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(Rhincodon Typus) from the GULF of CALIFORNIA INSTITUTO POLITECNICO NACIONAL CENTRO INTERDISCIPLINARIO DE CIENCIAS MARINAS BIOACCUMULATION AND BIOMAGNIFICATION OF TRACE ELEMENTS IN TISSUES OF WHALE SHARK (Rhincodon typus) FROM THE GULF OF CALIFORNIA TESIS QUE PARA OBTENER EL GRADO DE DOCTORADO EN CIENCIAS MARINAS PRESENTA FRANCESCA PANCALDI LA PAZ, B.C.S., JULIO DE 2020 En la Ciudad de La Paz, B.C.S., el día 06 del mes de Junio del año 2020 El (la) que suscribe M en C. FRANCESCA PANCALDI Alumno (a) del Programa DOCTORADO EN CIENCIAS MARINAS con número de registro B161000 adscrito al CENTRO INTERDISCIPLINARIO DE CIENCIAS MARINAS manifiesta que es autor(a) intelectual del presente trabajo de tesis, bajo la dirección de: Dr. FELIPE GALVÁN MAGAÑA Y DR. FEDERICO PAEZ OSUNA y cede los derechos del trabajo titulado: “BIOACCUMULATION AND BIOMAGNIFICATION OF TRACE ELEMENTS IN TISSUES OF WHALE SHARK (Rhincodon typus) FROM THE GULF OF CALIFORNIA” al Instituto Politécnico Nacional, para su difusión con fines académicos y de investigación. Los usuarios de la información no deben reproducir el contenido textual, gráficas o datos del trabajo sin el permiso expreso del autor y/o director del trabajo. Éste, puede ser obtenido escribiendo a la siguiente dirección: [email protected] - [email protected] – Si el permiso se otorga, el usuario deberá dar el agradecimiento correspondiente y citar la fuente del mismo. M en C. FRANCESCA PANCALDI Nombre y firma del alumno Dedication ...all’Oceano e a tutte le meravigliose creature che vivono in lui, soprattutto gli squali balena... Acknowledgements Al Instituto Politécnico Nacional (IPN) y al Centro Interdisciplinario de Ciencias Marinas (CICIMAR) que me dieron la oportunidad de ser parte de esta grande familia. Al Consejo Nacional de Ciencia y Tecnología (CONACyT), Subdirección académica (SAI) y la Beca de Estímulo Institucional de Formación de Investigadores (BEIFI) por los apoyos económicos y académicos brindados. A CONANP y SEMARNAT por los permisos otorgados para la recolección de las muestras. A los doctores Felipe y Rogelio; infinitas gracias para la confianza que depositaron en mí, por apoyarme y darme la oportunidad de seguir mi sueño de estudiar los tiburones ballena. A la Dra. Ana Judith Marmolejo, por todos sus consejos, por su apoyo y por la motivación que siempre me ha dado y que me ha impulsado a mejorar. Usted es un ejemplo de mujer en la ciencia que siempre voy a tener presente. Al Dr. Federico Páez Osuna y todo el equipo del laboratorio de Geoquímica y Contaminación Costera del Instituto de Ciencias del Mar y Limnología de la UNAM. Muchísimas gracias por la ayuda, el apoyo y los valiosos consejos brindados. Gracias doctor por introducirme al misterioso mundo de la química, y por las horas invertidas explicándome las metodologías de laboratorio. Gracias por todos sus consejos que me ayudaron a publicar mis trabajos. Al Qco. Humberto Bojórquez Leyva, por su apoyo y asesoría en los análisis (liofilización, digestión y lectura) de varios de los elementos químicos estudiados. To Dr. Todd O’Hara, thank you for the valuable advices that allowed me to improve my work. To Darren, thank you for your help, support, and friendship! A Marta, Tania, Erica, Lara, Abel, Viri y todo el maravilloso Galván team! A todos los que seguramente me estoy olvidando, que de alguna manera han contribuido a la realización de este doctorado. A Erick, gracias por tu amor, por aguantar mis momentos de estrés, por tu ayuda y por todas las maravillosas aventuras marinas y terrestres pasadas y futuras. Alla mia familia, quelli che ci sono e quelli che non ci sono piú. Grazie per avermi capita, per avere accettato tutte quelle decisioni che mi hanno condotta lontana per cosí tanti anni. Vi penso sempre e vi amo. Funding and products Este trabajo fue financieramente apoyado por los siguientes proyectos: • Proyecto SIP 20180012 titulado: “Cambios en la concentración de ácidos grasos en las presas zooplanctónicas en un sitio de alimentación del tiburón ballena Rhincodon typus en el Golfo de California.” • Proyecto SIP 20190272 titulado: “Estructura de la comunidad zooplanctónica en una zona de alimentación del tiburón ballena R. typus en Bahía de La Paz” • Proyecto SIP 20195126 titulado: "Biogeoquímica de elementos traza en sistemas costeros influenciados por minería de cobre." • Proyecto SIP 253700 titulado: “Biología básica de las especies de tiburones y rayas de importancia comercial en la costa occidental de BCS.” • Proyecto SIP 20181417 titulado: “Ecología trófica de los tiburones en la costa occidental del golfo de california". • Tesis apoyada parcialmente por la Dirección General de Asuntos del Personal Académico, Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica de la Universidad Nacional Autónoma de México (DGAPA-PAPIIT-UNAM) Proyecto IN200619 titulado “Metales y metaloides en ríos y presas de cuencas mineras de Sinaloa: identificando contaminación y riesgos para la salud”. Parte de los datos e información de esta tesis se encuentran publicados en los siguientes artículos científicos: • Pancaldi, F., Galván-Magaña, F., González-Armas, R., Soto-Jiménez, M.F., Whitehead, D.A., O'Hara, T., Marmolejo-Rodríguez, A.J., Vázquez-Haikin, A., and Páez-Osuna, F., 2019. Mercury and selenium in the filter–feeding whale shark (Rhincodon typus) from two areas of the Gulf of California, Mexico. Marine Pollution Bulletin, 146: 955-961. • Pancaldi, F., Páez-Osuna, F., Soto-Jiménez, M.F., González-Armas, R., O'Hara, T., Marmolejo-Rodríguez, A.J., Vázquez-Haikin, A., and Galván- Magaña, F. 2019. Trace elements in tissues of whale sharks (Rhincodon typus) stranded in the Gulf of California, Mexico. Bulletin of Environmental Contamination and Toxicology, 103 (4): 515-520. • Whitehead, D.A., Petatán-Ramírez, D., Olivier, D., González-Armas, R., Pancaldi, F., and Galván-Magaña, F. 2019. Seasonal trends in whale sharks sightings in an established tourism site in the Gulf of California, Mexico. Journal of Fish Biology, 95: 982–984. • Whitehead, D.A., Jakes-Cota, U., Pancaldi, F., Galván Magaña, F. and González Armas, R. 2020. The influence of zooplankton communities on the feeding behaviour of whale shark in Bahia de La Paz, Gulf of California. Revista Mexicana de biodiversidad, 91: 1-8. • Whitehead, D.A., Jakes-Cota, U., Galván Magaña, F., Pancaldi, F., and González Armas, R. 2020. Composition and abundance of macro zooplankton in the coastal waters off the El Mogote Sandbar. Hidrobiológica, 30 (1): 21-27. TABLE CONTENTS CHAPTER 1. GENERAL INTRODUCTION ........................................................ 1 1.1 .THE WHALE SHARK: HISTORY, BIOLOGY AND ECOLOGY .................... 1 1.2 .TRACE ELEMENTS (TEs) ........................................................................... 4 1.2.1 Bioaccumulation and biomagnification..................................................... 8 1.2.2 Toxicity in marine organisms ................................................................... 9 1.2.3 Toxicity in human health ........................................................................ 11 1.3 . DEFENCE MECHANISMS ........................................................................ 13 1.3.1 Enzymatic response .............................................................................. 13 1.3.2 Metallothioneins (MTs) .......................................................................... 14 1.3.3 Antagonism between TEs ...................................................................... 15 1.4 .BACKGROUND ......................................................................................... 16 1.4.1 Trace elements and contamination in whale shark ................................ 16 1.4.2 Trace elements in zooplankton .............................................................. 18 1.5 . JUSTIFICATION ....................................................................................... 19 1.6 . RESEARCH OBJECTIVES ....................................................................... 20 1.7 . SPECIFIC OBJECTIVES .......................................................................... 20 1.8 . STUDY AREA ........................................................................................... 21 1.8.1 Bahía de Los Ángeles (BLA) ................................................................. 21 1.8.2 Bahía de La Paz (LAP) .......................................................................... 23 1.8.3 La Paz lagoon ........................................................................................ 24 1.9 . MATERIAL AND METHODS ..................................................................... 25 1.9.1 Biopsy collection .................................................................................... 25 1.9.2 Zooplankton collection ........................................................................... 26 1.9.3 Laboratory procedures ........................................................................... 27 CHAPTER 2. Hg AND Se BIOACCUMULATION AND BIOMAGNIFICATION IN EPIDERMIS OF WHALE SHARK FROM TWO SEASONS AND TWO AREAS OF THE GULF OF CALIFORNIA, MEXICO ..................................................... 32 2.1. ABSTRACT ............................................................................................... 32 2.2. INTRODUCTION ....................................................................................... 33 2.3. RESULTS .................................................................................................. 34 2.3.1 Sex and total length (TL) of the sharks ...................................................
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