UNIVERSIDADE FEDERAL DO CEARÁ CENTRO DE CIÊNCIAS
DEPARTAMENTO DE BIOLOGIA
PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA E RECURSOS NATURAIS
DJAN ZANCHI DA SILVA
EVIDÊNCIAS DE VARIAÇÃO INTERINDIVIDUAL NA DIETA DE Ameivula ocellifera (SQUAMATA: TEIIDAE) DEVIDO A PADRÕES DE ANINHAMENTO DE
PARTIÇÃO DE RECURSOS ENTRE OS INDIVÍDUOS
FORTALEZA 2020
DJAN ZANCHI DA SILVA
EVIDÊNCIAS DE VARIAÇÃO INTERINDIVIDUAL NA DIETA DE Ameivula ocellifera (SQUAMATA: TEIIDAE) DEVIDO A PADRÕES DE ANINHAMENTO DE PARTIÇÃO DE
RECURSOS ENTRE OS INDIVÍDUOS
Tese apresentada ao Programa de Pós-Graduação em Ecologia e Recursos Naturais da Universidade Federal do Ceará, como requisito parcial à obtenção do título de Doutor em Ecologia. Área de concentração: Ecologia e Recursos Naturais.
Orientador: Profa. Dra. Diva Maria Borges-Nojosa.
Coorientadores: Prof. Dr. Marcelo Zacharias Moreira.
Dra. Raquel Susana Brazão Xavier.
FORTALEZA 2020
DJAN ZANCHI DA SILVA
EVIDÊNCIAS DE VARIAÇÃO INTERINDIVIDUAL NA DIETA DE Ameivula ocellifera (SQUAMATA: TEIIDAE) DEVIDO A PADRÕES DE ANINHAMENTO DE PARTIÇÃO DE
RECURSOS ENTRE OS INDIVÍDUOS
Tese apresentada ao Programa de Pós-Graduação em Ecologia e Recursos Naturais da Universidade Federal do Ceará, como requisito parcial à obtenção do título de Doutor em Ecologia. Área de concentração: Ecologia e Recursos Naturais.
Aprovada em: 28/08/2017.
BANCA EXAMINADORA
________________________________________ Profa. Dra. Diva Maria Borges-Nojosa (Orientadora)
Universidade Federal do Ceará (UFC)
_________________________________________ Profa. Dra. Carla Ferreira Rezende
Universidade Federal do Ceará (UFC)
_________________________________________ Prof. Dr. Paulo Cascon
Universidade Federal do Ceará (UFC)
_________________________________________ Prof. Dr. David James Harris
Universidade do Porto
_________________________________________ Prof. Dr. Daniel Mesquita
AGRADECIMENTOS
A minha querida esposa, Marcela Costa da Silva, por todo o amor, companheirismo, paciência, apoio, e tanto outros fatores que contribuíram para o meu ingresso no doutorado e possibilitaram o desenvolvimento deste estudo.
Aos meus Pais, aos meus sobrinhos e aos meus irmãos, por tudo que representam para mim.
À Profa. Dra. Diva Maria Borges-Nojosa, que dentre os agradecimentos que devo, destaco a oportunidade de realização deste estudo, a confiança depositada em mim e o apoio emocional nos momentos mais difíceis.
Ao Dr. James Harris, pela oportunidade de estágio no Centro de Investigação em Biodiversidade da Universidade do Porto, além do exemplo de seriedade e dedicação profissional.
À Dra. Raquel Xavier, pela seriedade, dedicação e exemplo profissional.
A todos os meus amigos e colegas do Núcleo Regional de Ofiologia da Universidade Federal do Ceará (NUROF-UFC), por toda a ajuda, pelo companheirismo, e pelo apoio e força ao longo desse processo tortuoso.
Aos meus amigos do NUROF-UFC, Ítalo Hipólito, Gabriel Aguiar, Raul Vasconcelos, Luan Tavares Pinheiro e John pela ajuda nas coletas de campo.
Às minhas amigas e colegas de NUROF-UFC, Castiele Holanda Bezerra e Roberta Rocha, pela amizade e apoio e grande contribuição no esforço de bancada.
Ao meu colega de laboratório Lucas Araújo, por sua colaboração nos esforços de bancada.
Ao Sr. Borges, proprietário da Fazenda Maceió, e à Dona Miriam, proprietária do Sítio Eliezer, por permitirem que a amostragem dos lagartos fosse realizada em suas propriedades.
A Sra. Maria Monteiro da Silva e ao Sr. Francisco José Monteiro da Silva, por permitirem que a amostragem dos lagartos fosse realizada na Localidade Pedras, em Aracati-CE.
À Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico – FUNCAP, pela bolsa de estudos ao longo do doutorado, e ao Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq, pela bolsa de doutorado-sanduíche.
“Não tá morto quem peleia!” (Ditado Popular Gaúcho)
RESUMO
A especialização individual na dieta (EID) de Ameivula ocellifera (Spix, 1825) foi avaliada em três estudos no estado do Ceará. No primeiro, a EID, os padrões de usos de recursos e a topologia das redes tróficas de jovens, machos e fêmeas foram avaliadas em habitat litorâneo. O grau de variação na dieta dos indivíduos e os graus de aninhamento e de “clustering” foram avaliados por abordagem baseada na teoria de redes. Houve nível elevado de variação interindividual na dieta dos três grupos, que parecem relacionados a padrões aninhados de uso de recursos para machos e fêmeas. Os resultados se adequam ao Modelo das Preferências Compartilhadas, onde indivíduos consomem as mesmas presas ótimas quando os recursos alimentares são abundantes, substituindo-os por itens sub-ótimos quando aqueles se tornam escassos no ambiente. O segundo estudo testou a previsão de MacArthur e Pianka (1966) de que forrageadores ativos mantêm os hábitos alimentares mesmo quando os recursos alimentares são escassos. A dieta de A. ocellifera foi avaliada quanto a variações entre os períodos seco e chuvoso em dois habitats e entre os habitats nos dois períodos climáticos. Houve variação sazonal na abundância das presas em um dos habitats e no volume das presas no outro, além de variação na abundância de presas consumidas entre as duas áreas no período seco. Ameivula ocellifera agiu como especialista em um dos habitats e como generalista no outro, demonstrando que sua dieta parece estar mais relacionada à variação na disponibilidade de presas. Os resultados suportam a previsão de MacArthur e Pianka (1966) de que uma exceção à sua teoria poderia ocorrer em espécies forrageadoras ativas.No terceiro estudo, a dieta de A. ocellifera foi reanalisada para testar se padrões de partição de recursos previamente descritos ocorrem em outros habitats. A EID, os padrões de uso de recursos e a topologia das redes tróficas foram avaliadas por abordagem baseada na teoria de redes. Houve evidências de EID nos dois habitats, além de padrões aninhados de uso de recursos. O nível de EID foi maior no período chuvoso, enquanto que o aninhamento foi maior no período seco. A maioria dos resultados confirma o estudo anterior, além de evidenciar que os padrões de especialização na dieta e o uso de recursos de indivíduos podem variar em populações distintas de habitats similares, o que reforça a relevância de utilizar abordagens baseadas em redes para avaliar a autoecologia das espécies em nível individual.
Palavras-chave: Lagarto neotropical. Variação interindividual. Dieta aninhada. Caatinga. Brasil.
ABSTRACT
Individual specialization in the diet (ISD) of Ameivula ocellifera (Spix, 1825) was evaluated in three studies in the state of Ceará. In the first, the EID, the patterns of resource use and the topology of the trophic networks of juveniles, males and females were evaluated in a coastal habitat. The degree of variation in the diet of individuals and the degree of nestedness and clustering were assessed using a network-based approach. There was a high level of inter-individual variation in the diet of the three groups, which seem to be related to nested patterns of resource use for males and females. The results fits to the Shared Preferences Model, where individuals consume the same optimal prey when food resources are abundant, replacing them by sub-optimal items when those become scarce in the environment. The second study tested MacArthur and Pianka's (1966) prediction that active foragers maintain food habits even when food resources are scarce. The diet of A. ocellifera was evaluated for variations between the dry and rainy periods in two habitats and between the habitats in the two climatic periods. There was seasonal variation in prey abundance in one habitat and in prey volume in the other, in addition to variation in prey abundance consumed between the two areas in the dry period. Ameivula ocellifera acted as a specialist in one habitat and as a generalist in the other, demonstrating that its diet seems to be more related to variation in prey availability. The results support MacArthur and Pianka's (1966) prediction that an exception to their theory could occur in active forager species. In the third study, the diet of A. ocellifera was re-analyzed to test whether previously described resource partition patterns occur in other habitats. ISD, resource use patterns and the topology of trophic networks were assessed using a network-based approach. There was evidence of ISD in both habitats, as well as nested resource use patterns. The level of ISD was higher in the rainy period, while nestedness was higher in the dry period. Most of the results confirm the previous study, in addition to showing that patterns of specialization in the diet and resources use by individuals may vary in different populations of similar habitats, which reinforces the relevance of using network-based approaches to assess the autoecology of species at the individual level.
SUMÁRIO
1 INTRODUÇÃO ... 14
2 CAPÍTULO 1 - MANUSCRITO: “PATTERNS OF DIET COMPOSITION OF A WHIPTAIL LIZARD SPECIES CONFORMS TO THE SHARED PREFERENCES MODEL OF INTERINDIVIDUAL VARIATION IN PREY CONSUMPTION”. ... 19
2.1 Introduction ... 20
2.2 Material and Methods ... 23
2.2.1 Study Area ... 23
2.2.2 Sampling Procedures ... 23
2.3 Results ... 26
2.4 Discussion ... 27
2.5 Acknowledgements ... 32
3 CAPÍTULO 2 - MANUSCRITO: “DISTINCT DIETARY PATTERNS FOR A WHIPTAIL LIZARD (AMEIVULA OCELLIFERA, TEIIDAE) IN COASTAL AND CAATINGA HABITATS IN NORTH EAST BRAZIL”. ... 46 3.1 Introduction ... 47 3.2 Methods ... 49 3.2.1 Study Areas ... 49 3.2.2 Procedures ... 50 3.3 Results ... 52 3.4 Discussion ... 55 3.5 Acknowledgements ... 60
4 CAPÍTULO 3 - MANUSCRITO: “PATTERNS OF RESOURCES USE PARTITION AMONG AMEIVULA OCELLIFERA (SPIX, 1825) (SQUAMATA, TEIIDAE) INDIVIDUALS IN A COASTAL AND IN A CAATINGA HABITATS AT NORTHEASTERN BRAZIL”. ... 69
4.1 Introduction ... 71
4.2 Material and Methods ... 73
4.2.1 Study Areas ... 73
4.2.3 Dietary Analysis and Network-based Approaches ... 75 4.3 Results ... 77 4.4 Discussion ... 79 4.5 Acknowledgements ... 84 5 CONCLUSÃO ... 94 REFERÊNCIAS ... 97
APÊNDICE A – LISTA DE FIGURAS ... 104
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1 INTRODUÇÃO
Tradicionalmente na ecologia, estudos de uso de recursos e de dinâmica das populações consideram indivíduos coespecíficos como ecologicamente equivalentes, ignorando processos ecológicos que ocorrem em nível individual, como a especialização individual na dieta (EID) (BOLNICK et al., 2003).
Entretanto, atualmente é possível avaliar se espécies distintas que ocorrem em um mesmo habitat ou populações de uma mesma espécie de habitats diferentes divergem quanto aos níveis de EID, através da utilização de índices que permitem mensurar esses níveis de variação (BOLNICK et al., 2002; ARAÚJO et al., 2010). Adicionalmente, abordagens baseadas na Teoria de Redes têm sido eficazes para descrever a topologia das redes tróficas dos indivíduos e os padrões de partição de recursos entre eles, que podem ser responsáveis pela ocorrência de EID (p.ex., ARAÚJO et al., 2010; PIRES et al., 2011; TINKER et al., 2012). Com isso as descrições dos sistemas biológicos se tornam mais completas e permitem que ocorra uma transição de modelos fenomenológicos de dinâmica das populações para modelos mecanicistas nos quais as dinâmicas são preditas pelas propriedades dos seus componentes (SVANBÄCK; BOLNICK, 2008).
Ameivula ocellifera (Spix, 1825) é um lagarto neotropical amplamente encontrado em formações abertas da América do Sul, do nordeste do Brasil até a Bolívia (VANZOLINI et al., 1980). É uma espécie tipicamente forrageadora ativa (PIANKA; VITT, 2003), que percorre o ambiente em busca de presas que são localizadas através de pistas visuais e químicas (VITT; CALDWELL, 2014). No Brasil, ocorre em formações vegetais abertas da Caatinga (VITT, 1983; VITT, 1995; MENEZES et al., 2011) e de restingas costeiras da Mata Atlântica (SANTANA et al., 2010). Estudos anteriores demonstram que a espécie apresenta algum conservadorismo na sua dieta, devido ao elevado consumo de isópteros e/ou larvas de insetos em ambientes variados (p.ex., DIAS; ROCHA, 2007; MENEZES et al., 2011; SALES et al.,
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2012, SALES; FREIRE, 2015).
A autoecologia de A. ocellifera é relativamente bem estudada, sobretudo no que diz respeito à dieta de suas populações em ambientes variados. Entretanto, grande parte destes estudos utilizou abordagens tradicionais para avaliar uso de recursos alimentares da espécie, com seu nicho alimentar sendo avaliado como uma propriedade das populações ou da espécie como um todo, e os indivíduos sendo considerados ecologicamente equivalentes. Entretanto, como “o nicho é uma propriedade emergente dos fenótipos individuais, e, portanto, deve ser definido ao nível individual” (BOLNICK et al., 2010), há carência de estudos que permitam identificar os padrões de partição de recursos entre os indivíduos que podem levar à ocorrência de EID em populações de A. ocellifera.
Em virtude disso, na presente tese, intitulada “Evidências de Variação Interindividual na Dieta de Ameivula Ocellifera (Squamata: Teiidae) devido a Padrões de Aninhamento de Partição de Recursos entre os Indivíduos”, serão apresentados três estudos que utilizam abordagens tradicionais e recentes para avaliar o uso de recursos alimentares em nível populacional e a partição de recursos em nível individual. Estes estudos foram realizados com três populações de A. ocellifera em dois habitats litorâneos e um habitat de Caatinga no estado do Ceará, nordeste do Brasil. Os mesmos foram redigidos nos formatos exigidos pelos periódicos científicos aos quais já foram publicados ou a que serão submetidos.
No primeiro manuscrito, intitulado “Patterns of diet composition of a whiptail lizard species conforms to the Shared Preferences Model of interindividual variation in prey consumption”, analisou-se a variação interindividual nas refeições, os padrões de uso de recursos e a topologia das redes tróficas de uma população da espécie em São Gonçalo do Amarante, litoral oeste do estado do Ceará. Trata-se do primeiro estudo que utiliza redes tróficas para identificar os padrões de partição de recursos entre indivíduos da espécie, os
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quais podem levar à ocorrência de variação interindividual nas refeições de jovens, machos e fêmeas em um habitat sazonal tropical.
No segundo manuscrito, denominado “Distinct dietary patterns for a whiptail lizard (Ameivula ocellifera, Teiidae) in coastal and Caatinga habitats in North East Brazil”, dados de dieta de duas populações da espécie foram utilizados para testar a predição derivada da Teoria do Forrageio Ótimo de que forrageadores ativos podem manter seus hábitos alimentares mesmo quando os recursos alimentares são escassos (MacARTHUR; PIANKA, 1966). Avaliou-se ainda, a composição das refeições das duas populações, a ocorrência de variação sasonal nas refeições em ambos os habitats e variações entre as refeições dos dois habitats na mesma estação climática.
O terceiro manuscrito, nomeado “Patterns of resources use partition among Ameivula ocellifera (Spix, 1825) (Squamata, Teiidae) individuals in a coastal and in a Caatinga habitats at northeastern Brazil”, avalia se padrões de partição de recursos em nível individual, que foram previamente identificados para a espécie, são encontrados em populações de habitats distintos. Adicionalmente, avalia-se se esses padrões levam a ocorrência de variação entre as refeições dos indivíduos nas populações estudadas.
REFERÊNCIAS
ARAÚJO, M. S.; MARTINS, E. G.; CRUZ, L. D.; FERNANDES, F. R.; LINHARES, A. X.; REIS, S. F.; GUIMARÃES, P. R. Nested diets: a novel pattern of individual-level resource use. Oikos, v. 119, p. 81-88, 2010.
BOLNICK, D. I.; YANG, L. H.; FORDYCE, J. A.; DAVIS, J. M.; SVANBӒCK, R. Measuring individual-level resource specialization. Ecology, v. 83, p. 2936-2941, 2002. BOLNICK, D. I.; SVANBÄCK, R.; FORDYCE, J. A.; YANG, L. H.; DAVIS, J. M.; HULSEY, C. D.; FORISTER, M. L. The ecology of individuals: incidence and implications of individual specialization. The American Naturalist, v. 161, n. 1, p. 1-28, 2003.
BOLNICK, D. I.; INGRAM, T.; STUTZ, W. E.; SNOWBERG, L. K.; LAU, O. L.; PAULL, J. S. Ecological release from interspecific competition leads to decoupled changes in
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population and individual niche width. Proceedings of the Royal Society of London B: Biological Science, v. 277, p. 1789-1797, 2010.
DIAS, E. J. R.; ROCHA, C. F. D. Niche differences between two sympatric whiptail lizards (Cnemidophorus abaetensis and C. ocellifer, Teiidae) in the restinga habitat of northeastern Brazil. Brazilian Journal of Biology, v. 67, n. 1, p. 41-46, 2007.
MacARTHUR, R. H.; PIANKA, E. R. On optimal use of a patchy environment. The American Naturalist, v. 100, n. 916, p. 603-609, 1966.
MENEZES, V. A.; VAN SLUYS, M.; FONTES, A. F.; ROCHA, C. F. D. Living in a caatinga-rocky field transitional habitat: ecological aspects of the whiptail lizard
Cnemidophorus ocellifer (Teiidae) in northeastern Brazil. Zoologia, v. 28, p. 8-16, 2011. PIANKA, E. R.; VITT, L. J. From racerunners to night lizards. In: PIANKA, E. R.; VITT, L. J. (Ed.). Lizards – Windows to the Evolution of Diversity. The University of California Press, 2003, p. 195-201.
PIRES, M. M.; GUIMARÃES, P. R.; ARAÚJO, M. S.; GIARETTA, A. A.; COSTA, J. C. L.; REIS, S. F. The nested assembly of individual-resource networks. Journal of Animal
Ecology, v. 80, p. 896-903, 2011.
SALES, R. F. D.; RIBEIRO, L. B.; JORGE, J. S.; FREIRE, E. M. X. Feeding habits and predator-prey size relationships in the whiptail lizard Cnemidophorus ocellifer (Teiidae) in the semiarid region of Brazil. South American Journal of Herpetology, v. 7, n. 2, p. 149-156, 2012.
SALES, R. F. D.; FREIRE, E. M. X. Diet and foraging behavior of Ameivula ocellifera (Squamata: Teiidae) in the Brazilian semiarid caatinga. Journal of Herpetology, v. 49, n. 4, p. 579-585, 2015.
SANTANA, G. G.; VASCONCELLOS, A.; GADELHA, Y. E. A.; VIEIRA, W. L. S.;
ALMEIDA, W. O.; NÓBREGA, R. P.; ALVES, R. R. N. Feeding habits, sexual dimorphism and size at maturity of the lizard Cnemidophorus ocellifer (Spix, 1825) (Teiidae) in a
reforested restinga habitat in northeastern Brazil. Brazilian Journal of Biology, v. 70, p. 409-416, 2010.
SVANBÄCK, R.; BOLNICK, D. I. Food specialization. In: JØRGENSEN, S. V.; FATH, B. D. (Ed.). Behavioral Ecology, v. 2, Encyclopedia of Ecology. Elsevier, 2008, p. 1636-1642. TINKER, M. T.; GUIMARÃES JR, P. R.; NOVAK, M.; MARQUITTI, F. M. D.; BODKIN, J. L.; STAEDLER, M.; BENTALL, G.; ESTES, J. A. Structure and mechanism of diet specialization: testing models of individual variation in resource use with sea otters. Ecology Letters, v. 15, p. 475-483, 2012.
VANZOLINI, Paulo Emílio; RAMOS-COSTA, Ana Maria M.; VITT, Laurie J. Répteis das Caatingas. Rio de Janeiro: Academia Brasileira de Ciências, 1980.
VITT, L. J. Reproduction and sexual dimorphism in the tropical teiid lizard Cnemidophorus ocellifer. Copeia, v. 1983, p. 359-366, 1983.
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VITT, L. J. The ecology of tropical lizards in the caatinga of northeast Brazil. Occasional Pappers of the Oklahoma Museum of Natural History, v. 1, p. 1-29, 1995.
VITT, Laurie J.; CALDWELL, Janalee. P. Herpetology - An Introductory Biology of Amphibians and Reptiles. 4. ed. London: Academic Press, 2014.
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CAPÍTULO 1
MANUSCRITO: “Patterns of diet composition of a whiptail lizard species conforms to the Shared Preferences Model of interindividual variation in prey consumption”.
(Publicado online em Amphibia-Reptilia, disponível em https://doi.org/10.1163/15685381-bja10023)
Djan Zanchi-Silva 1,2, Conrado Galdino 3, Diva Borges-Nojosa 1,2
1) Núcleo Regional de Ofiologia da Universidade Federal do Ceará (NUROF-UFC), Universidade Federal do
Ceará, Campus do Pici, Bloco 905, CEP 60440-554, Fortaleza, Ceará, Brazil
2) Programa de Pós-graduação em Ecologia e Recursos Naturais, Universidade Federal do Ceará, Campus do
Pici, Centro de Ciências, Bloco 902, CEP 60440-554, Fortaleza, Ceará, Brazil
3) Programa de Pós-graduação em Biologia de Vertebrados, Pontifícia Universidade Católica de Minas Gerais,
Avenida Dom José Gaspar, 290, Bairro Coração Eucarístico, CEP 30535-901, Belo Horizonte, Minas Gerais, Brazil
Corresponding author: DJAN ZANCHI DA SILVA, e-mail: djanzanchi@gmail.com
Type of Manuscript: Article. Number of Words: 7378.
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Abstract. We analysed the interindividual variation in diet, patterns of food resource use and topology of the trophic networks of juvenile, male, and female Ameivula ocellifera (Spix, 1825) during one year, covering wet and dry seasons. Using a network-based approach, we evaluated the degree of variation in the diet of individuals, and the degree of nestedness and clustering to identify patterns of resource use and the topology of individuals food webs. We found a high degree of interindividual variation in the diet of juveniles, males, and females during the study period, which seems to be related to nested patterns of resource use of males and females. These results also suggest that males and females seem to have both generalist and specialist individuals, of which the diets of specialists are nested within the diets of generalists. For juveniles, we found evidence of interindividual variation in diet in both seasons, although patterns of food resource partition that may cause it could not be identified. Insect larvae of several groups were the main food resource in all three lizard groups during the wet season, while termites were the dominant food item during the dry season. Our results conform to the Shared Preferences Model where individuals should consume the same top-ranked prey when they are abundant in the environment, replacing it with suboptimal items as preferred ones become scarce.
Keywords: neotropical lizard, interindividual variation, nested diet, Caatinga, Brazil.
Introduction
Individual specialization in diet (ISD) happens when food resources consumed by individuals are subsets of the total food item spectrum consumed by populations. Therefore, ISD is interindividual differences in diet composition (e.g., Rosa et al., 2011; Sales, Ribeiro and Freire, 2011; Pitilin, Araújo and Buschini, 2012), which occur in several animal species (Bolnick et al., 2003; Araújo, Bolnick and Layman, 2011). Three models were proposed to
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explain ISD: The Competitive Refuge Model, the Distinct Preferences Model, and the Shared Preferences Model (Svanbäck and Bolnick, 2005). The Competitive Refuge Model predicts that individuals will share the same top-ranked resources, differing in the consumption of alternative prey. Thereby, as preferred prey become scarce, individuals shift to alternative resources, reducing dietary overlap and increasing clustering among diets. Conversely, the Distinct Preferences Model predicts that individuals will differ in preferences for optimal prey, and as it becomes scarce, new ones will be added to the diet. This will lead to an increase in diet overlap among individuals, thereby increasing clustering. Alternatively, according to the Shared Preferences Model, all individuals have similarities in the preferred prey, although they differ in the acceptance of suboptimal prey, leading to nested diets, as the diets of the most selective individuals become a subset of the diet of the next most
opportunistic individuals (Pires et al., 2011).
Nonetheless, to evaluate individual specialization in diet it is necessary to have temporal consistency in the record of prey consumption by individuals. This, in turn, can only be
obtained by systematic samplings over time, which requires the observation of many events of prey-capture by each sampled individual. The inherent difficulty to sample feeding behaviour over time has led researchers to use other methods to obtain data, such as the evaluation of scat contents, regurgitation, or even the use of isotope analysis (Bolnick et al., 2002).
Evaluation of ISD in populations of small-sized ectotherms that are highly mobile and forage over large areas can be challenging. Therefore, the use of alternative approaches can shed light on ISD patterns for these species. Therefore, some studies analysed the stomach contents in order to address ISD in such species. As an example, Araújo et al. (2007) and Rosa et al. (2011) evaluated ISD in frogs by sampling their stomach contents, and Sales, Ribeiro and Freire (2011) used the same approach to study diet specialization in the lizard Ameiva ameiva (Linnaeus, 1758).
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Indeed, there are few studies addressing the ISD of lizards. Costa et al. (2008) found evidence of niche expansion in depauperate communities of lizards in the Brazilian Cerrado, due to an increase in within-individual variation. Therefore, dietary niche breadths of lizard species varied because the diets of individuals were composed according to their preferences for distinct preys. More recently, Sales, Ribeiro, and Freire (2011) studied the diet of Ameiva ameiva in a Caatinga habitat in north-eastern Brazil and found ISD between the dry and wet seasons. However, none of these studies on lizards were able to understand why individuals have specialization in their diets, and thus share food resources. Moreover, many ecological traits of lizards are affected by age and sex of individuals. For instance, ontogenetic variation was evidenced regarding body temperatures of Lioalemus lutzae (Mertens, 1938) in a
“restinga” habitat at southeastern Brazil, when juveniles had hotter bodies than adults, likely because they were excluded from areas with better thermal regimes by adults (Maia-Carneiro and Rocha, 2013). Similarly, juveniles and adults of Phrynosoma douglasii (Bell, 1829) differed regarding composition and size of prey consumed, which was attributed to distinct energetic allocation between age classes (Lahti and Beck, 2008). Regarding sexual variation, males of both Autarchoglossa and Iguania clades have larger home ranges than females, likely due to a higher “cost of reproduction” for males (Perry and Garland JR., 2002); another example are females of Ameivula ocellifera in a “restinga” habitat at northeastern Brazil, which become sexually mature with smaller body sizes than males, which may increase their reproductive success throughout lifetime (Santana et al., 2010). As seen, age and sex of lizards may affect several aspects of their ecology, therefore, one can expect that the underlying process leading to ISD can differ between sexes, and also between adults and juveniles (Silva and Araújo, 2008).
The whiptail lizard Ameivula ocellifera is a widespread species inhabiting open South American habitats (Harvey, Ugueto and Gutberlet Jr., 2012). These lizards actively search for
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prey over large areas (Pianka and Vitt, 2003). The diet of A. ocellifera is similar among populations, as the results of different studies have found a predominant consumption of termites (e.g., Dias and Rocha, 2007; Menezes et al., 2011) and insect larvae (e.g., Sales et al., 2012; Sales and Freire, 2015). As termites and insect larvae are the predominant prey in the diet of A. ocellifera, we predicted that the Shared Preferences Model would explain patterns of individual prey consumption for this species (Svanbäck and Bolnick, 2005). In addition, as not all individuals had necessarily consumed the same prey items, one should predict a nested pattern of diets leading to ISD (Pires et al., 2011).
Here, we used the digestive tract (stomachs and small and large intestines) of Ameivula ocellifera to evaluate interindividual variation in diet. Specifically, we asked if patterns of food item composition varied among ages and sexes. We also tested whether the observed patterns of food partition of individuals match the Shared Preferences Model as expected.
Material and Methods Study Area
Fieldwork was conducted in two study areas (3º30’49.49”S, 38º55’12.69”W; WGS84 and 3º33’54.80”S, 8º55’15.10”W; WGS84) at São Gonçalo do Amarante, Ceará, northeastern Brazil. The studied sites were open areas comprised of typical littoral zone formations, dominated by pasture and crops, with a few remnants of original vegetation, which, in turn, is characterised by arboreal vegetation covering the edge behind the coastal strip of dunes (see details in Nogueira et al., 2005). The climate of the region is tropical hot and semi-arid (Ipece, 2017). Rains occur from February to June, with most rainfall concentrated in April.
Sampling Procedures
Lizards were sampled monthly from September/2009 to August/2010, in trips of two to four days each. During collections, we searched actively for specimens in the environment from sunrise until sunset, which were killed by shooting them with an air gun or with rubber bands (Franco, Auricchio and Salomão, 2002). Individuals that were only stunned by the rubber bands were immediately euthanized with an intraperitoneal or intracoelomic injection of lidocaine, following the guidelines of Avma (2013). Individuals were preserved in ethanol and
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deposited in the herpetological collection of the “Núcleo Regional de Ofiologia” of the “Universidade Federal do Ceará” (CHUFC-NUROF).
We evaluated the digestive tract of lizards (stomachs and small and large intestines), under a
stereomicroscope. Invertebrates were identified up to order. We recorded prey abundance (N) and frequency of occurrence (F). We estimated N by counting the number of each prey category in each digestive tract, while F was estimated by calculating the proportion of digestive tracts containing a given prey category.
We also assembled resource availability in the environment in the dry (December/2009) and wet seasons (May/2010). In each study area, we randomly sampled 32 points (16 points in the wet season, eight per study area; 16 points in the dry season, eight per study area). Each point corresponded to 4m2 (2m X 2m), bounded
with a 1m high canvas. We used the following methodologies to sample for prey availability: 1) specimens in lower vegetation were sampled with an insect net that was passed in each plant in three series of ten movements; 2) the lower vegetation was hit with a wood stick in three series of ten hits, and the falling arthropods were collected with a forceps from a tray positioned bellow the plant; 3) potential prey present in the soil and fallen leaves were collected with a forceps during searches of ten minutes (Kiefer, 1998). All specimens collected were euthanised with ethanol or ether solution and preserved in ethanol (Nakano et al., 2002), and were identified with a stereomicroscope up to order. We recorded the abundance of each taxa sampled and used its proportions to test for variation between prey offer and diet composition of A. ocellifera in both seasons, through Kolmogorov-Smirnov tests (Zar, 1999). We performed the Kolmogorov-Kolmogorov-Smirnov tests in R (R Core Team, 2016).
To test for the occurrence of interindividual variation in the diet of Ameivula ocellifera, we followed Araújo et al. (2009) and estimated ISD for juveniles, males, and females (hereafter termed as groups of individuals). We considered males as adults when their body size was larger than 43.39 mm, and adult females those larger than 51.46 mm, which were the smallest sizes of reproductive males and females of A. ocellifera at the study site, respectively (Zanchi-Silva, Borges-Nojosa and Galdino, 2014).
We selected best-fit models of food consumption for individuals by performing nestedness and clustering analyses of the diet for each group (Svanbäck and Bolnik, 2005). We used the abundance of each prey type consumed by individuals to depict its individual-resource networks separately for the dry and wet seasons, based on individual-resource matrices (R). The R matrices were used to build networks in which individual lizards and resources are depicted as a distinct set of nodes, as well as links connecting individual lizards to prey types they consumed (Pires et al., 2011; Tinker et al., 2012). Next, the R matrices were used to build incidence matrices (#R), where the element rij was 1 when prey item j was consumed by individual i, or zero otherwise (Bascompte
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et al., 2003). The R matrices were then used to evaluate the degree of individual specialization in the
consumption of prey and the structural patterns of clustering, while the #R matrices were used to investigate the
structural patterns of nestedness in diet consumption.
We estimated the degree of interindividual variation in diet composition using the E index based on a network approach (Araújo et al., 2008). E is analogous to earlier indexes to measure ISD, it has known statistical properties and is more intuitive, providing results easily interpreted (Araújo et al, 2008). The E index varies from 0 (no diet variation among individuals) to 1 (maximum diet variation among individuals) (Araújo et al., 2008). To obtain the respective estimate of the degree of interindividual variation in diet, we calculated E index for each group of individuals. We tested for the significance of empirical E values through bootstrap procedures in which the diets of individuals were compared to null distributions of E-values. Each individual was reassigned to the same number of prey items it had ingested, drawn randomly from the population diet distribution via
multinomial sampling. We calculated E for each null population (10,000 simulations) and rejected the null hypothesis if there was no variation in the diet when the observed value of E was larger than 95% of the simulated values (Araújo et al., 2008).
We also used the Cws index to evaluate whether the diet of individuals was clustered or continuous through
the niche axis (see Araújo et al., 2008, 2010). Cws was calculated for each group of individuals. This index varies
from – 1 (continuous diet variation) to + 1 (clustered diet variation) (Araújo et al., 2008). Otherwise, if Cws = 0,
there is no diet variation and individuals feed randomly from a given set of resources. Using the Cws index
combined with E allows the identification of patterns of prey consumption among individuals within populations (Araújo et al., 2008; Araújo et al., 2010). When both E and Cws tend to 0, there is no diet variation; however, if E
tends to + 1 and Cws to – 1, the variation in diet is continuous because individuals niches overlap little with each
other, and consequently, the diet is overdispersed due to the occurrence of generalist individuals in the
population. When both E and Cws tend to + 1, then the diet variation is discrete because individuals form discrete
dietary groups, resulting in a clustered diet of specialist individuals in the population; moreover, when E tends to 1 and Cws to 0, then there are both specialist and generalist individuals in the population, as the diets of the
specialists are an ordered and predictable subset from the diets of the generalists (Araújo et al., 2008; Araújo et al., 2010). We tested the significance of the observed Cws values through a bootstrap resampling procedure
similar to that applied to test the observed values of E (see above), using 10,000 simulations. As Cws can assume
both positive and negative values, we rejected the null hypothesis that individuals fed randomly from a shared resource distribution if Cws was positive and larger than 97.5% of its null values, or in the case of a negative Cws,
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if it was lower than 97.5% of the null values (Araújo et al., 2008).
Finally, in order to evaluate whether the diets of the most selective individuals represented subsets of the diets of the more generalist individuals, we used the NODF index (Almeida-Neto et al., 2008) to calculate the level of nestedness for each group of individuals for the dry and rainy seasons. NODF will tend to 100 when matrices are highly nested (total nestedness) and tend to zero when the diets of individuals are overdispersed or clustered (no nestedness in both). The values of nestedness will be between zero and 100 when matrices have random patterns of resource use. The NODF index is less prone to type-I errors than other metrics of nestedness of networks (Almeida-Neto et al., 2008). We tested the significance of empirical NODF values against null distributions. Nevertheless, nestedness may be generated by stochastic processes, for example when individuals are captured at distinct points during their activity period that differ in time spent foraging (Pires et al., 2011). It can also arise from individuals randomly sampling a set of unevenly distributed resources (Pires et al., 2011). Thereby, we used Null Model II as proposed by Bascompte et al. (2003) to generate 1000 simulations of trophic networks. We rejected the null hypothesis that a random replicate is equally or more nested than the observed matrix when the values of NODF were larger than 95% of theoretical values (Bascompte et al., 2003).
Bootstrap simulations of E and Cws were performed using the program DIETA 1.0 (Araújo et al., 2008).
NODF analyses and the respective bootstrap simulations were undertaken in ANINHADO 1.0 (Guimarães and Guimarães, 2006). Networks were drawn in Pajek (http://vlado.fmf.uni-lj.si/pub/networks/pajek/).
Results
We recorded 559 potential prey from 12 taxa in the wet season, and 78 from nine taxa in the dry season (Table 1). We did not find variation between prey offer in the environment and diet composition of Ameivula ocellifera in both wet (Dmax = 0.3500; P = 0.3172) and dry seasons
(Dmax = 0.5217; P = 0.0590).
Table 1
We found IDS for all groups of individuals from both seasons (Table 2). However,
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highest E values in the dry season. Males had higher diet specialization than females, regardless of the season (Table 2).
Nestedness was found for all groups of individuals, except for juveniles in the wet season (Table 2, Figure 1). We found a clustered pattern only for juveniles in the dry season (Table 2).
Table 2
Figure 1
Juveniles in the wet season consumed mainly insect larvae, insect pupae, Coleoptera, and Hemiptera, while the most frequent food items were Coleoptera, insect larvae, and Hemiptera (Table 3). In the dry season, juveniles fed mainly on Isoptera, Hemiptera, and insect larvae, and the most frequent food items were Hemiptera, insect larvae, and Araneae (Table 3).
In the wet season, males consumed mainly insect larvae, Coleoptera, and Araneae, while females fed more upon insect larvae, Araneae, Isoptera, and Coleoptera (Table 3). The most frequent food items for males and females from the wet season were insect larvae and Coleoptera, followed by Orthoptera and Araneae, respectively (Table 3). On the other hand, during the dry season, males consumed mainly Isoptera, insect larvae, and Hemiptera, and females fed more on Isoptera, Acari, and insect larvae (Table 3). The most common prey items for both males and females, were insect larvae, Coleoptera, and Hemiptera (Table 3).
Table 3 Discussion
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regardless of seasons. Arthropods were available to consumption in both seasons, with a predominance of insects, which in turn are the main food items consumed by lizards [e.g., Tropidurus torquatus (Wied-Neuwied, 1820), Carvalho et al., 2007; Ameiva edracantha (= Medopheos edracanthus) (Bocourt, 1874), Jordán and Amaya, 2011; Cnemidophorus ocellifer (= Ameivula ocellifera) and Tropidurus hispidus (Spix, 1825), Albuquerque et al., 2018]. As in most seasonal tropical environments, the abundance of insects in the studied site was higher during the rainy period (Vasconcellos et al., 2010). The patterns of food consumption by A. ocellifera were consistent with individual specialization in the diet. We are aware that the evaluation of diet from gut contents may lead to an overestimation of the degree of interindividual variation (Bolnick et al., 2002; Pires et al., 2011), as this sampling technique provides a snapshot of the long-term food intake pattern of individuals. The overestimation in ISD can be remarkable in cases where individuals can hold only a few prey items in their stomachs (Bolnick et al., 2002). However, A. ocellifera actively searches for food resources and may harbour a large number of prey items in their digestive tract (we found that it
harbours up to 563 prey items). Therefore, the stomach content of A. ocellifera can be a proxy of the long-term pattern of prey consumption. In addition, lower null E values support a strong pattern of individual specialization when gut content was used to estimate the pattern of food consumption (see Costa et al., 2008 and Sales, Ribeiro and Freire, 2011). Thus, we are confident that our results support the occurrence of ISD in the studied population as all of the simulated E values were less than the empirical one.
We found different patterns of variation in ISD between juveniles and adults. Juveniles had a higher degree of diet specialization in the wet season, while males and females had a higher ISD in the dry season. Moreover, males had a higher associated ISD than females regardless of the season. These findings show a variation in ISD both ontogenetically as sexually for Ameivula ocellifera.
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The greater specialization in diet of juveniles occurred in the wet season when the abundance of food resources was higher in the environment. Therefore, high selectiveness in the consumption of prey by A. ocellifera juveniles occurred in a period with abundant food supply. Insect larvae and pupae, Coleoptera, and Hemiptera predominated in the diet of juveniles during the wet season. The ingestion of high-quality food by juveniles is imperative in order to grow and develop to attain sexual maturity (e.g., Galán, 1999; Allan, Prelypchan and Gregory, 2006; Petermann, Koch and Gauthier, 2017). Therefore, consuming mainly insect larvae, a prey with high protein content, may improve growth of juveniles (e.g., Feng et al., 2017). Moreover, the necessity to consume prey that contributes to individual growth might lead juveniles to consume the abundant top-ranked prey, resulting in an interindividual overlap in the consumption of those items in both seasons. However, compared to adults, juveniles might have spatially restricted foraging areas as observed in Liolaemus lutzae (Rocha, 1999). As a consequence, they might be more affected by variation in prey
availability within their smaller home ranges as they are not able to compensate prey scarcity by moving over larger ranges. Hence, during the wet season, the increase in prey abundance might increase the chances of juveniles ingesting in a variety of non-top-ranked prey.
Conversely, during the dry season, juveniles consumed mainly termites, Hemiptera, and insect larvae. These types of food also have high amounts of proteins (Feng et al., 2017), and termites and insect larvae also show high water content (Nagy, Huey and Bennet, 1984; Cooper and Withers, 2004), which might be important in order to maintain a hydric balance during the dry season. Therefore, the seasonal changes that we found in the diet composition of juveniles might be related to a response to their high nutritional demands as prey
availability changes over time in response to variations in the amount of rains (e.g., Araújo et al., 2010; Vasconcellos et al., 2010). Additionally, due to the decreased prey availability during the dry season, juveniles might have a less diverse diet. Indeed, in the dry season,
30
Hemiptera were consumed by the majority of individuals, while in the wet season, the most consumed prey by juveniles was found in less than 50% of the stomachs. This, in turn, shows that the diets of juveniles were less variable during the period with low prey availability. Therefore, we suggest that the high ISD during the wet season might be related to the increased chances of individuals feeding on less common, non-top-ranked prey.
Adults showed a higher individual specialization in the dry season, with their pattern of food consumption varying between seasons. We relate this pattern to their higher energetic requirements to reproduce in association with their high foraging capacity. Ameivula
ocellifera reproduces continuously throughout the year, with a peak during the end of the wet season (Zanchi-Silva, Borges-Nojosa and Galdino, 2014). In the wet season at least half of males and females consumed insect larvae. Thereby, the associated costs of reproduction might increase the needs of ingestion of types of prey that provides suitable energy to maintain reproduction. This would lead to a reduction in the diversity of ingested items, leading to a reduction in the diet variability among individuals during the wetter months. We relate the high level of specialization in the diet of adults during the dry season as a response to the reduction in the abundance of highly energetic foods (top-ranked prey) during this period. In this case, individuals might increase the intake of less calorific prey types, due to a scarcity of the more calorific ones, resulting in increased variability of ingested prey among individuals. Although insect larvae, Coleoptera, and Hemiptera represent prey of high
nutritional value (e.g., Kouřimská and Adámková, 2016), and were the most occurrent prey in the diet of males in the dry season, less than half of males of A. ocellifera had consumed them. Termites, which may show high protein (e.g., Rumpold and Schlüter, 2015) and gross energy content (e.g., Adepoju and Omotayo, 2014), were the most abundant prey, but they were not among the most occurrent prey for males. For females, termites, Acari, and insect larvae were mainly consumed (ca. 84.5% of overall diet), with termites encompassing more
31
than half of overall diet. However, only ca. 20% of females had consumed these types of prey in the dry season. Thus, ISD for adults might be related to changes in prey ingestion due to decreased availability of top-ranked food types in the dry season.
The Shared Preferences Model states that individuals should consume the same top-ranked preys when they are abundant in the environment, and as the preferred prey becomes scarce, they are replaced by suboptimal items (Svanbäck and Bolnick, 2005). We found a high consumption of insect larvae in the wet season by individuals, while termites become the dominant food item during the dry season. The consumption of insect larvae and termites might have influenced ISD in Ameivula ocellifera. These insects were represented in the diets in both seasons, and many individuals should have consumed this prey as some sort of
“guarantee prey” when they were encountered in the environment, varying regarding to suboptimal items added to their diets, as predicted by the model.
In addition, we found a nested pattern in the diet of males and females for both seasons, which gives additional support to the Shared Preferences Model explaining ISD (Svanbäck and Bolnick, 2005). Nested patterns are expected to occur when a population is composed of both specialist and generalist individuals (Araújo et al., 2010), and the diets of the more specialized individuals are subsets of the diets of the generalist ones (Pires et al., 2011). Nevertheless, we were not able to identify the patterns of resource partition that may cause ISD in juveniles during the wet season, as there was neither evidence for a nested pattern nor a clustered diet, while both nested and clustered patterns occurred in the dry season.
Nonetheless, Araújo et al. (2010) had already warned that a mixture of situations might explain how ISD may occur in real populations.
Studies applying conventional approaches to evaluate the diets of Ameivula ocellifera in different environments considered all individuals as ecologically equivalent (Dias and Rocha 2007; Menezes et al., 2011; Sales et al. 2012; Sales and Freire, 2015). However, our results
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suggest that individuals of distinct age classes respond differently to variation of prey in a seasonal tropical habitat. We suggest that distinct life history demands between juveniles (growth) and adults (reproduction) might be related to the different patterns of ISD we found. Moreover, the generalist population of A. ocellifera might be formed from a set of generalist and also specialist individuals.
Acknowledgements. We thank F.M. Borges and M.M.M. Amaral for the permission they granted us to work on their properties, R. Xavier for the English review, D.C. Passos for help in field and lab procedures, C.H. Bezerra for help in lab procedures, L.T. Pinheiro for help with the figures, and M.C. Kiefer for her suggestions on the manuscript. For this study, D. Zanchi-Silva received a grant from Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico BMD-0008-00060.01.14/10 and from Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior (CAPES). C.A.B. Galdino benefited from a grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) proc. 35.0241/2008-2; Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico conv. 22/2007, and is currently receiving a grant 313341/2017-6 from CNPq. We also thank the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for the permit #21963-1 to collect the animals.
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Tables Legends
Table 1. Invertebrates collected in two study areas at São Gonçalo do Amarante, Ceará, Brazil, during the dry (December/2009) and wet seasons (May/2010).
Taxon Dry Season Wet Season ARACHNIDA Acari - 1 Araneae 7 41 HEXAPODA Blattodea 1 - Coleoptera 5 117 Diptera 14 38 Hemiptera 15 219 Hymenoptera - F. Formicidae 31 85 Isoptera 1 - Lepidoptera - 2 Mantodea 2 5 Neuroptera - 1 Odonata - 1 Orthoptera 2 46 MYRIAPODA Diplopoda - 3 Σ 78 559
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Table 2. The degree of diet variation (E), the clustering coefficient (Cws), and the nestedness
metric (NODF) in the diet of juveniles, males, and females of Ameivula ocellifera in the wet and dry seasons. p-values were obtained by Monte Carlo bootstraps (10.000 simulations for E and Cws, 1000 simulations for NODF). Values for E vary from 0 (no diet variation) to 1
(maximum diet variation); values for Cws vary from – 1 (overdispersed diets) to + 1 (clustered
diets); and values for NODF vary from 0 (no nestedness) to 100 (total nestedness).
Wet Season Dry Season
Group n E Cws NODF n E Cws NODF
Juveniles 25 0.7920*** 0.1213NS 39.34NS 70 0.7751*** -0.010* 43.39***
Males 99 0.7962*** 0.0554NS 37.06*** 72 0.8059*** 0.0351NS 32.89***
Females 63 0.7819*** 0.0449NS 40.48*** 44 0.7894*** 0.0158NS 40.06***
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Table 3. Diet composition as the percentage of the number (N%) and the frequency of occurrence (F%) of food items of juveniles (J), males (M), and females (F) of Ameivula ocellifera in the wet and dry seasons.
Wet Season Dry Season
J (n = 25) M (n = 99) F (n = 63) J (n = 70) M (n = 72) F (n = 44) Prey categories N (%) F (%) N (%) F (%) N (%) F (%) N (%) F (%) N (%) F (%) N (%) F (%) ANNELIDA Oligochaeta - - - 0.11 1.39 - - ARACHNIDA Acari 0.44 4.00 0.40 4.04 0.22 1.59 1.45 8.57 1.69 5.56 16.61 6.82 Araneae 8.37 28.00 5.85 26.26 11.09 33.33 7.66 42.86 6.21 26.39 0.78 20.45 Scorpionida - - - 0.07 2.27 CRUSTACEA Isopoda 1.32 4.00 3.02 6.06 4.13 7.94 - - - - 0.07 2.27 HEXAPODA Blattodea - - 1.55 14.14 4.57 15.87 0.29 2.86 0.45 5.56 0.78 9.09 Coleoptera 11.01 48.00 9.01 42.42 10.22 42.86 8.82 38.57 9.04 44.44 4.90 40.91 Dermaptera - - - 0.14 1.43 - - - - Diptera 4.85 8.00 5.31 11.11 3.48 11.11 0.43 4.29 0.23 2.78 0.50 6.82 Hemiptera 11.01 32.00 2.76 22.22 7.61 23.81 20.95 51.43 9.27 38.89 3.48 29.55 Hymenoptera - Apidae - - - - 0.22 1.59 - - - - Hymenoptera - Formicidae 3.08 16.00 4.57 26.26 4.13 17.46 2.89 11.43 2.03 12.5 1.42 11.36 Hymenoptera - Vespidae - - - 0.34 2.78 - - Isoptera 4.41 16.00 2.49 4.04 11.09 7.94 38.29 24.29 32.32 18.06 56.56 20.45 Lepidoptera - - 0.20 2.02 - - 0.29 2.86 - - - - Mantodea - - - - 0.65 1.59 0.29 2.86 0.45 5.56 0.14 4.55 Neuroptera - - - 0.14 1.43 - - - - Odonata - - 0.13 2.02 - - - - Orthoptera 1.32 12.00 4.17 32.32 5.87 31.75 1.01 8.57 2.26 19.44 0.99 22.73 Plecoptera - - 0.07 1.01 - - - - Insect larvae 35.24 36.00 56.52 54.55 25.00 50.79 11.42 48.57 30.06 47.22 11.21 61.36 Insect nymph 2.20 16.00 0.40 4.04 1.52 6.35 2.17 8.57 0.68 5.56 0.71 13.64 Insect pupae 14.98 12.00 0.81 7.07 5.00 3.17 - - 0.11 1.39 - - MOLLUSCA Gastropoda 0.44 4.00 1.34 9.09 1.30 6.35 0.29 2.86 1.36 12.5 0.35 11.36 MYRIAPODA Chilopoda - - 0.13 2.02 1.09 4.76 0.14 1.43 0.11 1.39 0.57 4.55 Diplopoda - - - 0.14 1.43 - - - - OTHERS Plant material - - 0.40 5.05 1.96 4.76 1.45 10.00 2.15 15.28 0.07 2.27 Vertebrata material - - 0.34 5.05 - - - - 0.11 1.39 0.07 2.27 NIA 1.32 12.00 0.54 8.08 0.87 6.35 1.73 12.86 1.02 12.5 0.71 18.18 Miscellaneous - - - - Σ 100.00 - 100.00 - 100.00 - 100.00 - 100.00 - 100.00 -
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Figure Legend
Figure 1. Individual-resource networks of juveniles (a), males (b), and females (c) of
Ameivula ocellifera in the wet and dry seasons at São Gonçalo do Amarante, Ceará, northeast Brazil, from September 2009 to August 2010. Links represent the consumption of a food resource (grey circles, on the right) by each individual (black circles, on the left).
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Figure Figure 1
44
Appendix. List of vouchers deposited in the collection:
L4341, L4342, L4343, L4344, L4345, L4346, L4347, L4348, L4349, L4350, L4351, L4352, L4353, L4354, L4355, L4356, L4357, L4358, L4359, L4360, L4361, L4362, L4363, L4364, L4365, L4366, L4367, L4368, L4369, L4370, L4371, L4372, L4373, L4374, L4375, L4376, L4377, L4378, L4379, L4380, L4381, L4382, L4383, L4384, L4385, L4386, L4387, L4388, L4389, L4390, L4391, L4392, L4393, L4394, L4395, L4396, L4397, L4398, L4399, L4400, L4401, L4402, L4403, L4404, L4405, L4406, L4407, L4408, L4409, L4410, L4411, L4412, L4413, L4414, L4415, L4416, L4417, L4418, L4419, L4420, L4421, L4422, L4423, L4424, L4425, L4426, L4427, L4428, L4429, L4430, L4431, L4432, L4433, L4434, L4435, L4436, L4437, L4438, L4439, L4440, L4441, L4442, L4443, L4444, L4445, L4446, L4447, L4448, L4449, L4450, L4451, L4452, L4453, L4454, L4455, L4456, L4457, L4458, L4459, L4460, L4461, L4462, L4463, L4464, L4465, L4466, L4467, L4468, L4469, L4470, L4471, L4472, L4473, L4474, L4475, L4476, L4477, L4478, L4479, L4480, L4481, L4482, L4483, L4484, L4485, L4486, L4487, L4488, L4489, L4490, L4491, L4492, L4493, L4494, L4495, L4496, L4497, L4498, L4499, L4500, L4501, L4502, L4503, L4504, L4505, L4506, L4507, L4508, L4519, L4520, L4521, L4522, L4523, L4524, L4525, L4526, L4527, L4528, L4529, L4530, L4531, L4532, L4533, L4534, L4535, L4536, L4537, L4538, L4539, L4540, L4541, L4542, L4543, L4544, L4545, L4546, L4547, L4548, L4549, L4550, L4551, L4552, L4553, L4554, L4555, L4556, L4557, L4558, L4559, L4560, L4561, L4562, L4563, L4564, L4565, L4566, L4567, L4568, L4569, L4570, L4571, L4572, L4573, L4574, L4575, L4576, L4577, L4578, L4579, L4580, L4581, L4582, L4583, L4584, L4585, L4586, L4587, L4588, L4589, L4590, L4591, L4592, L4593, L4594, L4595, L4596, L4597, L4598, L4599, L4600, L4601, L4602, L4603, L4604, L4605, L4606, L4607, L4608, L4609, L4610, L4611, L4612, L4613, L4614, L4615, L4616, L4617, L4618, L4619, L4620, L4621, L4622, L4623, L4624, L4625, L4626, L4627, L4628, L4629, L4630, L4631, L4632, L4633, L4634, L4635, L4636, L4637, L4638,
45 L4639, L4640, L4641, L4642, L4643, L4644, L4645, L4646, L4647, L4648, L4649, L4650, L4651, L4652, L4653, L4654, L4655, L4656, L4657, L4658, L4659, L4660, L4661, L4662, L4663, L4664, L4665, L4666, L4667, L4668, L4669, L4670, L4671, L4695, L4696, L4697, L4698, L4699, L4700, L4701, L4702, L4703, L4704, L4705, L4706, L4707, L4713, L4714, L4715, L4725, L4726, L4727, L4728, L4729, L4730, L4731, L4732, L4733, L4734, L4735, L4736, L4737, L4738, L4739, L4740, L4741, L4742, L4743, L4744, L4745, L4746, L4747, L4748, L4749, L4750, L4751, L4752, L4753, L4754, L4755, L4756, L4757, L4758, L4759, L4760, L4761, L4762, L4763, L4764, L4765, L4766, L4767, L4768, L4769, L4770, L4771, L4772.
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CAPÍTULO 2
MANUSCRITO: “Distinct dietary patterns for a whiptail lizard (Ameivula ocellifera, Teiidae) in coastal and Caatinga habitats in North East Brazil”.
(A ser submetido ao Periódico “Journal of Tropical Ecology”, portanto, segue suas regras de formatação)
Djan Zanchi-Silva1,2,3, Luan Tavares Pinheiro1 and Diva Maria Borges-Nojosa1,2
1 Núcleo Regional de Ofiologia da Universidade Federal do Ceará (NUROF-UFC),
Universidade Federal do Ceará, Campus do Pici, Bloco 905, CEP 60440-554, Fortaleza, Ceará, Brazil
2 Programa de Pós-graduação em Ecologia e Recursos Naturais, Universidade Federal do
Ceará, Campus do Pici, Centro de Ciências, Bloco 902, CEP 60440-554, Fortaleza, Ceará, Brazil
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Abstract: We studied the diet of Ameivula ocellifera in two habitats in North East Brazil to test the derivative prediction of MacArthur and Pianka (1966) that active foragers may maintain dietary habits even when food resources are scarce. We collected lizards in dry and wet periods and analysed prey abundance, volume, frequency of occurrence and the
importance value index. We tested for variation in diet between dry and wet periods in both habitats, and for variation in the diet between the habitats in both climate periods. We found seasonal variation in the abundance in one locality and the volume of the prey item in the other, and variation in the abundance of prey consumed between the two localities during the dry period. In one locality, A. ocellifera behaved as a specialist species, mainly due to the high consumption of termites; in the other locality, the individuals were more generalists, and insect larvae were the main prey. Our results show that despite actively foraging, the
composition of the diets of A. ocellifera seems to be related more to variation in prey availability, supporting the prediction of MacArthur and Pianka (1966) that an exception to their theory could occur in active foraging species.
INTRODUCTION
The Optimal Foraging Theory (OFT) is a theoretical framework which has been developed in the last few decades by many authors (Emlen 1966, MacArthur & Pianka 1966, Pianka 1966), whose ultimate goal is to explain the strategies adopted by species to maximise the rate of energy intake. One of the greatest criticisms of OFT is that some of its theoretical predictions are not fully supported by empirical studies (for a revision see Perry & Pianka 1997).
However, some of the predictions have been successfully supported (Perry & Pianka 1997), for example, the prediction that “a more productive environment should lead to more restricted diet in number of different species eaten” (MacArthur & Pianka 1966). Essentially, it predicts that when the offer of prey is high in the environment, the diets should be more
