Marine species associated to Peruvian scallopPeruvianto associatedspeciesMarine Marine species associated to trophic interactions and contaminantexposureandinteractionstrophic Peruvian scallop Argopecten purpuratus culture: trophic interactions and contaminant exposure Argopecten by purpuratus Iván Loaiza Alamo culture: Iván EPA + DHA + ARA Mn Cu Zn Loaiza Fe As Alamo 2020 Cd Pb Ni Ghent University Faculty of Sciences Biology Department Marine Biology Research Group University of Antwerp Faculty of Sciences Biology Department Systemic Physiological and Ecotoxicological Research (SPHERE) Marine species drawings were made by the Peruvian artist Samantha Scavino, 2018 Printed by: Reproduct NV Voskenslaan 205 B-9000 Gent Academic year 2019-2020 Public defended on 28 February 2020 For citation of published work reprinted in this thesis, please refer to the original publication, as mentioned in the beginning of each chapter. To refer to this thesis, please cite as: Loaiza I. 2020. Marine species associated to Peruvian scallop Argopecten purpuratus culture: trophic interactions and contaminant exposure. Ghent University, 354 pp. 1 Marine species associated to Peruvian scallop Argopecten purpuratus culture: trophic interactions and contaminant exposure Iván Loaiza Alamo A dissertation submitted to Ghent University and University of Antwerp in fulfillment of the requirements for the degree of Doctor in Science (Marine Sciences) Promotors Prof. dr. Marleen De Troch Prof. dr. Gudrun De Boeck Academic year 2019 – 2020 2 MEMBERS OF THE EXAMINATION COMITTEE Chair: Prof. dr. Ann Vanreusel Universiteit Gent, Belgium Secretary: Dr. Carl Van Colen Universiteit Gent, Belgium Member of Jury Prof. dr. Stefaan De Henauw (GE39) Universiteit Gent, Belgium Prof. dr. Lieven Bervoets Antwerpen Universiteit, Belgium Dr. Marc Metian International Atomic Energy Agency-Environment Laboratories (IAEA-EL), France 3 Table of Contents SUMMARY ................................................................................................... 1 CHAPTER 1. GENERAL INTRODUCTION ............................................ 20 CHAPTER 2. Potential health risks via consumption of six edible shellfish species collected from Piura - Peru .............................................................. 50 CHAPTER 3. Peruvian scallop Argopecten purpuratus: from a key aquaculture species to a promising bioindicator species .............................. 88 CHAPTER 4. Marine species as safe source of LC-PUFA and micronutrients: insights in new promising marine food in Peru ................ 126 CHAPTER 5. Peruvian marine ecosystems: trophic interactions and metal transfer in aquatic food webs...................................................................... 167 CHAPTER 6. GENERAL DISCUSSION ................................................ 209 CITED LITERATURE............................................................................... 248 ADDENDUM ............................................................................................. 269 ACKNOWLEDGMENTS………………………………………………...339 PUBLICATION LIST…………………………………………….............340 4 LIST OF ABREVIATIONS AN Abrupt Niño 2017 IRZ Illescas Reserved Zone ARA Arachidonic acid (20:4n6) ISQG Interim Sediment Quality Guideline BDL Below the detection limit ITCZ Inter tropical Convergence Zone BDO Bottom dissolved oxygen JPQ Juan Paolo Quay port BMI Body mass index LC-PUFA Long-chain polyunsaturated CVD Cardiovascular disease fatty acid DHA Docosahexaenoic acid (22:6n-3) MPAs Marine Protected Areas EDI Estimated daily intake MRLs Maximum residual levels EDTA Ethylenediaminetetraacetic acid MT Metric tonnes EFA Essential fatty acids NHCS Northern Humboldt Current System EHS Environmental health status NL Northern location ENSO Niño Southern Oscillation NN No El Niño event EPA Eicosapentaenoic acid (20:5n-3) NSSs Nutritional species-specific-score ERL Effects Range-Low OMZ Oxygen Minimum Zone ERM Effects Range-Median OSPA Organizaciones Pesqueras FAs Fatty acids Artesanales FBS Food Balance Sheets PB Paracas Bay FFQ Frequency feeding questionnaire PC Peru Current GDP Gross Domestic Product PCA Principal component analysis GHG Greenhouse gas PCBM Monitoring program of mollusk HIs Total hazard indices bivalves in Peru HR-ICP-MS High resolution inductively PEL Probable effect level coupled plasma mass spectrometer PL1 Paracas location 1 ICP-MS Inductively coupled plasma PL2 Paracas location 2 mass spectrometry POM Particulate organic matter IMARPE Instituto del Mar del Peru PRODUCE Ministerio de la Producción IR Ingestion rate 5 PSJ Location in front Punta San Juan Reserved Zone PTDI Provisional Tolerance Daily Intake PTWI Provisional Tolerance Weekly Intake PUFA Polyunsaturated fatty acid RD River discharge RNSIIPG Peruvian Guano Islands, Isles and Capes National Reserve RSM Response surface methodology SANIPES Organismo Nacional de Sanidad Pesquera SB Sechura Bay SBT Sea bottom temperature SDGs Sustainable Development Goals SDO Surface dissolved oxygen SERNANP Servicio Nacional de Áreas Naturales Protegidas SFA Saturated fatty acid SHO Location in front of the iron company Shougang Hierro Peru S.A.A SIAR Stable isotope analysis in R SL Southern location SRM Standard reference material SS Surface salinity SST Sea surface temperature Tb1/2 Estimated biological half-lives THQs Target hazard quotients TMFs trophic magnification factors TP Trophic positions TRs Target cancer risks 6 SUMMARY The present study addressed current concerns related to the seafood safety in Peru. The potential strategies to determine the current environmental health status (EHS), through bio-monitoring approaches were investigated. The levels of chemicals (i.e. metals, fatty acids, stable isotopes) in environmental compartments (from POM to top- predators) were assessed and their consequences at different levels of organization were discussed, e.g. contaminant transfer through the food web, potential value as nutritive seafood and/or risk for seafood consumers. As result, an integrated approach for the assessment of risks and benefits for consuming marine species from Peru was addressed. In order to test whether the Peruvian seafood consumption could pose a human health risk due to the accumulated metal levels of these products, metal bioaccumulation was studied throughout the food chain (chapter 2). From this study it became apparent that in 6 of the studied marine edible species, around 10-20% of the molluscs (e.g. Argopecten purpuratus, Bursa ventricosa…) and 30-40% of the crustaceans (e.g. Romaleon setosum, Hepatus chilensis…) exceeded the maximum residual levels (MRLs) for human consumption in inorganic As and Cd. Integrated risk indices, e.g. target hazard quotient (THQs), total hazard indices (HIs), provisional tolerable weekly intake (PTWI) did not exceed their respective limits, however the target cancer risks (TRs) for inorganic As were always higher than the threshold (1x10-6), therefore an actual cancer risk is present. The results confirmed that Peruvian marine species are loaded with As and Cd and that MRLs and TRs were 1 again higher than the thresholds for some species (from the 54 studied species), such as the crab H. chilensis, the mantis shrimp Squilla sp., the mussel Semimytilus algosus, and the snail B. ventricosa, among others (chapter 4). Nevertheless, some marine species are also high in beneficial compounds: long-chain polyunsaturated fatty acids (LC-PUFAs): EPA, DHA, ARA; and micro-nutrients: Cu, Fe, Mn and Zn. The north of Peru was characterized by marine species with the highest LC-PUFAs (up to 180 mg EPA/100g), followed by those from the center and southern regions. Moreover, the species considered as potentially edible or non- edible species (e.g. C. sexdecimdentatus, C. filiformis, C. plebejus) are promising future foods due to their high nutritional values (high LC- PUFAs and micro-nutrients). Based on risk indices, it was concluded that the consumption of the estimated safe amounts of seafood could lead to a high contribution (up to 80% of the recommended values) of beneficial LC-PUFAs and micro-nutrients in Peruvian populations (chapter 4). Based on nutritional indices, the gastropods (e.g. B. ventricosa) were scored as the least beneficial species for human consumption. The quality of marine species as seafood was further monitored in the frame of the complexity of the Peruvian marine ecosystems, which are driven by the northern Humboldt Current system (NHCS), and simultaneously impacted by oceanographic drastic variations (i.e. El Niño event). The intensities of El Niño phenomenon effect on fatty acids and metal contamination were monitored and analyzed using the Peruvian scallop A. purpuratus in different regions of Peru (chapter 3). 2 A. purpuratus was identified as potential bioindicator species to be used along the coast of Peru. Gills, digestive gland and intestine were the tissues where metal accumulation was the highest in A. purpuratus. Fatty acids were good biomarkers when annual (El Niño effect) comparisons were performed, while metals allowed to discriminate amongst locations (degree of pollution). The application of a series of biomarkers (i.e. metals, fatty acids) is key to understand the response of organisms to natural and/or anthropogenic stressors. However, cost- benefit relationships should be considered for a long-term and sustainable scallop monitoring program in Peruvian water domains. Food web interactions and metal transfer in Peruvian marine ecosystems were integrated to understand the flow of