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A "Biomarker+Histopathology" Toolbox in Solea Spp

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A A "biomarker+histopathology" toolbox in Solea spp. for the assessment of the biological effects of pollution in the context of the EU Marine Strategy Framework Directive Tifanie Briaudeau International PhD Thesis 2019 Department of Zoology and Animal Cell Biology Research Group: Cell Biology in Environmental Toxicology A "biomarker+histopathology" toolbox in Solea spp. for the assessment of the biological effects of pollution in the context of the EU Marine Strategy Framework Directive International Thesis submitted to the Euskal Herriko Unibertsitatea/ Universidad del Pais Vasco in the candidature for the degree of the Philosophiae Doctor by Tifanie Briaudeau Plentzia, 2019 (c)2020 TIFANIE BRIAUDEAU This study was funded by: the Spanish Ministry of Economy and Competitiveness by means of the research project BMW-CTM2012-40203-C02-01. the University of the Basque Country UPV/EHU (UFI 11/37) and the Basque Government through Consolidated Research Groups fellowship (IT810-B) the Spanish Ministry of Economy, Industry and Competitiveness through a predoctoral and mobility fellowship Acknowledgments Without the tireless support and help of all the people and institutions involved in this PhD research, none of this would have been possible. - Full professor Ionan Marigómez, Director of the Plentzia Marine Station of the University of the Basque Country (PiE-UPV/EHU), and supervisor of my Ph.D. thesis. Thank you for introducing me to the world of research and for your guidance throughout these years, always in good temper. - Assistant professor Urtzi Izagirre from the Plentzia Marine Station of the University of the Basque Country (PiE-UPV/EHU), supervisor of my Ph.D. thesis. Thank you for following my thesis with sincerity from the very beginning, for being so supportive all along and for showing me that science is a difficult but fun learning process that is worth the risk. - Dr. Stephen W. Feist, Chief Scientific Advisor on Aquatic Animal Disease and Principal Pathologist and John P. Bignell, Pathology Team Leader and Aquatic Health Pathologist of the Centre for Environment Fisheries and Aquaculture Science (CEFAS, Weymouth, UK). Thank you both so much for your help, your patience and availability, and for your scientific support throughout the tricky process of learning immunohistochemistry and histopathology. - Dr. Izaskun Zorita, Researcher in Marine and Coastal Environmental Management and Dr. Javier Franco, Principal Researcher in Marine and Coastal Environmental Management of Azti-tecnalia. Thank you both so much for your availability, for giving me the incredible opportunity of collaborating with you and your research group in the Consorcio monitoring campaigns and for your support in the writing of my first scientific publication. - Full professor Manu Soto, Deputy Director of the Plentzia Marine Station of the University of the Basque Country (PiE-UPV/EHU). Thank you for your guidance and availability, you were always happy to answer my doubts, being very patient with me and supportive of my work. - Full professor Miren P. Cajaraville, Director of the Research Group Cell Biology in Environmental Toxicology (CBET) of the University of the Basque Country (UPV/EHU). Thank you for giving me the opportunity to evolve as a scientist within the CBET Research Group. Table of contents I. General Introduction 1 1. Environmental protection of the marine and coastal 3 ecosystems 2. Solea spp. as sentinel species for the assessment of 6 coastal and estuarine ecosystem health status 3. Biological responses to pollutants 12 4. Ecotoxicological experimentation with fish 22 II. State of the Art, Hypothesis and Objectives 41 III. Results 45 Chapter I. Multi-annual survey of health status disturbance in the Bilbao estuary (Bay of Biscay) based on sediment chemistry and juvenile sole (Solea spp.) histopathology 47 Chapter II. Biological responses and toxicopathic effects elicited in Solea senegalensis juveniles on exposure to contaminated sediments under laboratory conditions 79 Chapter III. Waterborne cadmium toxicopathic effects on sole, Solea senegalensis, juveniles 127 Chapter IV. Biological responses and toxicopathic effects elicited in Solea senegalensis juveniles by waterborne exposure to benzo[a]pyrene 165 IV. General Discussion, Conclusions and Thesis 203 V. Appendix 213 I. General Introduction 2 General Introduction 1. Environmental protection of the marine and coastal ecosystems 1.1. The anthropogenic pressure Concerns on environmental protection first emerged half a century ago and was strongly focused on human interest. The United Nations Conference on the Human Environment declared in 1972: “Man has the fundamental right to freedom, equality and adequate conditions of life, in an environment of a quality that permits a life of dignity and well-being, and he bears a solemn responsibility to protect and improve the environment for present and future generations.” The consciousness for marine environment pollution was already present in this declaration with the Principle 7: “States shall take all possible steps to prevent pollution of the seas by substances that are liable to create hazards to human health, to harm living resources and marine life, to damage amenities or to interfere with other legitimate uses of the sea.” Indeed, the aquatic environment has always attracted humans’ interest for its diverse advantages such as fishing activities, water transportation, offshore oil and gas exploitation, among others (Figure 1). Coastal and estuarine areas are particularly used as a strategic point for communication through navigation, for industrial development (e.g. metallurgy, smelters, paper milling, oil refineries, shipbuilding and power stations), agricultural activities and recreation (tourism, housing, water sports). Inevitably, the extensive use of marine resources and the extreme settlement of humans along the coastline have generated a high anthropogenic pressure on the aquatic ecosystem putting at risk its survival and the viability of its resources (Islam and Tanaka, 2004; Law et al., 2010; Pan and Wang, 2012). Discharge wastewaters reach the aquatic environment and Figure 1. Main anthropogenic activities along estuarine and coastal areas and subsequent sources of hazardous substances reaching the aquatic ecosystem. Scheme modified from OSPAR, 2010). 3 tend to accumulate in confined areas such as estuaries (Law et al., 2010). These areas are also victims of dredging activities, essential for water transportation but at the origin of habitat deterioration (Martins et al., 2012). Coastal and estuarine environments are particularly crucial for the marine ecosystem as they serve as nursery grounds for many marine species (Le Pape et al., 2007). Thus, the decline in estuarine ecosystem quality generated by pollution loading and habitat loss may affect species and species recruitment level and lead to severe consequences on the survival of the biota. 1.2. Awareness and actions In response to the clear deterioration of marine environmental conditions, legislative measures and policies have been taken to protect the aquatic ecosystem. In the European Union, the Water Framework Directive (WFD, 2000/60/EC) provides a list of chemicals described as priority substances to be surveyed to reach “good ecological status”. This implies that contaminants found in the ecosystem (water, sediment and biota) are at levels not leading to harmful effects in aquatic organisms. Likewise, the Marine Strategy Framework Directive (MSFD, 2008/56/EC) aims to ensure that “concentrations of contaminants are at levels not giving rise to pollution effects” in both coastal and offshore environments (Law et al., 2010). To do so, the concentration of contaminants in the environment and the measurement of biological parameters in relation with pollutants effects are used together to assess the general health status of the aquatic ecosystem. The protection of the European marine environment is also under the implementation of Regional Sea Conventions (RSCs): OSPAR (North-East Atlantic), HELCOM (Baltic Sea), Barcelona Convention (coastal region of the Mediterranean Sea) and Bucharest Convention (Black Sea). These international legal requirements provide strategies to prevent environmental pollution and preserve aquatic ecosystems. In the case of the North-East Atlantic, the Joint Assessment and Monitoring Programme (JAMP) and the International Council for the Exploration of the Sea (ICES) guide the assessment of the general health status of the aquatic environment under the OSPAR Commission. They include the regulation of priority chemical substances, the development of appropriate environmental management and guidelines to assess the general status of the marine environment with the implementation of monitoring programmes (Hylland et al., 2017a). 1.3. From chemical analysis to biological effects Monitoring programmes were first developed to prevent contaminants consumption for human health. Programmes were based on chemical analysis for the detection and quantification of pollutants in the different compartments of the aquatic environment (water column, sediment and biota). The Mussel Watch Program was one of the first biomonitoring programmes to assess contaminants accumulation and concentrations in aquatic organisms such as mussels and oysters, based on chemical analysis (Farrington et al., 1983; Goldberg et al., 1983; Martin, 1985). Later on, the development of biological approaches allowed for the assessment of biological effects of this chemical
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