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Small Mammals As Bioindicators in the Assessment of Toxicological Effects Resulting from the Exposure to Heavy Metals

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Small Mammals As Bioindicators in the Assessment of Toxicological Effects Resulting from the Exposure to Heavy Metals UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS DEPARTAMENTO DE BIOLOGIA ANIMAL SMALL MAMMALS AS BIOINDICATORS IN THE ASSESSMENT OF TOXICOLOGICAL EFFECTS RESULTING FROM THE EXPOSURE TO HEAVY METALS CARLA CRISTINA ANTUNES MARQUES DOUTORAMENTO EM BIOLOGIA (ECOFISIOLOGIA) 2008 UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS DEPARTAMENTO DE BIOLOGIA ANIMAL SMALL MAMMALS AS BIOINDICATORS IN THE ASSESSMENT OF TOXICOLOGICAL EFFECTS RESULTING FROM THE EXPOSURE TO HEAVY METALS CARLA CRISTINA ANTUNES MARQUES (FCT/SFRH/BD/5018/2001) Tese orientada por: Professora Doutora Maria da Luz Mathias Investigadora Doutora Ana Maria Viegas-Crespo DOUTORAMENTO EM BIOLOGIA (ECOFISIOLOGIA) 2008 NOTA PRÉVIA A presente Tese Doctoral foi financiada pelas seguintes intituições: Fundação para a Ciência e a Tecnologia (Projecto: POCTI/BSE/39917/2001; Bolsa de Doutoramento: FCT/SFRH/BD/5018/2001) e pelo Conselho de Reitores das Universidades Portuguesas (Projecto CRUP: Acção Integrada Luso-Espanhola E-1505). Na elaboração desta dissertação, e nos termos do n.º 1 do Artigo 40, Capítulo V, do Regulamento de Estudos Pós-Graduados da Universidade de Lisboa, publicado no Diário da República – II Série N.º 153, de 5 de Julho de 2003, foi efectuado o aproveitamento total de resultados de trabalhos já publicados, submetidos ou a submeter para publicação. Tendo em conta que os referidos trabalhos foram realizados em colaboração com várias entidades científicas, a candidata esclarece que em todos eles participou na sua concepção, na obtenção, análise e discussão dos resultados, bem como na redacção dos artigos científicos. Devido ao facto de esta tese integrar vários artigos, o padrão de redacção apresentado é diverso, variando de acordo com as normas de cada revista científica em que os artigos se encontram publicados, submetidos ou em preparação para publicação. Lisboa, Setembro de 2008 Carla Cristina Antunes Marques TABLE OF CONTENTS ACKNOWLEDGMENTS/AGRADECIMENTOS………………………….......................... i ABSTRACT………………………………………………………………………….......... vii RESUMO…………………………………………………………………………….......... ix LIST OF ABBREVIATIONS AND SYMBOLS…………………………………................. xv 1. GENERAL INTRODUCTION………………………………………………………….. 1 1.1. Abandoned mining areas in Portugal: present situation, environmental impacts and some examples……………………………………………….................. 3 1.2. Metals toxicity …………………………………………………………………… 7 1.3. Biological markers for metal toxicity…………………………………………… 12 1.3.1. Enzymatic antioxidant defenses……………………………………………….. 13 1.3.2. Metallothioneins………………………………………………………………. 15 1.3.3. Genotoxic biomarkers…………………………………………………………. 17 1.3.4. Morphological, histological and physiological biomarkers…………………… 19 1.4. Small mammals as bioindicators of metal pollution……………..…………….. 20 1.5. Thesis context and objectives …………………………………………………… 23 1.6. Thesis structure…………………………………………………………………... 25 1.7. References……………………………………………………………………........ 27 2. IN SITU MONITORING – THE SMALL MAMMALS AS BIOINDICATORS OF 41 MINING POLLUTION…………………………………………………………................ Paper I. How does the greater white-toothed shrew, Crocidura russula, responds to a long term heavy metal contamination? – A case study. Science of the Total Environment 2007, 376: 128-133………………………………………............... 43 3 Paper II. Metal bioaccumulation in the greater white-toothed shrew, Crocidura russula, inhabiting near an abandoned pyrite mine site. Chemosphere 2007, 67: 121- 130.................................................................................................................................... 51 Paper III. Haematology, genotoxicity, enzymatic activity and histopathology as biomarkers of metal pollution in the shrew Crocidura russula. Environmental Pollution (in press).………………………………………………………………......... 63 Paper IV. Environmental quality in metal abandoned mines: the use of several biomarkers in wild small mammals (in preparation)…………………………………... 73 Paper V. Metallothionein levels in Algerian mice (Mus spretus) exposed to elemental pollution: An ecophysiological approach. Chemosphere 2008, 71: 1340- 1347………………………………………………………………………….................. 105 3. EX SITU TOXICITY TESTS - DOSE-RESPONSE ASSESSMENT: CONTROLLED 115 LABORATORY CONDITIONS…………………………………………………………… Paper I. An assessment of time-dependent effects of lead exposure in Algerian mice (Mus spretus) using different approaches. Biological Trace Element Research 2006, 109: 75-89........................................................................................................................ 117 Paper II. Induction of micronuclei and sister chromatid exchange in bone marrow cells and sperm abnormalities in Algerian mice (Mus spretus) exposed to cadmium, lead and zinc (submitted to Mutation Research)………………………………………. 135 4. GENERAL DISCUSSION AND CONCLUDING REMARKS.......................................... 157 4.1. Metal abandoned mines as an environmental problem………………………... 159 4.2. Uptake of elements by small mammals…………………………………………. 161 4.3. Toxicity biomarkers during chronic elemental exposure……………………… 163 4.3.1. In Situ monitoring…………………………………………………………… 163 4.3.2. Ex Situ monitoring…………………………………………………………... 166 4.4. Final remarks…………………………………………………………………….. 168 4.5. Future perspectives………………………………………………………………. 169 4.6. References……………………………………………………………………........ 171 ACKNOWLEDGMENTS / AGRADECIMENTOS Ao olhar para o volume de papel em que resultou o presente trabalho ficamos na dúvida a pensar como pode só isto resultar de longos anos de trabalho. No entanto, o curioso é que mais uns tantos anos ainda seriam necessários sem a preciosa ajuda de todos aqueles que em diferentes fases contribuíram para a concretização deste estudo. Como tal, gostaria de expressar a minha sincera gratidão a: ▫ Fundação para a Ciência e a Tecnologia (Projecto: POCTI/BSE/39917/2001 e Bolsa de Doutoramento: FCT/SFRH/BD/5018/2001) e Conselho de Reitores das Universidades Portuguesas (Projecto CRUP: Acção Integrada Luso-Espanhola E-1505), pelo financiamento deste trabalho. ▫ Professora Doutora Maria da Luz Mathias e Doutora Ana Maria Viegas-Crespo. Às minhas duas orientadoras agradeço por me terem iniciado nesta área de investigação interessante que é a Ecotoxicologia, pelos diversos conhecimentos científicos que me transmitiram e pelos meios técnicos e financeiros que me disponibizaram. Não poderei nunca esquecer também, em fases mais complicadas deste percurso, as palavras de encorajamento, as mensagens a perguntar se tudo estava bem e a incentivar um último esforço. Obrigada pela vossa Amizade. ▫ Sofia, como Bolseira do Projecto de Ecotoxicologia. Para capturar os ratinhos apanhámos calor, frio, chuva e carraças até (mas agora já sei que o azeite é o melhor para as tirar...). No laboratório tinhamos quase como principal actividade a limpeza e tratamento dos animais. Em vários fins-de-semana lá estávamos nós a ouvir aquela impressora, ttrrr...ttrrr... Fomos a congressos levando posters que tu fazias questão de lhe dar o melhor aspecto estético possível. Mais para final fizeste revisões de alguns textos e de artigos. Que posso dizer mais..., foste imprescindível na concretização desta minha tese. Boa Sorte para o teu percurso científico é o que eu mais desejo. ▫ Doutora Teresa Pinheiro do Instituto Tecnológico e Nuclear que me acompanhou sempre fosse dia de semana ou fim-de-semana nas análises elementares através de PIXE. Que esteve sempre presente e disponibilizando-se para me apoiar em todos os domínios, quer ao nível laboratorial quer já na fase final na revisão de textos e artigos. Muito Obrigada. i ▫ Alejandro Sánchez-Chardi da Faculdade de Biologia da Universidade de Barcelona, pela colaboração científica que estabelecemos e que nos permitiu partilhar conhecimentos, experiências e no final publicar vários artigos. Obrigada Alejandro e também Professor Jacint Nadal pelo apoio que me deram quando me desloquei a Barcelona (belíssima cidade). ▫ Doutor Fernando Capela-Silva, do Departamento de Biologia da Universidade de Évora, pelas análises histológicas, pela bibliografia disponibilizada ao longo deste trabalho, pelas respostas rápidas quando eu tinha dúvidas sobre algum assunto e pela colaboração na redacção de artigos. ▫ Professora Doutora Maria Cristina Santos do Departmento de Química e Bioquímica pelo apoio científico na determinação das actividades de enzimas antioxidantes e pelas palavras de encorajamento. ▫ Professora Doutora Maria João Bebianno da Universidade do Algarve, por me ter recebido, mesmo não me conhecendo, no seu laboratório para a determinação das metalotioninas, pelo apoio científico dado e palavras de encorajamento para continuar a avançar. ▫ Joaquim, Bolseiro de Mestrado do Projecto de Ecotoxicologia, pela ajuda na implementação da experiência laboratorial, pela tua determinação e excelentes ideias no decorrer do trabalho. Acho que nunca mais vamos esquecer o trabalhão que dava manter todos aqueles animais, mas conseguimos. Boa Sorte para o teu projecto de Doutoramento. ▫ Doutora Graça Ramalhinho do Museu Bocage, pela preciosa ajuda durante a experiência laboratorial e pelas palavras de incentivo sempre que nos encontramos. ▫ Doutor Vitor Oliveira do Instituto Geológico e Mineiro de Beja e Doutor Luís Martins do Centro de Dados Geológico-Mineiros de Lisboa pela documentação valiosa sobre minas abandonadas. ▫ Centro de Biologia Ambiental, pelo determinante apoio financeiro e logístico para a realização desta tese. ▫ Doutora Alexandra Barreiros e Catarina Ralheta do Instituto Nacional de Engenharia e Tecnologia Industrial, pelas análises
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