Andreu Rico Environmental risk assessment of veterinary medicines used in Asian aquaculture Andreu Rico 1 Thesis committee Thesis supervisor Prof. Dr. Ir. Paul J. van den Brink Professor of Chemical Stress Ecology Wageningen University Other members Prof. Dr. Johan A. J. Verreth, Wageningen University Prof. Dr. Jonas S. Gunnarsson, Stockholm University, Sweden Dr. Ir. Cornelis A. M. van Gestel, VU University Amsterdam, The Netherlands Dr. Ir. Jeroen B. Guinée, Leiden University, The Netherlands This research was conducted under the auspices of the Graduate School for Socio-Economic and Natural Sciences of the Environment (SENSE) 2 Environmental risk assessment of veterinary medicines used in Asian aquaculture Andreu Rico Thesis Submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. Dr. M. J. Kropff, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Monday 26 May 2014 at 11.00 am in the Aula. 3 Andreu Rico Environmental risk assessment of veterinary medicines used in Asian aquaculture, 216 pages PhD Thesis, Wageningen University, Wageningen, NL (2014) With references, with summary in English, Dutch and Spanish ISBN 978-94-6173-956-8 4 To Neus and to my family 5 6 ‘’The chemicals to which life is asked to make its adjustments are no longer merely the calcium and silica and copper and all the rest of minerals washed out of the rocks and carried in rivers to the sea; they are the synthetic creations of man’s inventive mind, brewed in his laboratories, and having no counterparts in nature.’’ (Rachel Carson, 1962) 7 8 Contents Chapter 1. General introduction ...................................................................................................... 11 Chapter 2. Use of chemicals and biological products in Asian aquaculture and their potential environmental risks: a review ....................................................................... 19 Chapter 3. Use of veterinary medicines, feed additives and probiotics in four major internationally traded aquaculture species farmed in Asia ......................................... 37 Chapter 4. Modelling environmental and human health risks of veterinary medicinal products applied in pond aquaculture ........................................................................ 55 Chapter 5. Probabilistic risk assessment of veterinary medicines applied to four major aquaculture species produced in Asia .......................................................................... 71 Chapter 6. Use, fate and ecological risks of antibiotics applied in tilapia cage farming in Thailand ........................................................................................................................ 89 Chapter 7. Ecological risk assessment of the antibiotic enrofloxacin applied to Pangasius catfish farms in the Mekong delta, Vietnam .............................................................. 109 Chapter 8. Effects of the antibiotic enrofloxacin on the ecology of tropical eutrophic freshwater microcosms .............................................................................................. 125 Chapter 9. Predicting antibiotic resistance in aquaculture production systems and surrounding environments ......................................................................................... 145 Chapter 10. General discussion and conclusions........................................................................... 165 References. .................................................................................................................................... 179 Summary.... .................................................................................................................................... 195 Samenvatting (Dutch summary) .................................................................................................... 199 Resumen (Spanish summary) ........................................................................................................ 203 Acknowledgements ....................................................................................................................... 207 About the author ........................................................................................................................... 211 9 10 Chapter 1 General introduction 1. Background Aquaculture - the cultivation of fish, crustaceans, molluscs and water plants - has dramatically evolved during the last 30 years, becoming the fastest-growing animal food-producing sector in the world (FAO, 2012a). Nowadays, nearly 90% of the global aquaculture production is produced in Asia, with China being by far the largest producer (Fig. 1). Recent technological advances such as (1) the use of fertilizers and industrial feeds, (2) the use of electricity for water exchange management and aeration, (3) the distribution of genetically improved and pathogen free seed, and (4) the use of therapeutants and other chemicals for controlling water quality and disease outbreaks, have been introduced along the main aquaculture producing regions of Asia (Bostock et al., 2010; De Silva and Davy, 2010). These technological advances have facilitated the expansion and intensification of Asian aquaculture, leading to the so-called ‘blue revolution’ (Costa-Pierce, 2002), a process analogous to the Green Revolution experienced by the agriculture sector during the second half of the last century, which requires assessing a range of environmental issues, including water pollution and degradation of ecosystems (Bush et al., 2013). Figure 1. Aquaculture production quantities in 2010 (Mt). Data source: FAO (2012b). The majority of the Asian aquaculture is produced in inland systems such as excavated ponds and net pens or cages suspended in rivers and reservoirs, and discharge their effluents into surrounding freshwater and brackish water ecosystems (Bostock et al., 2010; Fig. 2). Effluent discharges from intensive and semi-intensive aquaculture facilities may contain high loads of nutrients and potentially toxic chemicals such as heavy metals and veterinary medicines. The increasing pressure of aquaculture production on surrounding aquatic ecosystems has been largely criticised because of their potential negative impacts on biodiversity (Primavera, 2006; De Silva, 2012; Diana, 2012), and important ecosystem services such as nutrient cycling and the provision of water and food (Beveridge et al., 1997; Soto et al., 2008). The contamination of streams and rivers may also result in negative impacts for aquaculture farmers since these 11 General introduction constitute their main source of input water for their production activities, and excessive water quality deterioration may be responsible for higher disease outbreaks and unaffordable economic losses (Bondad-Reantaso et al., 2005). The sustainable development of the Asian aquaculture industry demands an increased awareness of its environmental impacts as well as a greater commitment of science to develop the knowledge and tools required to quantify and minimize those impacts. Figure 2. Main aquaculture production systems in Asia include earthen ponds (left) and floating cages in freshwater rivers and reservoirs (right), which are hydrologically connected with the surrounding aquatic environment. 2. Veterinary medicines used in Asian aquaculture The proliferation of disease outbreaks in Asian aquaculture and the need to increase biosecurity and prevent unaffordable mortality losses has led to the introduction of a wide range of veterinary medicines (Bondad-Reantaso et al., 2005). Veterinary medicines are substances used for treating or preventing animal diseases, or for modifying physiological functions in animals1. Veterinary medicines reported to be used in Asian aquaculture include antibiotics, antifungals, anaesthetics, anthelmintics, parasiticides, hormones and growth promoters (Boyd and Massaut, 1999; Gräslund and Bengtsson, 2001; Le and Munekage, 2004; Sapkota et al., 2008; Bosma et al., 2009). They constitute a very diverse group of compounds with varied origin (e.g. synthetized by microorganisms, produced by plants, naturally occurring chemicals, synthetized by humans) and with specific modes of action. With the exception of some injectable anaesthetics, the majority of the veterinary medicines used in Asian aquaculture are administered either mixed with feed or directly to water. Aquaculture medicines may enter the environment by a number of different routes. For example, antibiotics applied mixed with feed to fish cages can enter the environment via fish faeces and urine, by the dissolution from feed, or by the sinking of uneaten feeds. Veterinary medicines applied to ponds may enter the environment via effluent discharges, by the environmental or agricultural deposition of sludge, and to a lesser extent by volatilization, percolation or leaching from aquaculture facilities (Boxall et al., 2004; Kümerer, 2009). Some studies have demonstrated that veterinary medicines applied to confined Asian aquaculture facilities constitute an important source of environmental pollution (Le and Munekage, 2004; Zou et al., 2011; Barbosa et al., 2013). For example, residues of 17α-methyl-testosterone, a hormone used to induce sex-reversal in tilapia hatcheries, have been detected in water samples collected in the surroundings of aquaculture facilities in Thailand (Barbosa et al., 2013), and antibiotics used in shrimp