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
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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 pré- requisito para a obtenção do título de Mestre em Ecologia e Biomonitoramento.
Salvador
2011
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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
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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
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Dedicatória
À minha mamãe, sempre!
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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).
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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.
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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),
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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.
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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
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Table 4 47 Regras para publicação no Journal of Animal Ecology 48
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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.
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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.
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1 Referências Bibliográficas
2 Alves-Silva, R. & Silva, H.R. (2009) Life in bromeliads: reproductive behaviour and the
3 monophyly of the Scinax perpusillus species group (Anura: Hylidae). Journal of
4 Natural History, 43, 205–217.
5 Armbruster, P., Hutchinson, R.A. & Cotgreave, P. (2002) Factors influencing
6 community structure in a South American tank bromeliad fauna. Oikos 96, 225–234.
7 Bastazini, C.V., Munduruca, J.F.V., Rocha, P.L.B. & Napoli, M.F. (2007) Which
8 environmental variables better explain changes in anuran community composition? A
9 case study in the Restinga of Mata de São João, Bahia, Brazil. Herpetologica, 63, 459–
10 471.
11 Bokermann, W.C. (1966) O gênero Phyllodytes Wagler (1830). Anais da Academia
12 Brasileira de Ciências 38, 335–344.
13 Bourne, G.R., Collins, A.C., Holder, A.M. & McCarthy, C.L. (2001) Vocal
14 communication and reproductive behavior of the frog Colostethus beebei in Guyana.
15 Journal of Herpetology 35, 272–281.
16 Brown, J.L., Morales, V. & Summers, K. (2008a). Divergence in parental care, habitat
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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 3Corresponding author: [email protected]
11 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
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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 HGH 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 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
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During submission, all authors must confirm that:
the work as submitted has not been published or accepted for publication, nor is being considered for publication elsewhere, either in whole or substantial part; the work is original and all necessary acknowledgements have been made; all authors and relevant institutions have read the submitted version of the manuscript and approve its submission; all persons entitled to authorship have been so included; the work conforms to the legal requirements of the country in which it was carried out, and to accepted international ethical standards, including those relating to conservation and animal welfare, and to the journal's policy on these matters (see 'Welfare and Legal Policy' above).
Pre-submission English-language editing Authors for whom English is a second language may wish to consider having their manuscript professionally edited before submission to improve the English. A list of independent suppliers of editing services can be found at www.blackwellpublishing.com/bauthor/english_language.asp. All services are paid for and arranged by the author, and use of one of these services does not guarantee acceptance or preference for publication.
Types of papers
STANDARD PAPERS A standard paper should not normally be longer than 10 printed pages (8500 words). (A page of printed text, without figures/tables carries c. 800 words.) The passive voice is preferred in describing methods and results. The active voice may be used occasionally to emphasize a personal opinion (typically in Introduction and Discussion sections). The typescript should be arranged as follows, with each section starting on a separate page.
Title page. This should contain:
1. A concise and informative title (as short as possible). Do not include the authorities for taxonomic names in the title. Titles with numerical series designations (I, II, III, etc.) are acceptable provided the editors agreement is sought and that at least Part II of the series has been submitted and accepted before Part I is sent to the printer. Such series must begin in one of the journals of the BES. 2. A list of authors' names with names and addresses of Institutions. 3. The name, address and e-mail address of the correspondence author to whom proofs will be sent. 4. A running headline of not more than 45 characters.
Summary. This should summarize the main results and conclusions of the paper, using simple, factual, numbered statements. It must not exceed 350 words.
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Summaries should be understandable in isolation. Summaries must start with point 1 describing, for example, the broad conceptual question addressed by the study Summaries should end with a final point highlighting the broader conceptual implication of the results and conclusions of the current study. Advice for optimizing your Summary (and Title) so that your paper is more likely to be found in online searches is provided at http://www.blackwellpublishing.com/bauthor/seo.asp
Key-words. Listed in alphabetical order, the key-words should not exceed 10 words or short phrases.
Please pay attention to the keywords you select: they should not already appear in the title or abstract. Rather, they should be selected to draw in readers from wider areas that might not otherwise pick up your paper when they are using search engines.
Introduction. This should state the reason for doing the work, the nature of the hypothesis or hypotheses under consideration, and should outline the essential background.
Materials and methods. This should provide sufficient details of the techniques to enable the work to be repeated. Do not describe or refer to commonplace statistical tests in Methods but allude to them briefly in Results.
Results. This should state the results, drawing attention in the text to important details shown in tables and figures.
Discussion. This should point out the significance of the results in relation to the reasons for doing the work, and place them in the context of other work.
Acknowledgements. In addition to acknowledging collaborators and research assistants, include relevant permit numbers (including institutional animal use permits), acknowledgment of funding sources, and give recognition to nature reserves or other organizations that made this work possible. Do not acknowledge Editors by name.
References (see Specifications).
Tables (see Specifications). These should be referred to in the text as Table 1, etc. Do not present the same data in both figure and table form.
Figure legends (see Specifications). Figures should be referred to in the text as Fig. 1, etc. (note Figs 1 and 2 with no period).
Illustrations (see Specifications) should be referred to as Figures.
REVIEWS The editors welcome short review articles on topical subjects which are of general
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interest to the readership. Intending authors are advised to consult with the editors before preparing essays for submission.
FORUM This section of the journal is designed to stimulate scientific debate. Contributions may be short articles presenting new ideas (without data), opinions or responses to material published in the journal. A cover letter is a requirement for all forum pieces.
IN FOCUS In Focus articles are short pieces designed to draw attention to papers of high expected interest in each issue of the journal. The In Focus articles act as mini-reviews that expand the context of the paper they are featuring, and they are generally commissioned by the Editors and Associate Editors. Guidelines for invited authors are available on the ScholarOne Manuscripts site at http://mc.manuscriptcentral.com/jae-besjournals.
BOOK REVIEWS Journal of Animal Ecology no longer publishes book reviews.
For general tips and guidance for authors or article preparation and submission visit the Wiley-Blackwell Author Services site.
Specifications
Figures The publishers would like to receive your artwork in electronic form. Please save vector graphics (e.g. line artwork) in Encapsulated Postscript Format (EPS), and bitmap files (e.g. half-tones) in Tagged Image File Format (TIFF). Ideally, vector graphics that have been saved in a metafile (.WMF) or pict (.PCT) format should be embedded within the body of the text file. Detailed information on the Wiley-Blackwell digital illustration standards is available at: http://www.blackwellpublishing.com/bauthor/illustration.asp
Figures should not be boxed (superfluous bounding axes) and tick marks must be on the inside of the axes. Where possible, figures should fit on a single page in the submitted paper. In a final version they will generally be reduced in size by about 50% during production. Wherever possible, they should be sized to fit into a single column width (c. 70mm final size). To make best use of space, you may need to rearrange parts of figures (e.g. so that they appear side by side). Please ensure that symbols, labels, etc. are large enough to allow reduction to a final size of c. 8 point, i.e. capital letters will be about 2 mm tall. Lettering should use a sans serif font (e.g. Helvetica and Arial) with capitals used for the initial letter of the first word only. Bold lettering should not be used. Units of axes should appear in parentheses after the axis name. Please note that line figures should be at least 600 dpi and half-tones (photos) should be at least 300 dpi.
Images in the printed version of the Journal of Animal Ecology are in black and white as it is the policy of the Journal of Animal Ecology for authors to pay the full cost for colour paper print reproduction (currently £150 for the first figure, £50 thereafter). Free colour reproduction is available for the on line version: if authors require this, they should write their figure legend to accommodate both versions of the figure, and indicate their colour requirements on the Colour Work Agreement Form. This form 52
should be completed in all instances where authors require colour, whether in print or online. Therefore, at acceptance, please download the form and return it to the Production Editor (Penny Baker, Wiley-Blackwell, John Wiley & Sons, 9600 Garsington Road, Oxford OX4 2DQ, UK. E-mail: [email protected]). Please note that if you require colour content your paper cannot be published until this form is received.
Figure legends Legends should be grouped on a separate sheet. Furnish enough detail so that the figure can be understood without reference to the text. In the full-text online edition of the journal, figure legends may be truncated in abbreviated links to the full screen version. Therefore, the first 100 characters of any legend should inform the reader of key aspects of the figure.
Tables Each table should be on a separate page, numbered and accompanied by a title at the top.
Supporting Information Journal of Animal Ecology rarely publishes Appendices in the printed version. However, Supporting Information that is referred to in the text may be made available in the online version of the article. Guidelines for the preparation of Supporting Information are available here.
For the printed version, any Appendices should be listed under 'Supporting Information', and added after the References, with the opening statement: 'The following Supporting Information is available for this article online' followed by brief captions for the Appendices/Figs/Tables to be included. These should be numbered Appendix S1, Fig. S1, Table S1, etc.
Any literature referred to in the Appendix or online Supporting Information should also be referenced in the Appendix or online Supporting Information so that it is a self- contained piece of work. This may mean duplicating references if any literature is cited in both the main text and the Supporting Information.
All Supporting Information should be submitted online as part of the main manuscript. Please name your online supporting files as „online supporting information' and upload them with the main document. This allows the submission web site to combine all the relevant files together but keep them separate when it comes to publication stage.
References References in the text to work by up to three authors should be in full, e.g. (Johnson, Myers & James 2006). If there are more than three authors, they should always be abbreviated thus: (Nilsen et al. 2009). When different groups of authors with the same first author and date occur, they should be cited thus: (Jonsen, Myers & James 2006a; Jonsen, James & Myers 2006b), then subsequently abbreviated to (Jonsen et al. 2006a, b). The references in the list should be in alphabetical order with the journal name in full. The format for papers, entire books, chapters in books, and PhD theses is as follows. 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.
References should only be cited as 'in press' if the paper has been accepted for publication. Other references should be cited as 'unpublished' and not included in the list. Work not yet accepted for publication may be cited in the text and attributed to its author as: author name (including initials), unpublished data. In press articles should be uploaded with the manuscript as „supplementary files‟.
We recommend the use of a tool such as EndNote or Reference Manager for reference management and formatting. EndNote reference styles can be searched for here: http://www.endnote.com/support/enstyles.asp
Reference Manager reference styles can be searched for here: http://www.refman.com/support/rmstyles.asp
Citations from the World Wide Web Citations from the world-wide-web are only allowed when alternative hard literature sources do not exist for the cited information. Authors are asked to ensure that:
Fully authenticated addresses are included in the reference list, along with titles, years and authors of the sources being cited. The sites or information sources have sufficient longevity and ease of access for others to follow up the citation. The information is of a scientific quality at least equal to that of peer reviewed information available in learned scientific journals.
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Units, symbols and abbreviations Authors are requested to use the International System of Units (SI, Système International d'Unités) where possible for all measurements (see Quantities, Units and Symbols, 2nd edn (1975) The Royal Society, London). Note that mathematical expressions should contain symbols not abbreviations. If the paper contains many symbols, it is recommended that they should be defined as early in the text as possible, or within a subsection of the Materials and methods section.
Scientific names Give the Latin names of each species in full, together with the authority for its name, at first mention in the main text. If they appear in the Summary/Abstract, use the common and Latin name only in the first instance, then the Latin or common name thereafter. If there are many species, cite a Flora or checklist which may be consulted for authorities instead of listing them in the text. Do not give authorities for species cited from published references. Give priority to scientific names in the text (with colloquial names in parentheses, if desired).
Makers' names When a special piece of equipment has been used it should be described so that the reader can trace its specifications by writing to the manufacturer; thus: 'Data were collected using a solid-state data logger (CR21X, Campbell Scientific, Utah, USA)'.
Mathematical material Mathematical expressions should be carefully represented. Suffixes and operators such as d, log, ln and exp will be set in Roman type; matrices and vectors will be set in bold type; other algebraic symbols will be set in italic. Make sure that there is no confusion between similar characters like 'l' (ell) and '1' (one). Also make sure that expressions are spaced as you would like them to appear, and if there are several equations they should be identified by eqn 1, etc.
Numbers in tables Do not use an excessive number of digits when writing a decimal number to represent the mean of a set of measurements (the number of digits should reflect the precision of the measurement).
Numbers in text Numbers from one to nine should be spelled out except when used with units; e.g. two eyes but 10 stomata and 5°C.
Accepted papers At the conditionally accepted stage all authors are asked to submit their final manuscript text in word format with figures and tables conforming to the specifications above and must include all required forms (nb Colour Artwork form for any colour figures and Exclusive Licence form).
Exclusive Licence Form Authors will be required to sign an Exclusive Licence Form (ELF) for all papers accepted for publication. This can also be downloaded via the 'Instructions and forms' icon located on the ScholarOne Manuscripts website. Please read carefully before 55
signing: conditions are changed from time to time and may not be the same as the last time you completed one of these forms.
Signature of the ELF is a condition of publication, and papers will not be passed to the publisher for production unless a signed form has been received. Please note that signature of the Exclusive Licence Form does not affect ownership of copyright in the material. After submission, authors will retain the right to publish their paper in various media/circumstances (please see the form for further details).
Production tracking is available for your article through Author Services Author Services enables authors to track their article, once it has been accepted, through the production process to publication online and in print. Authors can check the status of their articles online and choose to receive automated e-mails at key stages of production. The author will receive an e-mail with a unique link that enables them to register and have their article automatically added to the system. Authors can nominate up to 10 colleagues to have complimentary access to the article once published on line. Visit our Author Services site for more details on online production tracking, tips on article preparation and submission, and more.
Please ensure that a complete e-mail address is provided when submitting the manuscript. Visit our Author Services site for more details on online production tracking, tips on article preparation and submission, and more.
Handling the proofs The correspondence author will receive an e-mail alert when the proof, an Acrobat PDF (portable document format) file, can be downloaded from the e-proofing site. Acrobat Reader will be required in order to read this file. This software can be downloaded (free of charge) from the following web site: www.adobe.com/products/acrobat/readstep2.html
This will enable the file to be opened, read on screen, and printed out for any corrections to be added. Further instructions will be sent with the proofs. Proofs will be posted if no e-mail address is available; in your absence, please arrange for a colleague to access your e-mail to retrieve the proofs.
Alterations in the text, other than printers errors, may be charged to the author. Proofs must be returned by e-mail, first-class mail, or fax within 3 days of receipt to: Journal of Animal Ecology, Wiley-Blackwell John Wiley & Sons 9600 Garsington Road, Oxford OX4 2DQ, UK. Tel: +44 (0) 1865 476477 Fax: +44 (0) 1865 476772 E-mail: [email protected]
Foreign contributors might consider nominating someone in the UK to correct their proofs for them; they should do this when submitting their revised manuscript. The editors reserve the right to correct the proofs themselves, using the accepted version of 56
the manuscript, if the authors corrections are overdue and the journal would otherwise be delayed.
Early View publication Journal of Animal Ecology is covered by the Early View service. Early View articles are complete, full-text articles published online in advance of their publication in a printed issue. Articles are therefore available as soon as they are ready, rather than having to wait for the next scheduled print issue. They have been fully reviewed, revised and edited for publication, and the authors' final corrections have been incorporated. To register to receive an e-mail alert when your Early View article is published, click here and log-in to Wiley Online Library.
Because Early View articles are in their final, complete form, no changes can be made after online publication. Articles are given a Digital Object Identifier (DOI), which allows them to be cited and tracked before allocation to an issue. After print publication, the DOI remains valid and can continue to be used to cite and access the article. More information about DOIs can be found at http://www.doi.org/faq.html
OnlineOpen OnlineOpen is available to authors of primary research articles who wish to make their article available to non-subscribers on publication, or whose funding agency requires grantees to archive the final version of their article. With OnlineOpen, the author, the author's funding agency, or the author's institution pays a fee to ensure that the article is made available to non-subscribers upon publication via Wiley Online Library, as well as deposited in the funding agency's preferred archive. For the full list of terms and conditions, click here.
Any authors wishing to send their paper OnlineOpen will be required to complete the payment form.
Prior to acceptance there is no requirement to inform an Editorial Office that you intend to publish your paper OnlineOpen if you do not wish to. All OnlineOpen articles are treated in the same way as any other article. They go through the journal's standard peer-review process and will be accepted or rejected based on their own merit.
Offprints The corresponding author will receive a PDF file of their article free of charge at the time of publication within an issue of the journal (i.e. once the article is paginated). Printed offprints are normally dispatched by surface mail c.3 weeks after publication of the issue in which the paper appears; however, please note that they are sent by surface mail so delivery of overseas orders may take up to 6 weeks. Please contact the publishers if they fail to arrive.
The PDF file is e-mailed to the correspondence author at the e-mail address given on the title page of the paper (unless advised otherwise); therefore, please ensure that the name, address and e-mail of the correspondence author are clearly indicated on the manuscript title page if he/she is not the first author of the paper. A copy of the Publisher's Terms and Conditions for the use of the PDF file will accompany it and the file can only be distributed in accordance with these requirements. Authors can also 57
nominate up to 10 colleagues to receive complimentary access to their article by registering for Author Services.
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