécies de Phyllodytes.
18
Eterovick (1999) avaliou a seleção de bromélias por P. luteolus em um ambiente
19
modificado e concluiu que esta espécie seleciona as bromélias de acordo com suas
20
características físico-químicas em apenas uma das quatro espécies de bromélias
21
avaliadas no estudo. Entretanto, problemas de delineamento amostral (p.ex., pseudo-
22
replicação espacial) podem ser identificados neste estudo e o fato de ter sido feito em
23
“jardim” de bromélias pode ter influenciado o resultado encontrado, como sugerido pela
24
própria autora. Giaretta (1996) investigou os aspectos reprodutivos de P. luteolus e
25
atentou para a baixa fecundidade das fêmeas desta espécie, além do pequeno tamanho
5
1
da desova, o menor das espécies de Hylidae. Este autor discutiu ainda que a baixa
2
abundância de machos por bromélia pode ser um indício de territorialidade. Entretanto,
3
existem casos em que há mais de um macho vocalizante de Phyllodytes por bromélia,
4
como em P. luteolus (Eterovick 1999), P. melanomystax e P. tuberculosus (Marcelo F.
5
Napoli comunicação pessoal). As demais publicações sobre espécies do gênero
6
Phyllodytes são de caráter taxonômico (p.ex., Bokermann 1966, Caramaschi et al. 1992,
7
Peixoto et al. 1999, Caramaschi & Peixoto 2004, Caramaschi et al. 2004, Simon &
8
Gasparini 2003, Jowers et al. 2008, Vieira et al. 2009), ou são estudos com fins diversos
9
[p.ex., Weygoldt (1981) descreveu parte da biologia reprodutiva de P. luteolus; Papp &
10
Papp (2000) relataram o declínio em população de P. luteolus após queimada na área de
11
estudo] e que não objetivaram investigar a relação entre determinada espécie de
12
Phyllodytes e bromélias.
13
Entretanto, alguns trabalhos que investigaram a relação entre espécies
14
bromelígenas de outros gêneros de anfíbios anuros e as bromélias habitadas geraram
15
informações consistentes. Oliveira & Navas (2004) investigaram a seleção de bromélias
16
por Scinax perpusillus e sugeriram que o tamanho da bromélia e o nível de agrupamento
17
da planta (medido através do número de bromélias em um raio de 2 metros da planta
18
amostrada) são características influentes na seleção de bromélias por Scinax perpusillus.
19
Ainda sobre o grupo de S. perpusillus, Alves-Silva & Silva (2009) estudaram o
20
comportamento reprodutivo de seis das 11 espécies do grupo e revelaram um sistema
21
reprodutivo complexo nas espécies estudadas. Os machos das espécies do grupo de S.
22
perpusillus possuem um elaborado repertório acústico e as fêmeas apresentam um
23
sofisticado controle sobre a oviposição, que consiste em inspecionar previamente o sítio
24
reprodutivo e pôr geralmente apenas um ovo por axila foliar, característica considerada
25
sinapomorfia do grupo de S. perpusillus (Alves-Silva & Silva 2009). Sistemas
6
1
reprodutivos complexos também são observados em outros anuros bromelígenas, como
2
Anomaloglossus beebei (Noble, 1923) (Bourne et al. 2001) e anuros de outros tipos de
3
fitotelmo, como Kurixalus eiffingeri (Boettger, 1895) (Lin et al. 2008), Ranitomeya
4
variabilis (Zimmermann & Zimmermann, 1988), R. imitator (Schulte, 1986) (Brown et
5
al. 2008b) e Mantella laevigata Methuen & Hewitt, 1913 (Heying 2008). Nestas
6
espécies a seleção de hábitat já foi evidenciada e é possível que tal processo também
7
ocorra com as espécies de Phyllodytes, pois, como visto acima, talvez este seja um
8
processo crucial para a sobrevivência e sucesso reprodutivo das espécies que habitam
9
fitotelmos.
10
O local de estudo do presente trabalho está localizada numa área de restinga
11
arbóreo-arbustiva localizada na Área de Proteção Ambiental (APA) Litoral Norte (Fig.
12
1). A área é paralela à orla da praia e possui cerca de 1700 m de comprimento por 400
13
metros de largura. É delimitada ao sul por condomínios residenciais, ao norte por cerca
14
de arame de um grande resort, ao leste por moitas de arbustos próximos à orla da praia e
15
ao oeste por mata ciliar que margeia o Rio Timeantube (para mais detalhes, ver
16
Bastazini et al. 2007). A espécie escolhida como modelo para a realização deste
17
trabalho é Phyllodytes melanomystax (Fig. 2) que, assim como as demais espécies de
18
Phyllodytes (à exceção de P. luteolus, ver acima) possui muito pouco de sua história
19
natural descrita e carece de informações acerca de suas relações com as bromélias que
20
utilizam.
21
A presente dissertação tem por objetivos (1) investigar se há seleção de
22
bromélias por Phyllodytes melanomystax numa área de restinga arbóreo-arbustiva e,
23
caso haja, (2) determinar quais variáveis do microhabitat estão associadas à seleção das
24
bromélias por esta espécie.
25
7
1
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3
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Brown, J.L., Twomey, E., Morales, V. & Summers, K. (2008b) Phytotelm size in
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Mantella laevigata, with comparisons to the dendrobatids. Animal Behaviour 61, 567–
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Huey, R.B. (1991) Physiological consequences of habitat selection. The American
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Naturalist 137, 91–115.
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Kitching, R.L. (2000) Food Webs and Container Habitats: The Natural History and
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Ecology of Phytotelmata. Cambridge University Press, Cambridge, UK.
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Kitching, R.L. (2001) Food webs in phytotelmata: “bottom-up” and “top-down”
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explanations for community structure. Annual Review of Entomology 46, 729–60.
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Jowers, M.J., Downie, J.R., & Cohen, B.L. (2008) The golden tree frog of Trinidad,
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Phyllodytes auratus (Anura: Hylidae): systematic and conservation status. Studies on
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Neotropical Fauna and Environment 43, 181–188.
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Laessle, A.M. (1961) A micro-limnological study of Jamaican bromeliads. Ecology 42,
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499–517.
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Lannoo, M.J., Townsend, D.S. & Wassersug, R.I. (1987) Larval life in the leaves:
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arboreal tadpole types, with special attention to the morphology, ecology and behavior
12
of the oophagous Osteopilus brunneus (Hylidae) larva. Fieldiana Zoology 38, 1–31.
13
Lehtinen, R.M. Lanoo, M.J. & Wassersug, R.J. (2004) Phytotelm-breeding anurans:
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past, present and future research. Ecology and Evolution of Phytotelm Breeding
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Anurans, (ed R.M. Lehtinen), pp. 1–9. Miscellaneous Publications of the Museum of
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Zoology, University of Michigan.
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Lin, Y.S., Lehtinen, R.M. & Kam, Y.C. (2008) Time-and context-dependent oviposition
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site selection of a phytotelm-breeding frog in relation to habitat characteristics and
19
conspecific cues. Journal of Herpetology 64, 413–421.
20
Neill, W.T. (1951) A bromeliad herpetofauna in Florida. Ecology 32,140–143.
21
Oliveira, F.B. & Navas, C.A. (2004) Plant selection and seasonal patterns of vocal
22
activity in two populations of the bromeligen treefrog Scinax perpusillus (Anura,
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Hylidae). Journal of Herpetology 38, 331–339.
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Papp, M.G. & Papp, C.O.G. (2000) Decline in a population of the treefrog Phyllodytes
2
luteolus after fire. Herpetological Review 31, 93–95.
3
Peixoto, O.L. (1987) Caracterização do grupo „„perpusilla‟‟ e revalidação da posição
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taxonômica de Ololygon perpusilla perpusilla e Ololygon perpusilla v-signata
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(Amphibia, Anura, Hylidae). Arquivos da Universidade Federal Rural do Rio de
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Janeiro 10, 37–49.
7
Peixoto, O.L. (1995) Associação de anuros a bromeliáceas na Mata Atlântica. Revista
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Universidade Rural Série Ciencias da Vida 17, 75–83.
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Peixoto, O.L., Caramaschi, U., Freire, E.M.X. (1999) Two new species of Phyllodytes
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(Anura: Hylidae) from the state of Alagoas, northeastern Brazil. Herpetologica 59, 235–
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246.
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Resetarits, W.J. & Willbur, H.M. (1989) Choice of oviposition site by Hyla
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chrysoscelis: role of predators and competitors. Ecology 70, 220–228.
14
Romero, G.Q. & Vasconcellos-Neto, J. (2005) The effect of plant structure on the
15
spatial and microspatial distribution of a bromeliad-living jumping spider (Salticidae).
16
Journal of Animal Ecology 74, 12–21.
17
Rudolf, V.H.W. & Rödel, M.O. (2005) Oviposition site selection in a complex and
18
variable environment: the role of habitat quality and conspecific cues. Oecologia 142,
19
316–325.
20
Sampaio, M.C., Picó, F.X. & Scarano, F.R. (2005) Ramet demography of a nurse
21
bromeliad in Brazilian restingas. American Journal of Botany 92, 674–681.
11
1
Schiesari, L., Gordo, M. & Hodl, W. (2003) Treeholes as calling, breeding, and
2
developmental sites for the amazonian canopy frog, Phrynohyas resinifictrix (Hylidae).
3
Copeia 2, 263–272.
4
Schineider, J.A. & Teixeira, R.L. (2001) Relacionamento entre anfíbios anuros e
5
bromélias da restinga de Regência, Linhares, Espírito Santo, Brasil. Iheringia 91, 41–
6
48.
7
Silva, H.R. & Britto-Pereira, M.C. (2006) How much fruit do fruit-eating frogs eat? An
8
investigation on the diet of Xenohyla truncata (Lissamphibia: Anura: Hylidae). Journal
9
of Zoology 270, 692–698.
10
Simon, J.E. & Gasparini, J.L. (2003) Descrição da vocalização de Phyllodytes kautskyi
11
Peixoto e Cruz, 1988 (Amphibia, Anura, Hylidae). Boletim do Museu de Biologia Mello
12
Leitão 16, 47–54.
13
Smith, L.B. & Downs, R.J. (1979) Bromeliaceae (Bromelioideae). Flora Neotropica 14,
14
1493–2142.
15
Vieira, W.S., Santana, G.G., Dos Santos, S.C.D.C., Alves, R.R.N. & Pereira-Filho, G.A.
16
(2009) Description of the tadpoles of Phyllodytes brevirostris (Anura: Hylidae).
17
Zootaxa 2119, 66–68.
18
Weygoldt, P. (1981). Beobachtungen zur fortpflanzungsbiologie von Phyllodytes
19
luteolus (Wied 1824) im terrarium (Amphibia: Salientia: Hylidae). Salamandra 17, 1–1.
12
A
B
Figura 1. Área de estudo na Praia do Forte, Município de Mata de São João, Estado da Bahia, Brasil. A – área de estudo: ambiente de restinga
arbóreo-arbustiva com moitas de bromélias terrestres, estas últimas indicadas por setas na cor vermelha. B – detalhe da bromélia terrestre
Aechmea cf. aquilega, espécie abundante na área de estudo e utilizada por Phyllodytes melanomystax como sítio de vocalização.
13
A
B
C
D
Figura 2. O anuro Phyllodytes melanomystax em quatro diferentes momentos. A, girino
no tanque central da bromélia; B, macho vocalizante no tanque central da bromélia; C,
macho e fêmea juntos em uma mesma bromélia; D, vista frontal de P. melanomystax
destacando o “bigode” característico da espécie.
14
Artigo
Este capítulo é aqui apresentado sob a forma de artigo a ser submetido ao
periódico Journal of Animal Ecology, sob o título “Calling site selection by the
bromeliad-dwelling treefrog Phyllodytes melanomystax (Amphibia: Anura: Hylidae) in
a coastal sand dune habitat”. As normas de publicação no respectivo periódico se
encontram como anexo a esta dissertação.
15
1
Calling site selection by the bromeliad-dwelling treefrog Phyllodytes melanomystax
2
(Amphibia: Anura: Hylidae) in a coastal sand dune habitat
3
Maria Silva CUNHA¹,³ and Marcelo Felgueiras NAPOLI²
4
¹Programa de Pós-Graduação em Ecologia e Biomonitoramento, Instituto de Biologia,
5
Universidade Federal da Bahia, Rua Barão de Jeremoabo, Campus Universitário de
6
Ondina, 40170-115 Salvador, Bahia, Brazil
7
²Museu de Zoologia, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão
8
de Jeremoabo, Campus Universitário de Ondina, 40170-115 Salvador, Bahia, Brazil. E-
9
mail: [email protected]
10
11
3
Corresponding author: [email protected]
Running headline: Calling site selection by a bromeliad-dwelling frog
12
16
1
Summary
2
1. Tank bromeliads are able to accumulate rainwater within their rosettes, forming small
3
bodies of water known as phytotelms. These bromeliads are used by a great variety of
4
vertebrates and invertebrates and some species spend their entire life cycle inside tank-
5
bromeliads. It is known that for anurans there is a non-random use of bromeliads, but
6
the environmental factors that drive this selection are still poorly known.
7
2. In this study, variables associated to bromeliad selection by calling males of the
8
bromeliad-inhabiting frog Phyllodytes melanomystax were investigated. Novel natural
9
history observations of the focused species also were provided.
10
3. The study site was a sand-dune restinga environment, located in the Municipality of
11
Mata de São João, northern coast of Bahia State, northeastern Brazil. Two hundred and
12
two terrestrial bromeliads were sampled, 101 with and 101 without calling males of P.
13
melanomystax. Nine environmental variables (predictors) related in literature as
14
possibly associated to bromeliad selection by anurans were measured. Multiple logistic
15
regression analysis and Wald test were performed to test which environmental variables
16
could explain the occurrence of calling males of P. melanomystax within terrestrial
17
bromeliads.
18
4. The presence/absence of calling males of P. melanomystax in bromeliads was
19
influenced by number of bromeliads in a 2 meters radius and amount of debris inside
20
the rosettes, while physical and/or chemical variables of bromeliads and from stored
21
water inside the rosettes had no influence. The marking-recapture procedure of P.
22
melanomystax evidenced strong site fidelity for males. Yet, it was observed that males
23
calling sites were also used by the species as oviposition sites and for development of
24
tadpoles.
17
1
5. This is the first research to explain the pattern of bromeliad selection by a species of
2
the bromeliad-dwelling frog genus Phyllodytes.
3
4
Keywords: bromeligen species, microhabitat selection, phytotelm.
18
1
Introduction
2
Selection of calling sites is a critical factor that affects the success of males of
3
many anuran species, as females may choose their mates not only by its acoustic and
4
physical characteristics, but also by the quality of the site for offspring (Duellman &
5
Trueb 1986). Anurans from tropical regions show a great variety of reproductive modes
6
(Haddad & Prado 2005), using an array of different microhabitats. By using different
7
microhabitats they face different situations, and the environmental factors that influence
8
the mechanisms of calling site selection also can change.
9
Phytotelm-dwelling anurans face risks and situations unusual to traditional
10
habitats like ponds and streams (Lehtinen et al. 2004). Phytotelms are small bodies of
11
water formed by accumulation of rainwater within plants or parts of plants, such as
12
treeholes, bromeliad rosettes, and bamboo stumps (Kitching 2001; Schiesari, Gordo &
13
Hödl 2003). Not surprisingly, phytotelm-inhabiting anurans have to deal with situations
14
as unpredictable food availability, low dissolved oxygen concentrations, and high
15
desiccation risk (Lehtinen et al. 2004). However, compared to pond and streams,
16
phytotelms are known as safe reproduction sites, because these sites do not have major
17
traditional predators for eggs and tadpoles, and consequently forces like predation and
18
competition are not so pronounced (Schiesari, Gordo & Hödl 2003), though predators
19
like larvae of Zygoptera and Anisoptera (Insecta, Odonata) and crabs are not rare in
20
terrestrial bromeliads of restinga habitats (MF Napoli, personal observation). Predation
21
pressure on eggs and tadpoles are referred as major forces that influence the evolution
22
of alternative reproductive strategies (Magnusson & Hero 1991), like use of phytotelms
23
as reproductive sites by anurans.
24
Among phytotelms, bromeliads are known as key plants for tropical regions
25
because sometimes they hold inside their tanks the unique source of available
19
1
freshwater (Neill 1951). Many species of vertebrates and invertebrates use bromeliads
2
for shelter or during foraging activity, and some species can spend their entire life cycle
3
inside tank-bromeliads (Neill 1951; Laessle 1961; Juncá & Borges 2002; Srivastava et
4
al. 2004; Lopez et al. 2005). Tank-bromeliad is a common name given to bromeliad
5
species that accumulate water because of the configuration of its leaves. These leaves
6
alternate and arrange in spiral and this arrangement permit them to accumulate water
7
and dry leaves from the canopy within the leaf axils and inside the central tank (Fig. 1).
8
Bromeliad-dwelling
anurans
usually have
pronounced
mechanisms
of
9
microhabitat selection. Males of Scinax perpusillus (Lutz & Lutz, 1939), for example,
10
prefer clustered and terrestrial bromeliads, a preference associated to territorial behavior
11
(Oliveira & Navas 2004). Additionally, species of the S. perpusillus group have a
12
sophisticated reproductive system, which involves from an elaborated acoustic repertory
13
in males to a complex oviposition control in females (Alves-Silva & Silva 2009).
14
Complex reproductive systems and non-random bromeliad use were also reported for
15
other bromeliad frogs as Anomaloglossus beebei (Noble, 1923) (Bourne et al. 2001),
16
and for other phytotelm anurans like Kurixalus eiffingeri (Boettger, 1895) (Lin et al.
17
2008), Ranitomeya variabilis (Zimmermann & Zimmermann, 1988), R. imitator
18
(Schulte, 1986) (Brown et al. 2008), and Mantella laevigata Methuen & Hewitt, 1913
19
(Heying 2008).
20
The genus Phyllodytes Wagler, 1830 is entirely composed by small bromeliad-
21
dwelling treefrogs distributed along the Tropical Atlantic Forest (Caramaschi, Peixoto
22
& Rodrigues 2004), but little is known about the nature of the relationship between
23
Phyllodytes and bromeliads. These frogs spend their entire life cycle inside the
24
bromeliads, using them as calling and retreat sites (Eterovick 1999), and local for
25
reproduction and deposition of eggs and tadpoles (Peixoto 1995). Few data on natural
20
1
history and ecology are available for P. luteolus (Eterovick 1999; Schineider & Teixeira
2
2001), and the remaining studies on Phyllodytes have a taxonomic approach (e.g.:
3
Peixoto, Caramaschi & Freire 1999, Caramaschi, Peixoto & Rodrigues 2004, Vieira et
4
al. 2009). In view of the high microhabitat specificity of Phyllodytes species, and of the
5
poorly known relationship between them and bromeliads, it is important to conduct
6
studies to clarify some aspects of microhabitat use by these species.
7
The treefrog Phyllodytes melanomystax Caramaschi, Silva & Britto-Pereira,
8
1992, is distributed from southern State of Sergipe to southern State of Bahia, Brazil
9
(Peixoto & Pimenta 2008). This species is very abundant in northern coast of the State
10
of Bahia, in a region known as Litoral Norte, which is composed in most part by coastal
11
sand dune habitats covered with herbaceous and shrubby vegetation, which is common
12
along the Brazilian coast and known as ‘restinga’ (Suguio & Tessler, 1984). The region
13
is suffering a process of habitat loss due to unregulated tourism and to conversion of the
14
restingas into resorts and residential areas.
15
In this paper, Phyllodytes melanomystax was used as a model species for
16
investigating the variables associated to site selection by the bromeliad-dwelling frog
17
genus Phyllodytes. Two questions were addressed: (1) is there any pattern in bromeliad
18
use by these frogs? (2) Which environmental variables influence the selection of
19
bromeliads by calling males of P. melanomystax? Calling males were used as a model
20
for selection system, and we also made some novel natural history observations that
21
could help to understand our results.
22
21
1
Material and Methods
2
Study Area
3
The field study was conducted from 9 April to 7 May 2010 in a private property
4
located in Praia do Forte, Municipality of Mata de São João, State of Bahia, Brazil (12º
5
34' 12'' S; 38º 00' 04'' W, 10 m above sea level). The property is located in the State
6
environmental protected area APA Litoral Norte (see Bastazini et al. 2007 for a location
7
map). The study area is a coastal sand dune habitat covered with herbaceous and
8
shrubby vegetation, known as ‘restinga’, a sandy coastal plain vegetation from the
9
Brazilian Atlantic Forest biome (Scarano et al. 2002).
10
11
Research Design and Field Methods
12
A sampling polygon of 1700 x 400 m was delimited within the study area, in
13
which 202 bromeliads (sample units—SU) were randomly sampled following a point
14
map. For the construction of the map, 202 values ranging from 0 to 1700 m
15
(representing the major axis of the polygon) and 202 values from 0 to 400 m
16
(representing the minor axis of the polygon) were obtained at a random, and then
17
randomly combined into ordered pairs. Each ordered pair corresponded to a SU. When a
18
bromeliad was not in the exact point previously chosen at random, the nearest
19
bromeliad was measured. A single species of tank-bromeliad was sampled to avoid
20
sampling biases due to species-specific structural distinctiveness, of which was elected
21
for sampling the most abundant tank-bromeliad in the study area, Aechmea aquilega
22
(Salisb.) Griseb., 1864. Bromeliads (SUs) were divided into two categories: unoccupied
23
(category 0) and occupied bromeliads (category 1) by calling males of P. melanomystax.
24
The same number of bromeliads was sampled for each category (101 bromeliads per
22
1
category), totalizing 202 SUs. Voucher specimens of P. melanomystax were deposited
2
in the Museu de Zoologia da Universidade Federal da Bahia (UFBA 10653–10712).
3
Bromeliads with or without calling males of Phyllodytes melanomystax were
4
determined by active search from 17h30min to 22h30min, time interval corresponding
5
to the vocal activity for this species (M.S. Cunha personal observation). This procedure
6
was adopted assuming that we only could determine whether a bromeliad was occupied
7
or not by males of P. melanomystax when searching at night, because during periods of
8
sunlight these treefrogs always drop into the leaf axils, which makes it quite impossible
9
to see and reach them without damage the bromeliad. After each night, 10 bromeliads
10
were marked with small plastic strips and then georeferenced. These procedures were
11
repeated until we reached the total of 202 sampled bromeliads (20 days of searching).
12
It was respected the minimal distance of 20 m between SUs and this value was
13
assumed as enough to assure independence of sample units. In order to test the
14
efficiency of this value, the home range of Phyllodytes melanomystax was investigated
15
with a capture-marking-recapture experiment. Thus, if the home range of P.
16
melanomystax calling males was smaller than 20 m, the samples were independent.
17
From the 101 males observed in calling activity in bromeliads from category 1, it was
18
captured the maximal number of males as possible throughout the 20 days of data
19
collection. Fifty-two males of P. melanomystax were marked using the toe-clipping
20
method (Martoff 1953) with a small modification: instead of clipping the toe as a whole,
21
only the disc was removed. Marked individuals were released soon after the marking in
22
the same bromeliad where they were captured. The recapture period was in the last
23
week of field research (03–07 May 2010). Some natural history observations (for
24
example, calling position inside the bromeliad, presence of another calling males etc.)
25
were also made during data collection. Before capturing a male, it was spent
23
1
approximately 5 minutes in silent to observe how many active males there were in that
2
clump. This observation was also made during the time spent for marking the males and
3
signalizing the sample unit, which took approximately 10–15 minutes of observations in
4
each point.
5
In the morning after marking the bromeliads, from 6h to 11h, nine predictor
6
variables from each marked bromeliad were measured: (1) volume, (2) temperature, and
7
(3) pH of stored water in bromeliad rosette, (4) amount of debris inside the bromeliad
8
tank, (5) number of leaf axils with water, (6) bromeliad tank height, (7) maximum
9
bromeliad diameter, (8) number of bromeliads in a 2 m radius, and (9) distance of the
10
referred bromeliad to the next bromeliad cluster. Variables 8 and 9 correspond to a
11
measure of bromeliad/cluster isolation. Bromeliad clumps varied in size and shape, but
12
they were elliptical-shaped by most times. The size of the clump varied from clumps
13
formed by just three bromeliads (± 1 m2) to clumps with more than one hundred
14
bromeliads (more than 20 m2). Water temperature was recorded with a digital thermo-
15
hygrometer to the nearest 0.1ºC directly from inside the bromeliad. For variables 1 and
16
3 the entire volume of water was extracted inside the bromeliad rosette with a plastic
17
tube connected to a recipient, a device similar to that used by Guimarães-Souza et al.
18
(2006) and Jabiol, Corbara & Céréghino (2009). Water volume was measured in a
19
graduated cylinder to the nearest 0.1 ml, and pH with a digital pH meter to the nearest
20
0.1. The amount of debris was recorded following a similar procedure used by Osses,
21
Martins & Machado (2008), as an ordinal variable (1–4): 1—smallest amount of debris;
22
2—large amount of debris, but not enough to prevent a specimen of P. melanomystax
23
from passing through the bromeliad central tank or leaf axils; 3—very large amount of
24
debris, but still passage free; 4—largest amount of debris, blocking passage to central
25
tank and leaf axils. In order to avoid temporal biases during the period of the
24
1
measurement of variables (from 6h to 11h), as temperature increasing, we alternated the
2
sampling of bromeliads without (category 0) and bromeliads with P. melanomystax
3
(category 1).
4
5
Data Analysis
6
For the purpose of analysis, three data matrices were produced: (A) a matrix of
7
202 sample units (bromeliads, objects) vs. the presence (1) or absence (0) of Phyllodytes
8
melanomystax (attribute), representing the dependent variable of the analysis; (B) a
9
matrix of 202 sample units (bromeliads, objects) vs. 9 predictor variables, representing
10
the independent variables of the analysis; (C) similar to matrix B, but only with
11
uncorrelated predictor variables (n = 7). Five bromeliads lacked stored water in their
12
rosettes, and therefore no values referring to water related variables were entered in
13
matrices B and C. Descriptive statistics of predictor variables are in Table 1.
14
The multiple logistic regression was used to determine which predictor variables
15
(matrix C) were important for the selection of calling sites (bromeliads) by P.
16
melanomystax and to create a predictive habitat model based on presence/absence data
17
(matrix A). As in linear regressions, multiple logistic regressions have the assumption
18
of collinearity absence between independent variables (Gotelli & Ellison 2004). As
19
some variables did not present normal distribution, the existence of significant
20
correlations between predictor variables were tested using the Spearman rank
21
correlation (R), adjusting the α-level (P ≤ 0.05) by the Bonferroni correction (Bland
22
2000). Three significant correlations resulted from this analysis: number of leaf axils
23
with water vs. volume of stored water in bromeliad rosette, number of leaf axils with
24
water vs. amount of debris inside the bromeliad tank, and bromeliad tank height vs.
25
1
volume of stored water in bromeliad rosette (Table 2). The variables number of leaf
2
axils with water and bromeliad tank height were excluded from analysis because
3
volume of stored water in bromeliad rosette has a great biological meaning for
4
phytotelm-dwelling anurans (Bourne et al. 2001, Schiesari, Gordo & Hödl 2003), and
5
recent studies showed that amount of debris is a microhabitat selection criterion for
6
some bromeliad-inhabiting animals (Romero & Vasconcelos-Neto 2005; Osses, Martins
7
& Machado 2008). Therefore, the multiple logistic regression analysis was performed
8
with seven predictor variables. The Wald statistics (Quinn & Keough 2002) was used to
9
test the null hypothesis that any of the independent variables recorded influenced the
10
presence/absence of P. melanomystax in bromeliads. The Wald statistics tests the
11
contribution of each independent variable to the response variable individually when all
12
other variables are constant, revealing the effect of each variable independently. The α-
13
level (P ≤ 0.05) was Bonferroni corrected to control Type I error rate when using
14
multiple tests (Bland 2004). For evaluating the goodness of fit of the model and its
15
predictive performance, the statistics of Hosmer-Lemeshow was conducted (Hosmer &
16
Lemeshow 2000). In this analysis, the null hypothesis is that there is no evidence for
17
lack of fit of the model, and therefore if null hypothesis is rejected the model is not well
18
adjusted. Specificity or true negative fraction (proportion of correct predictions for the
19
absence), sensitivity or true positive fraction (proportion of correct predictions for the
20
presence), and overall success rate of the model were calculated (Rudolf & Rödel
21
2005).
22
26
1
Results
2
Microhabitat variables and natural history notes
3
Calling specimens of Phyllodytes melanomystax always were obtained from
4
bromeliads filled with water. Out of 52 marked males, 27 (52%) were recaptured, all of
5
them during calling activity. The distance between release and recapture points was low
6
(0.27–11.5 m, X = 4.30 m ± 3.4 m), and three recaptured males were found in the same
7
bromeliads they were released. The amount of recaptured males from the first sampling
8
days was similar to that from the last sampling days.
9
Calling activity of Phyllodytes melanomystax took place from sunset to dawn,
10
with the activity peak ranging from 19h to 21h. Calling males were located
11
preferentially in the central tank (n = 50, 94%), with the head pointed to the external
12
side of the bromeliad (Fig. 2). Males calling from leaf axils were less frequent (n = 3,
13
6%). By three times we saw a female in the same bromeliad of a calling male, but not in
14
amplexus, and by one time we observed a female perched on the vegetation above the
15
bromeliad with a calling male. In two occasions we saw two calling males in a single
16
bromeliad, one on the central tank and the other in a leaf axil. Both pairs of calling
17
males were performing advertisement call. More frequently (not quantified), we
18
observed only one male per bromeliad cluster, but there were a few occasions where
19
there were more than one calling male in a single cluster.
20
We found tadpoles of Phyllodytes melanomystax in 25 (25%) of the 101
21
bromeliads with calling males, with 1 to 32 tadpoles per bromeliad ( X = 6.0±6.0).
22
Tadpoles or eggs were not observed in bromeliads without calling males of P.
23
melanomystax. The volume of water inside bromeliads rosettes with tadpoles varied
27
1
from 130 ml to 1237 ml ( X = 429.4±257.0 ml). We observed egg clutches of P.
2
melanomystax in two bromeliads that also had tadpoles, one with 12 eggs and the other
3
with 14 eggs. The 12-eggs clutch was found in a bromeliad of 480 ml with four
4
tadpoles; the 14-eggs clutch in a bromeliad of 270 ml with 32 tadpoles. All tadpoles and
5
egg clutches were found in the water stored inside the central tank of the bromeliad. It
6
was not possible to determine the stages (Gosner 1960) of the tadpoles found in the
7
same bromeliads, but it was visually possible to confirm that there were tadpoles two to
8
three times larger than others from the same site.
9
10
Statistical analysis
11
The Wald hypothesis test indicated that only predictor variables (1) number of
12
bromeliads in a 2 meter radius and (2) amount of debris inside the bromeliad tank
13
influenced the presence/absence of calling specimens of Phyllodytes melanomystax in
14
terrestrial bromeliads (Table 3). The number of bromeliads in a 2 meter radius
15
influenced positively the probability of occurrence of calling males in bromeliads,
16
indicating an avoidance of isolated bromeliads, and a preference for clustered
17
bromeliads (Fig. 3a). On the other hand, the amount of debris influenced negatively the
18
probability of occurrence of calling males in bromeliads, indicating an avoidance of
19
bromeliads with a great amount of debris, and a preference for calling sites with no or
20
with small amount of debris (Fig. 3b). The Hosmer-Lemeshow statistics accepted the
21
null-hypothesis that there is no evidence for lack of fit of the data (Chi-Square = 4.04,
22
DF = 8, P > 0.85), and therefore the model is well data adjusted. The high specificity
23
(71.6%), sensitivity (73.5%), and overall success rate (72.5%) of the model indicated
24
that it predicted most of the unused and used sites correctly (Table 4).
28
1
Discussion
2
The calling site of Phyllodytes melanomystax in terrestrial bromeliads of the
3
study area was similar to that published for P. luteolus (Wied-Neuwied, 1824)
4
(Eterovick 1999). Both species use the central tank of bromeliads and their leaf axils to
5
call, but P. melanomystax differs by using the central tank as the primary calling site,
6
while in P. luteolus there was no detected difference. The more frequent use of the
7
bromeliad central tank as the main calling site by P. melanomystax possibly is due to
8
the structure of the terrestrial bromeliads investigated, with close leafs and central tank
9
as the main bromeliad water reservoir. The morphological structure of these bromeliads
10
may be a response to the high sunlight incidence over these plants. It is known that
11
bromeliads can modify structural characteristics, as morphology of leaves, shape and
12
size of the tank, and photochemical efficiency in response to variations in light and
13
flooding regimes (Cogliatti-Carvalho, Almeida & Rocha 1998; Scarano et al. 2002).
14
Although up till now there is no study providing these responses for Aechmea cf.
15
aquilega, we assume that as phenotypic plasticity is a common characteristic of
16
Bromeliaceae, it is possible to be happening to this species in our study site.
17
The volume of stored water in terrestrial bromeliads was not able to explain the
18
calling site selection by adult males of Phyllodytes melanomystax. The results presented
19
here agree with Schineider & Teixeira (2001), which argued that the volume of water
20
stored in bromeliads is not important for P. luteolus. Nevertheless, Eterovick (1999)
21
observed for P. luteolus that volume and pH of water were statistically different
22
between occupied and unoccupied bromeliads. In fact, in the study area, calling males
23
of P. melanomystax did not occur in terrestrial bromeliads without stored water, which
24
points out to the presence of it as a primary condition for choice of the bromeliad by this
29
1
treefrog. A water reservoir is essential for the maintenance of hydric balance by the
2
animal, and for the development of tadpoles (Duellman & Trueb 1986). On the other
3
hand, bromeliads with small amounts of stored water (minimum of 85 ml) were used as
4
call sites by males of P. melanomystax, which led us to conclude that the presence of
5
stored water, even in low volumes, qualifies a terrestrial bromeliad of an open habitat to
6
host a calling male of P. melanomystax, but the increase of stored water does not
7
improve the chance of the bromeliad to be inhabited by a calling male.
8
In the present research, isolated or clustered terrestrial bromeliads were often
9
occupied by a single calling male of Phyllodytes melanomystax, which suggests a
10
territorial behavior for adult males, and the choice of calling sites as a valuable
11
parameter for the species reproductive success. In assuming the territoriality of adult
12
males, the preference for clustered bromeliads by a calling male also implies that its
13
territory was represented by the entire bromeliad cluster. Similar territoriality was
14
reported for Scinax perpusillus, where adult males defend not only a single bromeliad,
15
but also prefer isolated clusters of bromeliads, possibly to have access to several
16
potential oviposition sites that might confer reproductive advantages, and to reduce
17
intra-sexual competition (Oliveira & Navas 2004). As for P. melanomystax, variables
18
related to spatial distribution of bromeliads were more important to call site selection in
19
S. perpusillus than physical and chemical parameters of the bromeliad (Oliveira &
20
Navas 2004).
21
The presence of tadpoles and eggs of Phyllodytes melanomystax in the same
22
terrestrial bromeliads of conspecific calling males points out that the species possibly
23
uses the same sites for calling, egg-laying, and tadpole development, as observed for P.
24
luteolus by Eterovick (1999). Nevertheless, the reproductive characteristics of P.
30
1
melanomystax in the study site differs from that of P. luteolus because eggs and
2
tadpoles of P. melanomystax were found in the central tank of the bromeliads, whereas
3
that of P. luteolus were found not only in the central tank, but also in leaf axils.
4
Furthermore, we observed a higher amount of tadpoles and eggs per clutch in P.
5
melanomystax (1–32 tadpoles, 12–14 eggs) than in P. luteolus (1–3 tadpoles, 1–3 eggs,
6
Giaretta 1996, Eterovick 1999). In respect to the number of eggs per leaf axil,
7
Caramaschi, Silva & Britto-Pereira (1992) accounted a single egg for P. melanomystax
8
(and also only 1–2 tadpoles per bromeliad), similar number observed for Scinax
9
littoreus, S. perpusillus and S. v-signatus by Alves-Silva & Silva (2009), which greatly
10
differ from our results. As any data is provided on the bromeliads investigated by
11
Caramaschi, Silva & Britto-Pereira (1992), we can not relate this distinct number of
12
eggs and tadpoles (compared to the numbers presented here) to environmental
13
differences between the two sites. However, an important question that remains
14
unresolved is whether the eggs and tadpoles housed in a same bromeliad came from the
15
same couple, or from the same male with different females, as tadpoles were of distinct
16
body sizes and perhaps from different hatchings. This information is important, as it
17
implies that a same bromeliad, or bromeliad cluster, could house a male that is chosen
18
by distinct females and reproduce with them during the same breeding season.
19
The importance of amount of debris accumulated inside the rosettes regarding to
20
its influence on bromeliad selection was first reported for the bromeliad-living spider
21
Psecas chapoda Peckham & Peckham, 1894 (Romero & Vasconcellos-Neto 2005), and
22
later, to the bromeliad-dwelling harvestmen Bourguyia hamata Kury, 2003 (Osses,
23
Martins & Machado 2008). In both cases, the influence of amount of debris was
24
negatively related for bromeliad selection, as the dry leaves prevent these animals of
31
1
reaching the center of the rosettes, and thus they cannot use bromeliads as reproduction
2
and/or shelter sites. In the case of P. chapoda, the authors conclude that these
3
observations partially agree with their previous hypothesis that this species did not
4
occur in bromeliads in the forest because of the dry leaves that fall from the forest
5
canopy inside the bromeliads. Bastazini et al. (2007) reported the high abundance of P.
6
melanomystax in our study area, and devoted this to the great number of terrestrial
7
bromeliads. However, in an adjacent area of arboreal restinga (covered by arboreal
8
vegetation, containing springs, streams, and rivers), the authors also observed plots with
9
a great amount of terrestrial bromeliads, but where P. melanomystax occurred in a much
10
lower abundance. As Romero & Vascocellos-Neto (2005) observed, terrestrial
11
bromeliads from forested areas tend to accumulate more dry leaves inside their rosettes
12
than in open areas. Based on the results presented here that amount of debris
13
(represented by dry leaves) inside the bromeliads had a negative influence on
14
occurrence of P. melanomystax, we conclude that the low abundance of this species in
15
forested areas compared to open areas (Bastazini et al. 2007) is possibly due to the great
16
amount of debris inside bromeliads in forested areas. We understand that, as in P.
17
chapoda and B. hamata, debris accumulated inside bromeliads prevent individuals of P.
18
melanomystax to reach the center of the bromeliads during the day, when they use
19
bromeliads as shelter sites, and during the night, when they go out to forage or
20
reproduce, but in danger enter through the bromeliad tank.
21
The present research determined which variables were able to explain the pattern
22
of bromeliad selection by calling males of the bromeliad-dwelling frog Phyllodytes
23
melanomystax. The number of clustered bromeliads and the amount of debris
24
accumulated inside the rosette are the most important variables affecting the presence of
32
1
calling males. None of the physical and/or chemical variables of the bromeliads, and
2
from the stored water inside the rosettes, influenced the occurrence of calling males.
3
Mark-recapture experiments showed strong site fidelity for males, as the distance
4
between the release and recapture point was very low and, in some cases, males were
5
recaptured in the same bromeliad they were released. Natural history observations
6
suggested that the pattern of bromeliad use by calling males is similar to that for
7
reproduction, egg-laying, and tadpoles’ development, but these observations are not
8
conclusive, and future studies should focus on these unanswered questions to ameliorate
9
the understanding about the narrow relationship between bromeligen anurans and
10
bromeliads.
11
33
1
Acknowledgements
2
We are grateful to E.M.S. Silva Jr., L. Menezes, R.O. Abreu, J. Ruggeri, V.
3
Bonfim, E. Petersen, T. Dória, T. Filadelfo, D. Lima, J. Melo, J. Herrera, A.L. Xavier
4
and Mr. Anísio for the excellent field assistance; we acknowledge A. Bolzico for
5
allowing us to access research areas under his care; we are grateful to L. Menezes by
6
figure 1 and T. Filadelfo by figure 2; to F.A. Juncá and M. Solé for helpful comments
7
on the manuscript; the Conselho Nacional de Desenvolvimento Científico e
8
Tecnológico (CNPq) and the Fundação de Amparo à Pesquisa do Estado da Bahia
9
(FAPESB) for fellowships to M.F. Napoli (proc. 302542/2008-6) and M.S. Cunha (term
10
of grant 0213/2009), respectively; the Instituto Brasileiro do Meio Ambiente e dos
11
Recursos Naturais Renováveis (IBAMA) that permitted collection and mark-recapture
12
of specimens (license number 22354-1).
13
34
1
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39
1
Figure captions
2
Figure 1. Schematic tank bromeliad similar to that used as sample unit in the present
3
research. 1, diameter of the bromeliad; 2, height of the central tank; 3, leaf axil; 4,
4
central tank.
5
Figure 2. Live calling male of Phyllodytes melanomystax in the central tank of a
6
terrestrial bromeliad. Males calling from central tank were more frequent than calling
7
from leaf axils.
8
Figure 3. A: presence and absence of Phyllodytes melanomystax according to the
9
number of bromeliads in a 2 meter radius. Circles of varying sizes (bubbles) represent
10
the relative frequencies of the number of points represented by a single plot position. B:
11
percentage of bromeliads used as oviposition site by the treefrog Phyllodytes
12
melanomystax (black bars) compared to the number of bromeliads not used (white bars)
13
according to the classes of amount of debris found inside the rosettes.
40
Figure 1
41
Figure 2
42
Figure 3
43
Table 1. Descriptive statistics of environmental variables in bromeliads with and
without calling males of Phyllodytes melanomystax. N, number of bromeliads; Mean,
arithmetic mean; SD, standard deviation; range, minimum and maximum values.
Abbreviations of environmental variables: temperature (TEMP), volume of stored water
in bromeliad rosettes (VOL), number of bromeliads in a 2 meter radius (NBRO),
distance of bromeliad to the next bromeliad cluster (DCL), maximum bromeliad
diameter (DIAM), amount of debris inside the bromeliad tank (DEB), number of leaf
axils with water (NAX); bromeliad tank height (HGH).
With P. melanomystax
Without P. melanomystax
Variables
N
Mean
SD
Range
N
Mean
SD
Range
TEMP
99
28.9
2.5
(24.4–35.9)
95
29.4
2.7
(25.2–36.7)
PH
101
5.0
1.0
(3.4–8.0)
96
5.2
1.1
(3.5–8.1)
VOL
101
396.4
222.3
(85.0–1237.0)
101
269.4
243.2
(0.0–1275.0)
NBRO
101
30.0
14.3
(3.0–103.0)
101
20.0
12.3
(3.0–72.0)
DCL
101
5.07
3.4
(0.86–20.9)
101
5.1
3.6
(0.5–21.0)
DIAM
101
32.2
10.9
(10.0–55.0)
101
28.4
10.2
(8.0–54.0)
DEB
100
1.0
0.6
(1.0–3.0)
101
2.0
1.1
(1.0–4.0)
NAX
101
6.0
2.4
(1.0–14.0)
101
5.0
2.8
(0.0–13.0)
HGH
101
44.2
12.7
(18.0–79.0)
101
42.9
11.9
(20.0–77.0)
44
Table 2. Spearman rank correlation coefficients for predictor variables (see caption of
table 1 for variables abbreviations). The α-level (P ≤ 0.05) was Bonferroni corrected
(*P ≤ 0.001).
Variables
TEMP
PH
VOL
NBRO
DCL
DIAM
DEB
NAX
TEMP
1.00
PH
0.04
1.00
VOL
0.02
-0.07
1.00
NBRO
-0.12
-0.02
0.07
1.00
DCL
-0.10
0.01
0.05
-0.13
1.00
DIAM
0.12
0.18
0.12
0.11
-0.02
1.00
DEB
-0.13
0.18
-0.19
-0.02
0.20
0.12
1.00
NAX
0.08
-0.01
0.46*
0.09
-0.03
0.17
-0.38*
1.00
HGH
-0.08
-0.21
0.24*
0.15
-0.05
-0.20
0.04
-0.08
HGH
1.00
45
Table 3. Variables in the equation of the multiple logistic regression analysis. See
caption of table 1 for variables abbreviations. β, regression coefficient; W, Wald value;
P, significance value (P ≤ 0.007).
Variables
β
Wald
P
CONST
0.244
0.012
0.912
NBRO
0.065
18.665
0.000
DEB
0.750
9.930
0.002
46
Table 4. Percentage of correct classification of bromeliads in two categories of response
variables: without (0) and with (1) calling males of P. melanomystax. The percentage of
correct predictions of bromeliads without males is called specificity, while that from
bromeliads with males is called sensitivity of the logistic model.
Observed
Predicted
% Correct
Without (0)
With (1)
Without (0)
68
27
71.6
With (1)
26
72
73.5
% Overall
72.5
47
Author Guidelines
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51
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53
Underwood, N. (2009) Effect of genetic variance in plant quality on the population
dynamics of a herbivorous insect. Journal of Animal Ecology, 78, 839–847.
Jonsen, I.D., Myers, R.A. & James, M.C. (2006) Robust hierarchical state–space models
reveal diel variation in travel rates of migrating leatherback turtles. Journal of Animal
Ecology, 75, 1046–1057.
Nilsen, E.B., Linnell, J.D.C., Odden, J. & Anderson, R. (2009) Climate, season, and
social status modulate the functional response of an efficient stalking predator: the
Eurasian lynx. Journal of Animal Ecology, 78, 741–751
Otto, S.P. & Day, T. (2007) A Biologist's Guide to Mathematical Modeling in Ecology
and Evolution. Princeton University Press, Princeton, New Jersey, USA.
Conway. G. (2007) A Doubly Green Revolution: ecology and food production.
Theoretical Ecology: Principles and Applications, 3rd edn (eds R. May & A. McLean),
pp. 158–171. Oxford University Press, Oxford.
Stevenson, I.R. (1994) Male-biased mortality in Soay sheep. PhD thesis, University of
Cambridge, Cambridge.
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54
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