2.2 Contribution of Capture Fisheries and Aquaculture in Philippine Economy

Public Disclosure Authorized Public Disclosure Authorized An Overview of Agricultural Pollution

Public Disclosure Authorized in the Philippines The Fisheries Sector 2016 Public Disclosure Authorized

An Overview of Agricultural Pollution in the Philippines The Fisheries Sector 2016

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Cite this report as: Cuvin-Aralar, M.L.A., C.H. Ricafort, and A. Salvacion. 2016. “An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector.” Prepared for the World Bank. Washington, D.C.

Publication design and typesetting by The Word Express, Inc. Cover photos courtesy of istock.com and shutterstock.com. CONTENTS

Abbreviations and Acronyms...... vii Foreword...... ix

1 Introduction...... 1 1.1 History of Capture Fisheries and Aquaculture in the Philippines. . . 1 1.2 Capture Fisheries and Aquaculture Development in the Philippines. . 3

2 Increased Population and Drive for Economic Growth Pushed for Increasing Fisheries Production in the Philippines ...... 15 2.1 Population Pressure to Increase Fish Production from Capture Fisheries and Aquaculture...... 15 2.2 Contribution of Capture Fisheries and Aquaculture in Philippine Economy...... 17

3 Approaches to Improve Fisheries Production Resulted in the Various Impacts and Became Sources of Environmental Problems and Pollution...... 21 3.1 Conversion of Land and Water Resources for Aquaculture. . . . . 21 3.2 Practices to Prepare and Improve Culture Environment ...... 24 3.3 Practices to Improve Production...... 26 3.4 Practices to Improve Aquatic Animal Health...... 29 3.5 Practice to Diversity Cultured Commodities...... 30

4 Physical Impacts...... 33 4.1 Environmental Impacts ...... 33 4.2 Impact of Diversification of Culture Commodities through Species Introductions...... 37 iv An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

5 Socioeconomic and Health Impacts of Fisheries and Aquaculture Practices...... 41 5.1 Human Health Impacts ...... 41 5.2 Socioeconomic Impacts...... 42

6 Solutions to Mitigate Impacts of Aquaculture Pollutants...... 45 6.1 Use of Eubiotics and Strategies to Improve Health of Aquatic Animals...... 45 6.2 Legislations and Regulations on the Use of Chemicals and Fisheries and Aquaculture. . .47 6.3 Regulations on the introduction of nonnative species for culture and protecting local species...... 52 6.4 Technologies to Reduce Nutrients from Aquaculture...... 52

References ...... 57

List of Figures Figure 1: The Philippines’ total fisheries production compared to total world production from capture fisheries and aquaculture...... 3 Figure 2: Percentage contribution and rank of Philippine fisheries to world production. . . . 4 Figure 3: Trend of fisheries production in the Philippines...... 4 Figure 4: Average change in volume of production in Philippine fisheries from 1980 to 2014...... 5 Figure 5: Capture fisheries data for the Philippines...... 5 Figure 6: Average change in volume of production in Philippine capture fisheries from 1980 to 2014 ...... 5 Figure 7: Marine and inland capture fisheries data...... 6 Figure 8: Average change in volume of production in Philippine marine capture fisheries from 1980 to 2014 ...... 6 Figure 9: Average volume of production in Philippine marine capture fisheries from 1980 to 2014 ...... 6 Figure 10: Average volume of production in Philippine inland capture fisheries from 1980 to 2014 ...... 7 Figure 11: Average change in volume of production in Philippine inland capture fisheries from 1980 to 2014 ...... 7 Figure 12: Aquaculture production in marine, freshwater, and brackish-water culture environments (excluding aquatic plants) ...... 8 Figure 13: Average volume of production in Philippine brackish-water aquaculture from 1996 to 2014 ...... 8 Figure 14: Average change in volume of production in Philippine brackish-water aquaculture from 1996 to 2014 ...... 9 Figure 15: Average volume of production in Philippine freshwater aquaculture from 1996 to 2014 ...... 9 Figure 16: Average change in volume of production in Philippine freshwater aquaculture from 1996 to 2014 ...... 9 Figure 17: Top aquaculture fishery commodities in Philippine aquaculture ...... 10 Figure 18: Average volume of production in Philippine marine aquaculture from 1996 to 2014 ...... 10 Contents v

Figure 19: Average change in volume of production in Philippine marine aquaculture from 1996 to 2014 ...... 11 Figure 20: Volume of production in Philippine small-farm reservoir in 2014...... 11 Figure 21: Average change in volume of production in Philippine peneid shrimp aquaculture from 1996 to 2014...... 11 Figure 22: Average volume of production in Philippine peneid shrimp aquaculture from 1996 to 2014 ...... 12 Figure 23: Average volume of production in Philippine tilapia aquaculture from 1996 to 2014 ...... 13 Figure 24: Average change in volume of production in Philippine tilapia aquaculture from 1996 to 2014 ...... 13 Figure 25: Average change in volume of production in Philippine milkfish aquaculture from 1996 to 2014 ...... 13 Figure 26: Average volume of production in Philippine milkfish aquaculture from 1996 to 2014 ...... 14 Figure 27: Philippine population growth ...... 16 Figure 28: Value of fisheries production in Philippine pesos from 1980 to 2014...... 17 Figure 29: Contribution of fisheries to the Philippines’ GDP...... 17 Figure 30: Contribution of fisheries to GVA at constant prices...... 18 Figure 31: Comparison of value of exports and imports of fisheries products...... 18 Figure 32: Import dependency ratio of three major fish culture commodities...... 19 Figure 33: Production cost, farm gate price, and profit margins for milkfish culture...... 19 Figure 34: Process of establishment of MPs in the Philippines ...... 22 Figure 35: Site of MPs for establishment in the Philippines ...... 23 Figure 36: Number of aquatic animal species introductions in the Philippines in the various decades ...... 30 Figure 37: The loss of mangrove areas and the development of brackish-water ponds in the Philippines...... 33 Figure 38: Occurrences of fish kill in Taal Lake due to various factors including lake overturn, population, oxygen depletion, sulfur upwelling, and timud infestation based on BFAR announcements and reports from 1998 to 2011...... 36 Figure 39: Schematic diagram of direct and indirect impacts of species introduction on biodiversity...... 39 Figure 40: Sources and pathways of how antibiotics are released into the environment. . . . .43 Figure 41: Schematic diagram of farm layout (top-top view; bottom-cross-sectional view) of rice-prawn culture in Laguna based on a 1,000 m2 area...... 54 Figure 42: Cost and return for rice monoculture and rice-prawn integrated culture for a 1,000 m2 plot from pilot studies of the BFAR...... 54

List of Tables Table 1: Estimated fish consumption, fish production, and surplus/deficit in the Philippines...... 16 Table 2: Performance of two MPs...... 23 Table 3: Groups of chemicals and additives used in aquaculture...... 24 Table 4: Application of inorganic fertilizer in shrimp Penaeus monodon and milkfish Chanos chanos ponds for the period surveyed in 1995–1996 and 2006–2007. . . .26 Table 5: Summary of organic fertilizers used in milkfish and shrimp ponds and in polyculture of these two commodities ...... 27 vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Table 6: Use and dosage of other chemicals to modify soil or water quality for aquaculture of milkfish and shrimp and polyculture of the two species...... 27 Table 7: Application of common piscicides and molluscicides in milkfish and shrimp culture and polyculture of these two commodities...... 28 Table 8: Sample of hormone dosage used for induced spawning of the Asian catfish Clarias microcephalus and bighead carp Aristichthys nobilis...... 28 Table 9: Common anesthetics and dosage used in common aquaculture species found in the Philippines...... 29 Table 10: Antibiotic feed additives and their use and dosage as applied to shrimp culture. . . 29 Table 11: Disinfectants used in black tiger shrimp brackish-water farms in the Philippines in 2006–2008*...... 30 Table 12: Partial list of invasive and potentially invasive introduced species to the Philippines...... 31 Table 13: Estimated organic matter and nutrient loading for one ton of harvested shrimp released at different FCRs ...... 34 Table 14: Comparison of phosphorus values from marine aquaculture sites in the Philippines...... 35 Table 15: Level of OTC, OXA, and OCP in fish samples from the Philippines ...... 37 Table 16: Production value (in PHP, thousands) of milkfish and tilapia as well as total cultured fish production in Laguna de Bay...... 43 Table 17: Probiotics used in shrimp brackish-water farms in the Philippines...... 46 Table 18: Banned veterinary drugs in aquaculture feeds...... 48 Table 19: PNS for various fishery products...... 49 Table 20: List of chemicals used in aquaculture and their status in the Philippines and other ASEAN member countries...... 50 ABBREVIATIONS AND ACRONYMS

AFMA Agriculture and Fisheries Modernization Act ASEAN Association of Southeast Asian Nations BFAR Bureau of Fisheries and Aquatic Resources BFT Biofloc Technology BW Body Weight CA Competent Authority CFA Committee on Fisheries and Aquaculture CHED Commission on Higher Education DA Department of Agriculture DENR Department of Environment and Natural Resources DOH Department of Health FAO Food and Agriculture Organization FCR Feed Conversion Ratio FLA Fishpond Lease Agreement FOS Fructooligosaccharides FPA Fertilizer and Pesticide Authority GAqP Good Aquaculture Practice GDP Gross Domestic Product GVA Gross Value Added HCG Human Chorionic Gonadotropin IAA Integrated Agri-Aquaculture ICMSF International Commission on Microbiological Specifications for Food IMTA Integrated Multitrophic Aquaculture KDF Potassium Diformate LGU Local Government Unit LHRHa Luteinizing Hormone Releasing Hormone-Analog MOS Mannanoligosaccharides MF Maintenance Feeding viii An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

MP Mariculture Park PNS Philippine National Standards MRL Maximum Residue Limit OCP Organochlorine Pesticides MT Methyltestosterone OTC Oxytetracycline NDF Sodium Diformate OXA Oxalinic Acid NPK Nitrogen, Phosphorus and SEAFDEC/AQD Southeast Asian Fisheries Devel- Potassium opment Center, Aquaculture OA Organic Acid Department PCAF Philippine Council for Agriculture SF Submaximum Feeding and Fisheries WHO World Health Organization PEL Permissible Exposure Limit FOREWORD

This report is part of a national overview of agricultural pollution in the Philip- pines, commissioned by the World Bank. The overview consists of three “chapters” on the crops, livestock, and fisheries sub-sectors, and a summary report. This “chap- ter” provides a broad national overview of (a) the magnitude, impacts, and drivers of pollution related to the fisheries sector’s development with a focus on aquaculture; (b) measures that have been taken by the public sector to manage or mitigate this pollution; and (c) existing knowledge gaps and directions for future research. This report was prepared on the basis of existing literature, recent analyses, and national and international statistics, as well as extensive interviews. It did not involve new primary research and did not attempt to cover pollution issues that arise in the broader aquaculture value chain, relating for instance to processing, packaging and transportation, feed processing, or veterinary drug factories.

INTRODUCTION 1

1.1 History of Capture Fisheries and Aquaculture in the Philippines

There are limitations in the availability of historical data on capture fisheries in the Philippines. Fairly accurate national statistics on the country’s capture fisheries are relatively recent. Although it is difficult to clearly establish capture fishery practices in prehistoric times, ethnographic evidence shows that in Southeast Asia, its inhab- itants have used some technical devices to obtain food from the sea. It is assumed that in the Philippines, coastal dwellers also engaged in fishing activities. Capture fisheries was limited to the land-water interface of the coastal areas and those of rivers and lakes. Early observations by colonizing Spaniards in the 1500s describe the barter-type relationship between fishermen who lived on the coast and farmers who lived in upland areas (Blair and Robertson 1903, as cited by Spoehr 1984). His- torical records also show some semblance of control on marine fisheries resources in precolonial Philippines where village chiefs give permission to people outside their village to fish within the designated limits of their village after paying for the privilege (Blair and Robertson 1903, as cited by Spoehr 1984). During the Span- ish colonial times, the control of the fishing areas came under the purview of the colonial government (Spoehr 1984). Specialized fishing villages/communities came about during the Spanish colonial times, with the subsequent growth of Manila and other towns providing established fixed markets for fishery products. In the early 1900s, fishing towns as they are known at present emerged, wherein their primary activity centered on catching, processing, bulking, and marketing of fish on a much larger scale compared to heretofore village-size fishing communities (Spoehr 1984). Thus, with a combination of population growth, technological advancement, and changes in economic structure, the small fishing villages evolved into fishing towns 2 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector and some areas into fish port and fish landing areas sup- is a consequence of rapid population growth accompa- porting large-scale commercial fishing. nied by increased demand for fish and fishery products Capture fisheries technology in the Philippines since production from capture fisheries has become in- also evolved through time. Early trades with China and creasingly unable to meet the demand due to a variety the settlement of Chinese communities resulted in the of factors, foremost of which are over exploitation and introduction of some capture fisheries gears by this eth- the depletion of natural stocks (Sapkota et al. 2008). nic group, such as the large lever net or ‘salambaw’ as In Southeast Asia, the early development of well as gill and casting nets (Rasalan 1952, as cited by aquaculture first started in the 15th century in Indo- Spoehr 1984). The capture fishing industry during the nesia with brackish-water culture and spread to neigh- Spanish colonial times was relatively static from a tech- boring countries. The Philippines being an archipelago, nological standpoint. In the late 1800s, Tagalog inno- with more water than land like Indonesia, followed suit. vations such as a type of round haul seine ‘sapiao’ and Expansion of the aquaculture industry in the a deepwater fish corral spread to the archipelago (Um- Philippines was further stimulated with the establish- ali 1950, as cited by Spoehr 1984). In pelagic fishing, ment of the Bureau of Fisheries and Aquatic Resources more innovations such as a type of purse seine, gill net, (BFAR) in the late 1940s. The BFAR established and and lift net were adopted. Japanese commercial fish- implemented schemes to promote aquaculture through ing innovations such as the beam trawl and ‘muro-ami’ the construction of ponds (Primavera 1995). Since were introduced. With these innovations, the Philip- then, aquaculture has evolved in the country with a di- pines’ capture fisheries transformed from a broad-spec- verse list of species cultured in a variety of ecosystems. trum, small-scale type to more capital-intensive and The bulk of the production is from aquatic plants (sea- highly specialized fish-catching methods. The period weeds), milkfish, tilapia, shrimp, carp, and bivalves like since World War II has seen the greatest technological oyster and mussel. Like capture fisheries, aquaculture advances in capture fisheries in the country than any has significantly contributed to food security and rural other period before that (Spoehr 1984). livelihood. The Philippines ranked 4th with regard to Details on the early history of aquaculture are aquaculture production in 1997, but dropped to 12th unclear, although people have been farming fish for place by 2012 (FAO 2014) and moved slightly to 11th thousands of years based on evidence of fish farming place in 2013 (FAO FishStat 2015). in the Arab Republic of Egypt and China in 2500 BC Milkfish was the primary coastal aquaculture and 1100 BC, respectively (Landau 1992). In South- commodity cultured in brackish-water ponds, with east Asia, brackish-water pond culture can be traced Food and Agriculture Organization (FAO) records dat- from Indonesia almost 600 years ago (Schuster 1952, ing back to 1950. The culture of this euryhaline species as cited by Primavera 1995). This gradually spread to spread to freshwater and by the 1990s to marine cages. other Southeast Asian countries. In the Philippines, the Hand in hand with developments in the technology of earliest fishpond record was in Rizal Province in 1863 milkfish culture and success in the captive breeding of (Philippine Census of 1921 in Siddall, Atchue, and the commodity pioneered by the Southeast Asian Fish- Murray 1985). At the turn of the century, there were eries Development Center/Aquaculture Department reports of pond culture in the Manila area (Radcliffe (SEAFDEC/AQD) (Marte and Lacanilao 1986; Juario 1912, as cited by Primavera 1993). et al. 1984) coupled with the promotion of the culture Traditional aquaculture involved minimal in- of the commodity by the locals, the production of the puts, small farm size, and low stocking density. This commodity spread to other areas of the country. type of fish farming has been practiced in many parts of The culture of peneid shrimps, mainly the the world for centuries. Intensification of aquaculture black tiger shrimp Penaeus monodon, evolved from Introduction 3 traditional, to extensive, to semi-intensive, and finally from 17 in 1950–1965 to 5 in 2010. In 2013, the to an intensive farming system (Primavera 1991). From country ranked eighth in the world (Figure 2). being a by-product (from accidental entries into ponds) The contribution of aquaculture to the coun- of milkfish aquaculture, the tiger shrimp industry de- try’s production has increased dramatically from just veloped as a separate and important aquaculture com- 10.7 percent (25,649 tons) in 1950 to 50.4 percent modity. Traditional and extensive culture shrimp farm- (4,708,790 tons) in 2013, including aquatic plants ing systems relied on tidal water exchange and available (Figure 3). Despite advances in aquaculture, there was natural productivity since stocking rates are quite low −4 percent growth in the fisheries sector for the peri- from less than 1 prawn/m2 (traditional) to 1–3 prawns/ od 2013 to 2014 compared to 1.2 percent growth in m2 (extensive) and maybe in polyculture with milkfish. the agriculture and forestry sector for the same period (PSA 2015). Among the 81 provinces in the country, Pala- 1.2 Capture Fisheries and Aquaculture wan exhibited the fastest increase in production in the Development in the Philippines last 34 years. Palawan set an average annual increase of 14,000 tons in production from the years 1980 to The Philippines’ fisheries production, capture and 2014. This is way higher when compared to the 1980s’ aquaculture combined, has steadily increased since the top producer, Laguna, which rather suffered from an 1950s. From 0.230 million tons in 1950, the produc- average annual decrease of 5,000 tons in production for tion steadily increased to 5.158 million tons, an equiv- the same period (Figure 4). alent average growth of 22.4-fold. However, there was a slight decrease in total production from 2011 to 2013 (Figure 1). 1.2.1 Capture Fisheries The percentage contribution of the Philippines’ The average growth of the Philippine marine capture fisheries to world production ranged from 1.2 percent fisheries from 2003 to 2012 is just 4.6 percent. This is in 1950 to 3.1 percent in 2010. The country’s world low in comparison to China (13.6 percent), Indonesia ranking also improved with its percentage contribution, (27 percent), and Vietnam (46.8 percent) for the same

Figure 1: The Philippines’ total fisheries production compared to total world production from capture fisheries and aquaculture

200 180 160 140 120 100 80 60 40

Production, tons (x 1,000,000); 20 Phil. Production, tons (x 100,000) 0 1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010 2011 2012 2013 World production Philippine production

Source: FAO FishStat 2015. 4 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Figure 2: Percentage contribution and rank of Philippine fisheries to world production

3.5% 1 3.0% 3 5 2.5% 7 2.0% 9 1.5% 11

1.0% 13 World Ranking 0.5% 15

Contribution to World Production 17 0% 1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010 2011 2012 2013 Contribution, % World Rank

Source: FAO FishStat 2015.

period. Myanmar with 121.4 percent has the highest provincial level, Laguna exhibited the fastest decline in growth in the world (FAO 2014). production from 1980 to 2014 (Figure 5). Based on FAO FishStat (2015), total capture fish- On the other hand, South Cotabato achieved an eries in the Philippines peaked in 2010 with 2,615,801 average annual increase of 7,000 tons in production for tons, equivalent to a more than 12-fold increase from the same period, making it the highest contributor in 213,227 tons in 1950 (Figure 5). capture fisheries. In 2014, the total production declined to Ninety percent of the total production in cap- 2,351,479 tons. This corresponds to about 10 percent ture fisheries is attributed to marine commodities and decrease in production relative to the 2010s. At the the remaining 10 percent to inland capture fisheries

Figure 3: Trend of fisheries production in the Philippines

2 million of metric tons Volume of Production, 1

0 1950 1953 1956 1959 1962 1965 1968 1971 1974 1977 1980 1983 1986 1989 1992 1995 1998 2001 2004 2007 2010 2013 Capture Aquaculture Total

Source: FAO FishStat 2015. Introduction 5

Figure 4: Average change in volume of Figure 6: Average change in volume of production in Philippine fisheries production in Philippine capture from 1980 to 2014 fisheries from 1980 to 2014

Source: Based on PSA 2015 data. Source: Based on PSA 2015 data.

Figure 5: Capture fisheries data for the based on the data of FAO FishStat from 1950 to 2013 Philippines (Figure 7). 3.0 The major provinces contributing to marine capture fisheries are shown in Figure 8. 2.5 Laguna Province is one of the main players in 2.0 inland capture fisheries. In 2014, the province con- 1.5 tributed 19 percent to the total production in inland capture fisheries next to Rizal (28 percent), mainly due 1.0 to production from the country’s largest inland water million of metric tons Volume of Production, 0.5 body, Laguna de Bay, bounded by these two provinces (Figure 10). However, it is in this specific subsector 0 that Laguna had the fastest decline in total production

1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010 2015 in capture fisheries from 1980 to 2014 as shown in Source: FAO FishStat 2015. Figure 11. 6 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Figure 7: Marine and inland capture Figure 8: Average change in volume of fisheries data production in Philippine marine capture fisheries from 1980 to 3.0 2014 2.5

2.0

1.5

1.0 million of metric tons Volume of Production, 0.5

0 1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010 2015 Inland Marine

Source: FAO FishStat 2015.

1.2.2 Aquaculture From the 1950s to 1970s, brackish-water aquaculture dominated the fish culture scene, contributing to 87 percent of total production while the remaining was mainly from freshwater aquaculture (Figure 12). Source: Based on PSA 2015 data.

Figure 9: Average volume of production in Philippine marine capture fisheries from 1980 to 2014

Source: Based on PSA 2015 data. Introduction 7

Figure 10: Average volume of production in Philippine inland capture fisheries from 1980 to 2014

Source: Based on PSA 2015 data.

In 2014, 15 percent of the 322,668 tons of pro- Figure 11: Average change in volume of duction in brackish-water aquaculture came from Pam- production in Philippine inland panga (Figure 13). In line with this, it was reported to capture fisheries from 1980 to have an average annual increase of 1,000 tons in pro- 2014 duction in the last 18 years (Figure 14). Moreover, Pampanga also contributed the most in freshwater aquaculture, but in much greater volume. In 2014 alone, the province produced 103,131 tons (35 percent) of cultured fish from freshwater farms (mainly fishponds) or about the same as the combined production of Batangas (22 percent) and Rizal (16 percent) as shown in Figure 15. Freshwater aquaculture production in the country increased to 299,000 tons in 2014 as compared to just 3,300 tons in 1950. Pampanga, along with Batangas and Rizal, are the fastest-growing provinces with regard to production in freshwater aquaculture. On the other hand, marine aquaculture was generally confined to seaweeds and other aquatic plants up until the early 1970s. However, since then marine fish aquaculture grew in volume and by 2014, marine fish production from aquaculture contributed almost 125,000 tons compared to a measly 38 tons in 1972 (Figure 17). Seventy-six Source: Based on PSA 2015 data. 8 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Figure 12: Aquaculture production in marine, freshwater, and brackish-water culture environments (excluding aquatic plants)

0.9 0.8 0.7 0.6 0.5 0.4 0.3 million of metric tons

Volume of Production, 0.2 0.1 0 1950 1953 1956 1959 1962 1965 1968 1971 1974 1977 1980 1983 1986 1989 1992 1995 1998 2001 2004 2007 2010 2013 Brackish Freshwater Marine

Source: FAO FishStat 2015.

percent of this came from Pangasinan alone. As the top In addition, small-farm reservoirs are also pres- contributor in marine fish aquaculture, Pangasinan had ent in the country, which produced almost 100 tons of an average annual increase of 5,000 tons in production cultured fish annually. These mainly came from Quiri- from 1996 to 2014 (Figure 18). no and North Cotabato (Figure 19).

Figure 13: Average volume of production in Philippine brackish-water aquaculture from 1996 to 2014

Source: Based on PSA 2015 data. Introduction 9

Figure 14: Average change in volume Figure 16: Average change in volume of production in Philippine of production in Philippine brackish-water aquaculture freshwater aquaculture from from 1996 to 2014 1996 to 2014

Source: Based on PSA 2015 data. Source: Based on PSA 2015 data.

Figure 15: Average volume of production in Philippine freshwater aquaculture from 1996 to 2014

Source: Based on PSA 2015 data. 10 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Figure 17: Top aquaculture fishery commodities in Philippine aquaculture

0.9 0.8 0.7 0.6 0.5 0.4 0.3 million of metric tons

Volume of Production, 0.2 0.1 0 1950 1953 1956 1959 1962 1965 1968 1971 1974 1977 1980 1983 1986 1989 1992 1995 1998 2001 2004 2007 2010 2013 Others Shrimps Milkﬁsh Tilapias

Source: FAO FishStat 2015.

Dominant fish species cultured are peneid total volume of 730,000 tons and at an estimated total shrimps (mainly tiger shrimps), tilapias (mainly Nile ti- value of US$1.8 million (Figure 20). lapia), and milkfish. These three commodities comprised From these three commodities, with the devel- 77 percent of fish aquaculture production by 2013 at a opment of aquaculture technologies for other aquatic

Figure 18: Average volume of production in Philippine marine aquaculture from 1996 to 2014

Source: Based on PSA 2015 data. Introduction 11

Figure 19: Average change in volume of Figure 21: Average change in volume of production in Philippine marine production in Philippine peneid aquaculture from 1996 to 2014 shrimp aquaculture from 1996 to 2014

Source: Based on PSA 2015 data. Source: Based on PSA 2015 data.

Figure 20: Volume of production in Philippine small-farm reservoir food species, the list of aquaculture commodities ex- in 2014 panded by the 1980s to include crabs and snappers. By 2013, the list included groupers and siganids. Peneid shrimps were produced in brackish-water and marine culture systems, with peak volume in 1993 close to 96,000 tons. Thereafter, production sharply declined to a low of less than 38,000 tons in 1998, equivalent to only 40 percent of its peak production. The decline was due to the onset of devas- tating diseases which decimated the shrimp industry not only in the country but in many shrimp-producing countries as well. At the provincial level, Negros Occi- dental suffered the most with a 95 percent decrease in production from 1996 to 1998. The production of the said province continues to decline by an average of 991 tons each year. From the 18,000 tons of production in 1996, Negros Occidental produced only 46 tons of Source: Based on PSA 2015 data. peneid shrimps in 2014 (Figure 21). 12 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Figure 22: Average volume of production in Philippine peneid shrimp aquaculture from 1996 to 2014

Source: Based on PSA 2015 data.

But then again, the country’s production gradu- the strains developed in the Philippines. A few of these ally picked up. As of 2014, however, it has not yet fully technologies and strains are now being used in other recovered with just 51,000 tons of production valued at tilapia-producing countries. (Macaranas et al. 1995; US$500,000. This increase can primarily be attributed Bolivar et al. 1993). to Pampanga, which produced 20,000 tons (39 per- Milkfish (Chanos chanos) on the other hand is a cent) of peneid shrimps in 2014. This is followed by commodity with wide salinity tolerance, making it ideal Lanao del Norte with 10,000 tons (21 percent) of pro- for culture in all three aquaculture environments: ma- duction as presented in Figure 22. rine, brackish, and freshwater farming systems. From In line with this, Pampanga also surpassed 80 oth- 1950 to the mid-1990s, based on FAO records (Fish- er provinces in the country by producing 100,000 tons Stat), milkfish was cultured mainly in brackish-water of tilapia. It is equivalent to 41 percent of the total tilapia ponds with about a tenth of total production from produced in 2014. It is 50 percent higher when compared freshwater aquaculture. The culture of milkfish in fish to the second-highest producer, Batangas (Figure 23). pens in Laguna de Bay, the largest inland water body Tilapia culture started off with the Mossambique in the country, started in the early 1970s (Delmendo tilapia (Oreochromis mossambicus) and was gradually re- and Gedney 1976) and gradually spread to other in- placed by Nile tilapia (Oreochromis niloticus) (Gupta land water bodies like Taal Lake (Tan, Garcia, and Tan and Acosta 2004). A number of genetic improvement 2011) (Figure 25). By 2013, total milkfish production programs for Nile tilapia have been undertaken by var- in the three culture environments was at its highest at ious government institutions as well as universities. The over 401,000 tons, in which 25 percent came from GIFT, Get Excel, FAST, and GMT are just a few of Pangasinan alone (Figure 26). Introduction 13

Figure 23: Average volume of production in Philippine tilapia aquaculture from 1996 to 2014

Source: Based on PSA 2015 data.

Figure 25: Average change in volume Figure 24: Average change in volume of of production in Philippine production in Philippine tilapia milkfish aquaculture from 1996 aquaculture from 1996 to 2014 to 2014

Source: Based on PSA 2015 data. Source: Based on PSA 2015 data. 14 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Figure 26: Average volume of production in Philippine milkfish aquaculture from 1996 to 2014

Source: Based on PSA 2015 data. INCREASED POPULATION AND 2 DRIVE FOR ECONOMIC GROWTH PUSHED FOR INCREASING FISHERIES PRODUCTION IN THE PHILIPPINES

2.1 Population Pressure to Increase Fish Production from Capture Fisheries and Aquaculture

The Philippines’ population tripled from 30.9 million in 1965 to 92.3 million in 2010 (PSA 2015). It is projected to be 101.45 million by the end of 2015 and if current growth continues, it may reach 110.97 million in 2020, 130.47 million in 2030, and 142.73 million in 2045 (Figure 27, Trading Economics 2015). Popu- lation growth rate has slowed down—the growth rate for the period 2000–2010 was 1.9 percent compared to 2.34 percent for the period 1990–2000 (PSA 2015). The increase in population is accompanied by increase in fish consumption. The continued increase in the country’s population (Figure 27) was accompanied by an increase in total fish production (Figure 3), with aquaculture’s contribution increasing significantly in the last decade. 16 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Figure 27: Philippine population growth

120

100

Million 60

20 1969 1980 1991 2002 2013

Source: Trading Economics 2015.

In 1965, fish consumption of Filipinos was at average consumption for the last four decades which is 23.09 kg/capita/year. This increased to 31.58 kg/cap- close to 32 kg/capita/year. ita/year by 2013, with the highest consumption of With regard to self-sufficiency in fish produc- 35.64 kg/capita in 2010 (Table 1). This translates to a tion compared with fish consumption, there was a defi- total fish consumption of 3.1 tons in 2013 and 3.3 tons cit from 1961 to 1975. To address the deficit in fish in 2010. If the country’s population grows as expect- supply for local consumption, various programs to ed, with a population projection of 110.97 million in improve capture fisheries and aquaculture production 2020, fish consumption would reach 3.5 tons using the were undertaken by the Government’s BFAR through

Table 1: Estimated fish consumption, fish production, and surplus/deficit in the Philippines

Per Capita Fish Total Fish Consumption, Total Fish Production, Surplus/Deficit, Year Consumption, kg/year tons tons tons

1961 23.04 625,881.60 500,047.0 (125,834.6) 1965 25.79 797,246.27 715,638.0 (81,608.3) 1970 33.58 1,202,331.90 1,102,316.0 (100,015.9) 1975 37.40 1,544,470.40 1,466,241.0 (78,229.4) 1980 32.43 1,537,117.14 1,708,683.0 171,565.9 1985 32.87 1,785,662.75 2,048,587.0 262,924.3 1990 35.64 2,207,862.36 2,500,183.0 292,320.6 1995 31.59 2,198,88C.13 2,801,499.0 602,613.9 2000 28.83 2,238,707.16 2,997,051.0 758,343.8 2005 32.75 2,810,637.75 4,165,586.0 1,354,948.3 2010 35.64 3,330,344.16 5,157,735.0 1,827,390.8 2013 31.58 3,107,250.94 4,705,107.0 1,597,856.1 Source: Fish Consumption Data from PSA (2015) and Fish Production Data from FAO (2015). Increased Population and Drive For Economic Growth Pushed For Increasing Fisheries Production In The Philippines 17

Figure 28: Value of fisheries production in Philippine pesos from 1980 to 2014

300

250

200

150

100

50 Value of Production, million PhP 0 1980 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008 2010 2012 2014 Aquaculture Capture Fisheries Total

Source: PSA 2015.

its Ginintuang Masaganang Ani for Fisheries Program This translates to 1.9 percent in 2013, down for 2002–2004, with specific developmental road maps from a peak of 4.9 percent in 1987 at constant prices, for various commodities (BFAR 2015). with an average of 4.0 percent since 1978. This is in line with a sharp drop in the gross domestic product (GDP) contribution starting in 2010 (Figure 29). 2.2 Contribution of Capture Fisheries With regard to gross value added (GVA) contribu- and Aquaculture in Philippine tion, the fisheries sector contributed 18.5 percent in 2013, Economy with a high of 24.4 percent in 2009 (since 1988) and an average of 20 percent at constant prices (Figure 30). The fisheries sector contributed almost PHP 242 mil- On the other hand, fishery exports far exceeded lion in 2014 to the country’s economy (Figure 28). imports with a balance of trade of US$1,086 million

Figure 29: Contribution of fisheries to the Philippines’ GDP

GDP at Constant Price 1

0 1978 1980 1982 1985 1988 1990 1992 1994 1996 1998 2000 2003 2005 2007 2009 2011 2013

Source: BFAR 1978 to 2013. 18 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Figure 30: Contribution of fisheries to GVA at constant prices

5 GVA at Constant Price, %

0 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013

Source: BFAR 1988 to 2013.

in 2013 (Figure 31). Major exports in terms of val- fish farmers worldwide live in Asia. China, India, Indo- ue are tuna, seaweeds, crabs, and shrimps, equivalent nesia, the Philippines, and Vietnam have a significant of 28.91 percent, 9.48 percent, 3.65 percent, and number of fishers and fish farmers (FAO 2008). Most 2.86 percent, respectively, as of 2013 (BFAR 2013). fishers and fish farmers are small-scale, artisanal fishers, Of the three top fish commodities cultured, im- operating on coastal and inland fishery resources. In the port dependency ratio is relatively high for shrimps and Philippines, about a million people are employed in the prawns and low for milkfish and tilapia (Figure 32). fisheries and fish farming sector. Available census data In the last three decades, employment or engage- show that in the 1990s, 990,872 people were under this ment in the fisheries and aquaculture sector has grown sector, which is estimated at 5 percent of the country’s faster than the world’s population and employment in population. Fishermen in the municipal fisheries sec- traditional agriculture. Eighty-six percent of fishers and tor consisted 68 percent (675,677). Those involved in

Figure 31: Comparison of value of exports and imports of fisheries products

45 40 35 30 25 20 15 Value, billion PhP 10 5 0 1977 1979 1981 1983 1985 1987 1989 1991 1993 1995 1997 1999 2000 2001 2003 2005 2007 2009 2011 2013 Exports Imports

Source: BFAR 1977 to 2013. Increased Population and Drive For Economic Growth Pushed For Increasing Fisheries Production In The Philippines 19

Figure 32: Import dependency ratio of three major fish culture commodities

0.18 9 0.16 8 0.14 7 0.12 6 0.10 5 0.08 4 0.06 3 Ration Shrimps

Milkﬁsh and Tilapia 0.04 2 Import Dependency

Import Dependency Ration 0.02 1 0 0 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008 2010 2012 2014 Milkﬁsh Tilapia Shimps and Prawns

Source: PSA 2015. aquaculture and commercial fisheries sectors comprise Those engaged in the culture of milkfish know 26 percent (258,480) and 6 percent (56,715), respec- the profitability of this enterprise. Milkfish aquaculture tively (BFAR 19977–2014). In the 2002 census, the profit margins averaged 110 percent and were in the number of people involved in fisheries increased to range of 63 to 153 percent between 2001 and 2013 more than 1.6 million. There was a marked increase (Figure 33). Production cost remained fairly constant in the number of people employed in the municipal from 2001 in the range of PHP 23.5–39.2 per kilo- fisheries sector at close to 1.4 million people (85 per- gram, while farm gate price tended to increase from a cent), while aquaculture was slightly down to 226,195 low PHP 53.5 per kilogram to a high PHP 87.7 per (14 percent) and the commercial sector further reduced kilogram. to just 16,498 (1 percent) (BFAR 1977–2014).

Figure 33: Production cost, farm gate price, and profit margins for milkfish culture

100 200 90 80 150 70 60 50 100 Proﬁt, %

Cost, PhP 40 30 50 20 10 0 – 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 Production cost per Kg, Ph Farmgate price per Kg, PhP Proﬁt, %

Source: PSA 2015.

APPROACHES TO IMPROVE FISHERIES 3 PRODUCTION RESULTED IN THE VARIOUS IMPACTS AND BECAME SOURCES OF ENVIRONMENTAL PROBLEMS AND POLLUTION

3.1 Conversion of Land and Water Resources for Aquaculture

The spread of aquaculture resulted in the conversion of natural water bodies into husbandry-type production of fish through the establishment of marine cage clusters (as mariculture parks [MPs]) and fish pens and cages in inland water bodies such as lakes and rivers. Land has been excavated and converted into fishponds. 22 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

3.1.1 Conversion of Mangroves to Figure 34: Process of establishment of Fishponds MPs in the Philippines

At least 35 percent of the world’s mangrove forests have Initial environment been lost in the last two decades, which far exceeds the assessment If site is loss of two other significantly threatened environments: Sanguniang suitable tropical rain forests and coral reefs (Valiela, Bowen, and An Executive Bayan/Panglunsod York 2001). Management enacts an ordinance Council manages declaring the area as MP If LGU and Mangrove areas in the Philippines were around the MP BFAR agree 400,000 to 500,000 ha at the turn of the century BFAR and LGU sign a (Brown and Fisher 1918, as cited by Primavera and MOA to develop and Agbayani 1997). This declined to 132,000 ha by 1990 co-manage the MP (Auburn University 1993, as cited by Primavera and Source: Adora 2009. Agbayani 1997). The decrease in mangrove area in the last few decades has been traced back to the conversion of these areas into milkfish and shrimp ponds. infrastructure and equipment that will allow fisherfolk There was only around 61,000 ha of fishponds in the and investors to operate in a cost-effective and secure 1940s. This expanded to 223,000 ha by 1990 (Prima- manner; and (d) promote environment-friendly inputs vera 1994) at the peak of fishpond construction from and farm management practices. mangrove areas, between 1988 and 1990 alone. Initial- A ‘mariculture highway’ in the eastern and west- ly, milkfish monoculture dominated the brackish-water ern seaboard of the country was envisioned to provide a pond system, but the development of culture technol- sustainable strategy to ensure food security from aqua- ogies for the peneid shrimp Penaeus monodon, or black culture and to contribute to the country’s economic tiger shrimp, transformed many of these converted growth. These planned MPs will prevent the unregu- mangrove areas to the culture of this high-value com- lated establishment of mariculture facilities across the modity with excellent export potential. country without regard for the overall sustainability of the industry. Figure 34 shows the process for establish- ing an MP in a designated area. 3.1.2 Establishment of Mariculture Parks Careful site evaluation is done before a site is con- The Philippines’ BFAR spearheaded the establishment sidered for MP development. If the site is found suitable, of MPs in selected coastal areas of the country. The the local Sanguniang Bayan or Sanguniang Panlungsod concept of an MP is similar to the establishment of enacts an ordinance declaring the area as an MP. If the an industrial estate on land where the Government in BFAR and the local government unit (LGU) involved partnership with the local Government and private sec- agree, a memorandum of agreement is signed by the tor puts up the facilities for a managed marine aquacul- BFAR and the LGU to develop and co-manage the MP. ture enterprise. The rationale behind the establishment An Executive Management Council manages the MP. of MPs is to address issues such as declining capture The first MP in the Philippines was established fisheries due to over exploitation, destructive fishing in 2001 in the Island Garden City of Samal in Davao. methods, pollution, and habitat deterioration. The Since then a number of mariculture areas have been de- MP project aims to (a) generate employment and alle- veloped (Figure 35). viate poverty in the countryside; (b) promote marine Table 2 shows the operation of two MPs, one fish culture as an alternative livelihood for marginal- in Panabo and another in San Juanico. Aside from the ized fisherfolk; (c) develop an area with appropriate production and economic benefits of these two MPs, Approaches to Improve Fisheries Production 23

Figure 35: Site of MPs for establishment Table 2: Performance of two MPs in the Philippines Parameter Panabo MP San Juanico MP

Area, ha 1,075 2,700 Fish cages, no. 323 168 Production, tons 1,855.03 3,539.785 Commodity Milkfish Milkfish Jobs generated, no. 425 304 Investors from ancillary 61 178 industry, no. Year of data covered 2006 to 2009 2004 to 2009 Source: Adora 2009.

brackish-water ponds. Milkfish was thought to be an ideal species to utilize the eutrophic lake’s primary productivity since milkfish is an herbivorous species. The first fish pens was established as a pilot project of the BFAR and from a 40 ha pilot area in 1971, expanded to a peak of almost 29,011 ha in 1985 (Delmendo 1987). The initial success of the milkfish culture in Laguna de Bay resulted in the adoption of aquaculture in pens and cages in other inland water bodies in the country. The culture of Nile tilapia and bighead carp (Aristichthys nobilis) in Laguna de Bay and other lakes followed. Source: BFAR website. The infrastructure of fish cages and pens in inland water bodies for aquaculture had adverse impacts on the environment. Cage and pen structures affect fisherfolk in the area noted increased fish recruitment water bodies since (a) they take up space which es- and reduction, if not elimination, in unregulated, il- sentially competes with other uses of the inland water legal, and destructive fishing in the area, probably due body; (b) they alter flow regimes and circulation pat- to active management of the MP and its surrounding tern which in turn affects oxygen, sediment, as well as areas. The total area planned for MP development is plankton and fish larvae; and (c) they adversely alter the 50,150 ha, but only a small portion of this has been aesthetic quality of the area (Beveridge 1984). fully established (Salayo et al. 2012). Enclosures such as pens and cages are a more open-type of fish rearing system than land-based facilities such as ponds, tanks, and raceways; thus, there 3.1.3 Establishment of Inland Water is a greater degree of interaction between cages and Aquaculture Facilities penned fish and the outside environment (Beveridge The declining fish catch in the Philippines’ largest lake, 1984). Nutrients from unconsumed feeds, excreta, and Laguna de Bay, provided the impetus for the intro- the inevitable mortalities inside the pens/cages may di- duction of milkfish culture in fish pens in this lake. rectly affect the aquatic environment, often resulting in Heretofore, milkfish has been primarily cultured in eutrophication. 24 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

3.2 Practices to Prepare and Improve Table 3: Groups of chemicals and additives Culture Environment used in aquaculture

Group Compound/Product Reference With the intensification of aquaculture, the use of Azinphos-methyl a chemicals and other products during different phases Diazinon a of production has become inevitable. Fertilizers, water Trichlorfon c and soil treatment chemicals, disinfectants, antibiotics, Piscicides and pesticides (molluscicides, piscicides, algicides) are Nicotine a, c among the most common groups of compounds used Rotenone a in aquaculture. Table 3 lists these various compounds Saponin (teaseed cake) a, b, c used in Philippine aquaculture. Disinfectants Benzalkonium chloride a Calcium hypochlorite a, c Calcium sulfite a Table 3: Groups of chemicals and additives used in aquaculture Copper complex solution a Formaldehyde b, c Group Compound/Product Reference Iodine a Potassium monopersulfate a Inorganic fertilizers Ammonium phosphate a, c Potassium permanganate a Ammonium sulfate a, c Sodium cyanide c Calcium nitrate a Sodium hypochlorite a Diammonium phosphate c Antibiotics Macrolides Nitrogen, phosphorus and a potassium (NPK) Erythromycin a, b, f, g Organic fertilizers Horse manure c Nitrofurans Chicken manure a, c Furazolidone a, b, c, f Cow manure a, c Nifurpirinol a Molasses (sugar waste) c Quinolones Pig manure a, c Oxolinic acid a, b, f, d, g Urea a, c Sulfonamides Water and sediment Calcium carbonate a, b, c Sulfamethoxazole a Treatment compound Calcium hydroxide a, c Sulfamerazine a Dolomite a, c Sulfadimethoxine a Sodium thiosulfate a Tetracyclines Zeolite a Tetracycline a Pesticides Fungicides Doxycycline a Fentin acetate c Oxytetracycline (OTC) a, b Malachite green a Others Trifluralin a Chloramphenicol a, b, e, f, g Herbicides Nalidixic acid a 2,4-Dichlorophenoxyacetic a Rifampicin a acid Trimethoprim a Insecticides Source: Rico et al. 2012, © Wiley Publishing Asia Pty Ltd; Sapkota et al. 2008, Organochlorine (c) Elsevier. Reproduced with permission from publishers; further permission required for reuse. Endosulfan a, c Note: a - Cruz-Lacierda, dela Peña and Lumanlan-Mayo 2000; b - Tendencia and de la Peña 2001; c - Cruz-Lacierda et al. 2008; d - Inglis et al. 1997; e - Graslund and Organophosphate Bengtsson 2001; f - Primavera 1993; g - Primavera et al. 1993. Approaches to Improve Fisheries Production 25

3.2.1 Application of Fertilizers and Other (Cruz-Lacierda, de La Pena, and Lumanlan-Mayo 2000) Chemicals and in 2006–2007 (Cruz-Lacierda et al. 2008). Asia has a long history of organic and inorganic fertil- Organic fertilizers, mainly animal manure, is izer use in pond culture. Often, in extensive systems, also widely used in Philippine aquaculture. A wide va- fertilizers are the only input, most especially in small- riety of animal waste and their combination is used. scale, single pond operation. Almost all extensive and Chicken manure is the most widely used and as per semi-intensive aquaculture, with few exceptions, rely survey results between 2006 and 2007, 85 percent of on fertilizers and manure (de Silva and Hassan 2007). the 39 respondents use this organic fertilizer for their The Philippines imports most of its fertilizer needs as milkfish ponds while none of the 40 respondents en- self-sufficient supply is only available for diammonium gaged in shrimp culture use this organic fertilizer. phosphate. Chicken manure is the most readily avail- Cow and carabao manure are also used by 3 percent able and therefore the most commonly used organic of respondents for milkfish and 13 percent of respon- fertilizer. Low-cost, unprocessed organic fertilizers are dents for shrimp culture. Horse manure is used by only preferred by Philippine aquaculture operations, but 3 percent of the respondents for shrimp culture while the use of compost has also become popular. The Phil- pig manure is used by 5 percent of respondents for the ippine Government has strongly supported the fertil- polyculture of milkfish and shrimp (Cruz-Lacierda et izer industry with its deregulation in 1986 to encour- al. 2008). Table 5 shows a summary of the organic fer- age the entry of more traders. Quality assurance and tilizers used in aquaculture from two survey periods: monitoring, price control, and incentives are being 1996–1997 (Cruz-Lacierda, de La Pena, and Luman- implemented in line with the Agriculture and Fisheries lan-Mayo 2000) and 2006–2007 (Cruz-Lacierda et al. Modernization Act (AFMA) under Republic Act 843C 2008). With regard to use of organic fertilizers, there is (Sumagaysay-Chavoso 2007). a large increase in the rate of application for both the In pond culture, inorganic and organic fertiliz- pond preparation phase based, for example, for chicken ers are applied in extensive and semi-intensive systems manure, from 0.5 to 3 tons/ha in 1995–1996 to 1–10 to stimulate growth of natural food. In extensive pro- tons/ha in 2006–2007 for milkfish culture. duction systems, application of fertilizers allows for the Aside from fertilizers, there are other chemicals growth of natural food in sufficient quantity to com- used in the preparation of ponds before stocking to pletely do away with commercial feeds. Extensive sys- improve soil and water quality. These chemicals act as tems require heavy inputs of fertilizers since the growth soil or water conditioner. Lime is applied to adjust the of natural food should be sufficient to support fish pH of the pond soil to neutral or alkaline to promote growth, while semi-intensive and intensive systems re- volatilization of ammonia. Lime is also a disinfec- quire less fertilizers since the cultured fish are provid- tant. Application is broadcasting on dried and caked ed with formulated feeds (Cruz-Lacierda et al. 2008). pond bottom. Commonly used types of lime in pond Monoammonium phosphate (16-20-0), diammonium preparation are agricultural lime (CaCO3), hydrated phosphate (18-46-0), urea (46-0-0), and ammonium lime (Ca(OH)2), and dolomite (MgCO3). For soils sulfate (21-0-0) are the most widely used fertilizers in with very low pH and for new ponds, hydrated lime Philippine aquaculture. In combination with lime, am- is the choice, while agricultural lime is for old ponds monium sulfate is also used to kill unwanted species as (Cruz-Lacierda et al. 2008). To a limited extent some part of pond preparation before stocking. Table 4 shows farmers even use liming to kill potential pests and the use of various organic fertilizers in milkfish (Chanos predators. To remove ammonia and other nitrogenous chanos) and peneid shrimp (Penaeus monodon) ponds in compounds, zeolite is applied (Rico et al. 2012). Many the Philippines based on results of surveys in 1995–1996 of these water and soil conditioning chemicals have 26 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Table 4: Application of inorganic fertilizer in shrimp Penaeus monodon and milkfish Chanos chanos ponds for the period surveyed in 1995–1996 and 2006–2007

Fertilizer Commodity/Phase 1995–1996 2006–2007

Monoammonium phosphate (16-20-0) Shrimp/pond preparation (broadcast) 4–100 kg/ha 9–100 kg/ha Shrimp/rearing phase (periodic broadcast) 150–300 kg/ha — Milkfish/pond preparation 100–300 kg/ha 40–240 kg/ha Milkfish/rearing phase 3.2 kg/ha 20–100 kg/ha (every 15 days till harvest) Diammonium phosphate (18-46-0) Shrimp/pond preparation 3.2–50 kg/ha 3–120 kg/ha Shrimp/rearing phase 0.6–20 kg/ha Milkfish/pond preparation Broadcast 50–150 kg/ha 40–240 kg/ha Milkfish/rearing phase — 6–10 kg/ha NPK (14-14-14) Shrimp/pond preparation 7.5–15 kg/ha 10–20 kg/ha Shrimp/rearing phase 3 kg/ha — Milkfish/pond preparation Broadcast — 20–40 kg/ha Milkfish/rearing phase broadcast — — Urea (46-0-0) Shrimp/pond preparation 5–120 kg/ha 10–100 kg/ha Shrimp/rearing phase 3.2–5 kg/ha 4–5 kg/ha Milkfish/pond preparation Broadcast 25–200 kg/ha 40–150 kg/ha Milkfish/rearing phase broadcast 12 kg/ha 5–100 kg/ha (every 15 days till harvest) Solophos (0-20-0) Shrimp/pond preparation 3–20 kg/ha — Shrimp/rearing phase 5–10 kg/ha — Ammonium sulfate Shrimp/pond preparation 100–500 kg/ha 10–100 kg/ha (21-0-0) Shrimp/pond preparation (broadcast) 3–50 kg/ha — Calcium nitrate Shrimp/rearing phase (broadcast) 5–10 kg/ha — Source: Cruz-Lacierda, de La Pena, and Lumanlan-Mayo 2000; Cruz-Lacierda et al. 2008.

short environmental life and are relatively harmless, al- chemical agents are applied to kill fish and molluscs in though they do affect water quality. Table 6 shows the the pond bottom. Table 7 shows some of the common application rates for some of these chemicals in pond piscicides and molluscicides in aquaculture ponds. preparation.

3.3 Practices to Improve Production 3.2.2 Application of Piscicides and Molluscicides 3.3.1 Use of Hormones and Growth Typical for pond preparation before stocking any com- Promoters modity for culture is the eradication of other fish species Exogenous hormones, particularly gonadotropins, have and molluscs which may prey on the cultured species been used for years to induce final maturation of captive or compete for food, oxygen, and space in the culture female broodfish. Hormone products such as lutein- environment. As a routine part of pond preparation, izing hormone releasing hormone-analog (LHRHa), Approaches to Improve Fisheries Production 27

Table 5: Summary of organic fertilizers used in milkfish and shrimp ponds and in polyculture of these two commodities

Year Organic Fertilizer Milkfish Shrimp Polyculture

1996–1997 Chicken manure 500–3,000 kg/ha 100–3,000 kg/ha — (pond preparation, broadcast (pond preparation; tea bags) 200 kg/ha (rearing, tea bags) 100–1,000 kg/ha (rearing phase; tea bags) — Goat/pig manure 500–1,000 kg/ha — — (pond preparation, broadcast) BioearthTM 500 kg/ha — — (pond preparation, broadcast) Cow manure — 100–500 kg/ha (pond preparation; tea bags) — — 100–200 kg/ha (rearing phase; tea bags) — Carabao manure — 240–300 kg/ha (pond preparation; tea bags) — — 100–200 kg/ha (rearing phase, tea bag) — VIMACATM (Chicken/ — 1,000 kg/ha (pond preparation; tea bags) — pig manure) 2006–2007 Chicken manure 1–10 tons/ha — 0.5–10 tons/ha (pond preparation) (pond preparation) 0.1–1.5 tons/ha — — (rearing phase) Cow/carabao manure 2.5 tons/ha (pond preparation) 50–250 kg/ha (pond preparation) — Mud press (sugar mill) 6 tons/ha (pond preparation) — — Horse manure 16 kg/ha (pond preparation) Pig manure — — 1 ton/ha Source: Cruz-Lacierda, de La Pena, and Lumanlan-Mayo 2000; Cruz Lacierda et al. 2008.

human chorionic gonadotropin (HCG), and other have been used in the Philippines for commodities hormone containing products such as OvatideTM and such as milkfish, sea bass, bighead carp, catfish, grou- OvaprimTM (both are a combination of gonadotropin pers, and many other species (Kungvankij et al. 1986; and a dopamine antagonist). Hormones such as these Tan-Fermin and Emata 1993; Liao et al. 1979; Marte et

Table 6: Use and dosage of other chemicals to modify soil or water quality for aquaculture of milkfish and shrimp and polyculture of the two species

Year Chemical Milkfish Shrimp Polyculture

2006–2007 Agricultural lime 0.2–6 tons/ha 1–10 tons/ha; 1–5 tons/ha; (CaCO3) 200–300 kg/ha (rearing phase) 140–400 kg/ha (rearing phase) Hydrated lime 0.2–2 tons/ha 0.4–2 tons/ha; 0.75–1.5 tons/ha; (Ca(OH)2) 50–200 kg/ha (rearing phase) 200–300 kg/ha (rearing phase) Dolomite (MgCO3) 40–600 kg/ha 100–200 kg/ha/week 250 kg/ha 1996–1997 Agricultural lime 300–500 kg/ha — — Hydrated lime 150–1,000 kg/ha — — (Source: Cruz-Lacierda, de La Pena, and Lumanlan-Mayo 2000; Cruz Lacierda et al. 2008) 28 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Table 7: Application of common piscicides and molluscicides in milkfish and shrimp culture and polyculture of these two commodities

Year Chemical (active ingredient) Milkfish Shrimps Polyculture

2006–2007 Teaseed (saponin) 10–50 kg/ha 1C–30 kg/ha 20–25 kg/ha Brestan 60 (triphenyltin acetate) 0.25–1.5 kg/ha — 0.25–0.75 kg/ha Sodium cyanide 0.5–6 kg/ha — 1–6 kg/ha Tobacco dust (nicotine) 500–1,500 kg/ha — Thiodan (endosulfan) 0.1 ppm — 0.1 ppm D-crab (pyrethroid) — 1 liter/ha — Clear 97 (trichlorfon) — 20 kg/ha — 1996–1997 Teaseed (saponin) 5–400 kg/ha — — Tobacco dust (nicotine) 400 kg/ha — — Derris root (Rotenone) 300–800 kg/ha — — Brestan (organotin) 250–600 kg/ha — — Gusathion 0.1 ppm — — Source: Cruz-Lacierda, de La Pena, and Lumanlan-Mayo 2000; Cruz Lacierda et al. 2008.

Table 8: Sample of hormone dosage used growth rather than reproduction (Chakraborty et al. for induced spawning of the Asian 2011). The hormones 17-α-methyltestosterone (MT) catfish Clarias microcephalus and and estradiol-17β are the most common hormones for bighead carp Aristichthys nobilis masculinization and feminization, respectively (Pan- dian and Sheela 1995). In the Philippines, the most Hormone Catfish Bighead Carp common species that undergo sex reversal through HCG 4 IU/g body weight 2,000 IU/kg BW (female); hormone treatment of MT are tilapia. Since the mid- (BW) 1,000 IU/kg BW (for male) 1980s commercial-scale sex reversal, mainly masculin- LHRHa 0.05 μg/g BW 20–50 μ g/kg BW (female); 10–25 μ g/kg BW (male) ization, through MT treatment has been practiced in OvaprimTM 0.5 μ L/g BW 0.5 ml/kg BW (female); many tilapia-producing countries including the Philip- 0.25 ml/kg BW (male) pines (Popma and Green 1990). Diets are mixed with OvatideTM 0.2 μ L/g BW 0.5 ml/kg BW (female); MT at 10 mg/kg at a rate of 15–20 percent of BW 0.25 ml/kg BW (male) per day of tilapia for 20–30 days (Popma and Green Source: Tan-Fermin et al. 2008; Gonzal et al. 2001. Note: OvaprimTM and OvatideTM are commercial preparations containing LHRHa and 1990; Chakraborty et al. 2011). After this method, domperidone. 97–100 percent phenotypically male tilapia can be achieved and ready for grow-out. al. 1987; Fermin 1991; Almendras et al. 1988). Table 8 shows the dosage of various hormones used for induced breeding of catfish and bighead carp induced spawning. 3.3.2 Use of Anesthetics Another use of hormones in aquaculture is for Anesthetics are employed in fisheries and aquaculture in sex reversal, either for masculinization or feminization. instances when the fish need to be transported or han- The culture of monosex fish has been shown to improve dled, which is stressful to the fish. Stress can result in growth compared to mixed sex culture since a greater immunosuppression, physical injury, and even death portion of energy in feed is channeled toward somatic to the fish. During transport, anesthetics are used to Approaches to Improve Fisheries Production 29

Table 9: Common anesthetics and dosage used in common aquaculture species found in the Philippines

Anesthetics Common Carp Nile Tilapia Catfish Milkfish

MS-222 100–250 mg/L a 100–200 mg/La — — Benzocaine — 2C–100 mg/La — — Quinaldine 10–40 mg/La 2C–50 mg/La — — 2-Phenoxyethanol 400–600 mg/La 400–600 mg/La 0.75 mg/Lb (fingerlings); 125 mg/Ld 0.5 ml/Lc (brood stock) Clove oil 40–100 mg/La — — — Ethylene glycol — — — 125 mg/Ld Note: a - Coyle, Durborow, and Tidwell 2004; b - Öğretmen and Gökçek 2013; c - Tan-Fermin et al. 2008; d - Reyes et al. 2015. reduce metabolism which in turn reduces oxygen con- MS-222 is registered for use in food fish and requires sumption and excretion rates (Coyle, Durborow, and a 21-day withdrawal period (Coyle, Durborow, and Tidwell 2004; Strange and Shreck 1978). Immersion in Tidwell 2004). Thus far, there is no such list of approved anesthetic bath is the most common way anesthetics are anesthetics for use in aquaculture in the Philippines. applied to fish and crustaceans. For large-size fish, the anesthetic solution may be sprayed to the gills. The anesthetic is absorbed through the gills and enters the blood 3.4 Practices to Improve Aquatic stream to take effect on the fish. Table 9 is a list of com- Animal Health mon anesthetics and their dosage for various aquaculture commodities. Environmental and human safety regula- 3.4.1 Use of Antibiotics and Antimicrobials tions on the use of anesthetics in aquaculture are not yet Antibiotics and antimicrobials are generally substances in place in the Philippines. In the United States, only that kill or suppress the growth of microorganisms.

Table 10: Antibiotic feed additives and their use and dosage as applied to shrimp culture

Chemical Group (Commercial Product) Pattern of Use Amount Used

Chloramphenicol DOC 1–30 days 3 g/kg feed Disease control 2–2.5 g/kg feed Tetracycline (OTC) DOC 1–30 3 g/kg feed Disease control, 3 times/day for 3–7 days 3 g/kg feed Oxolinic acid DOC 12–60, 1-3 times/day 1 g/kg feed Disease control, 1-3 times/day for 7 days 0.2–4 g/kg feed Furazolidone (Furazolidone, 98%) DOC 1–100, 5 times/day 1 g/kg feed Furazolidone (PE-30) Disease control 1–35, alternate with vitamin/wk, all feedings for 1–2.5 g/kg feed 5–7 days 20 g/kg feed Furazolidone (PE-40) Disease control, 2–3 times/d for 5–7 days 20 g/kg feed Furazolidone (PE-60) DOC 1–30, alternate with PE-30 4–5 times/day 20 g/kg feed Source: Cruz-Lacierda, dela Pena, and Lumanlan-Mayo 2000. Note: DOC – days of culture. 30 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Table 11: Disinfectants used in black tiger Figure 36: Number of aquatic animal shrimp brackish-water farms in species introductions in the the Philippines in 2006–2008* Philippines in the various decades Chemical Shrimp (n = 40) Polyculture (n = 21) 60 Calcium hypochlorite 5–100 ppm (33%) 25–50 ppm (10%) Formalin 5–20 ppm (10%) — 50 Source: Cruz-Lacierda et al. 2008. 40 Note: * Values in parenthesis are percentage of farms surveyed; n=number of farms surveyed. 30

20 Antibiotics are substances produced by or derived from Introduced with Records specific microorganisms and can destroy or inhibit the Number of Exotic Species 10 growth of pathogenic organisms and prevent or treat 0 infection. The use of antibacterial treatment in aquaculture became widespread in the 1970s when bacterial 1900s 1910s 1920s 1930s 1940s 1950s 1960s 1970s 1980s 1990s 2000s pathogens became increasingly prevalent in aquacul- Source: Cagauan 2007. ture. However, antibacterial chemotherapy has been in practice for over 60 years, using sulphonamides to treat furunculosis in trout and tetracyclines against also in other shrimp-producing countries. To address gram-negative pathogens (Inglis 2000). Method of the problem of Vibrio infection, it has become a prac- dosing of these antibiotics may be through (a) immer- tice to disinfect inflowing water in some shrimp farms. sion or water bath; (b) injection; (c) topical applica- Chlorine (as calcium hypochlorite) or formalin is used tion; or (d) incorporation as a feed ingredient. The last to treat the water in reservoirs before use in the shrimp is the more common approach particularly for shrimp ponds (Cruz-Lacierda et al. 2008). Table 11 shows the culture. With the intensification of shrimp culture, dosage of disinfectants used in monoculture shrimp fueled by its attractive price not only locally but more ponds and in polyculture with milkfish. so in the international market, problems with shrimp diseases causing high mortalities need to be addressed to maintain production volume. Antibiotics and anti- 3.5 Practice to Diversity Cultured microbial agents became the drug of choice to address Commodities disease problems. 3.5.1 Introduction of Exotic Aquatic Species 3.4.2 Use of Chemotherapeutants New aquatic species from other countries are introduced As aquaculture operations intensified, disease occur- to boost both capture fisheries and aquaculture produc- rence from pathogenic organisms became a threat to tion. Figure 36 shows the recorded number of intro- production. These chemicals or drugs are selectively duced exotic species in the Philippines since the early toxic to the causative agent of the disease. For instance, 1900s. An estimated 45 percent of fish introductions are in shrimp culture, the prevalence of the luminous bacte- for aquaculture (food fish) purposes and 42 percent for ria Vibrio has resulted in the devastation of many farms the ornamental fish industry, 6 percent for recreational in the country, eventually resulting in the sharp decline fishing, 6 percent for mosquito control (Guerrero 2014), in shrimp production not only in the Philippines but and the remaining are probably incidental introductions Approaches to Improve Fisheries Production 31

Table 12: Partial list of invasive and potentially invasive introduced species to the Philippines

Species Origin Reason for Introduction

Arapaima gigas (Arapaima) South America Ornamental Channa striata (mudfish) Malaysia Culture Channa micropeltes (Giant snakehead) Thailand Ornamental Chitala (Clown knife fish) Thailand Ornamental Chitala ornata (Clown featherback) Thailand Ornamental Clarias batrachus Thailand Culture Monopterus albus Malaysia Culture Parachromis managuensis (Jaguar guapote) Central America Ornamental Pterygoplichthys disjunctivus (vermiculated sailfin catfish) South America Ornamental Pterygoplichthys pardalis (Amazon sailfin catfish) South America Ornamental Pygocentrus nattereri (red-bellied piranha) South America Ornamental Sarotherodon melanotheron (black-chinned tilapia) Unknown Ornamental Source: Guerrero 2014.

as ‘tag-along’ species. The peak of introduction of exotic carp, Aristichthys nobilis, introduced from Taiwan in fish species in the country was in the 1970s with more 1968 (Guerrero 2014). Table 12 shows a list of some than 50 species introduced (Cagauan 2007). species introduced to the Philippines, either as food fish Introduction of exotic species is the second lead- or for the ornamental fish industry, that have become ing cause for the loss of biodiversity, after habitat de- invasive or have the potential to become invasive. struction (Williams et al. 1989; IUCN 1999). Many fish species introduced for aquaculture have proven to be economically beneficial to many farming communi- 3.5.2 Translocation of Aquatic Species ties in the world, including the Philippines. Among the Even native fish species are not immune from being top freshwater species being farmed in the Philippines introduced to other bodies of water where they are is an introduced species, the Nile tilapia Oreochromis not part of the native population. The translocation niloticus. Although many countries consider the intro- of native species from one drainage system to another duction of this species as a nuisance and consider the in the same country is a widely accepted method for species to be invasive (Linde-Arias et al. 2008; Angien- enhancement of many natural waters around the world da et al. 2011), many more countries have accepted this (Innal and Erk’akan 2006). This may either be inten- species as an important aquaculture commodity. tional or unintentional. Translocation may be a way of One of the early records of fish introduction to enhancing fisheries productivity. An example of inten- the Philippines was in 1915 with the release of com- tional introduction is the case of milkfish Chanos chanos mon carp (Cyprinus carpio) from Hong Kong in Lake in Laguna de Bay for the fish pen culture industry. Milk- Lanao in Mindanao (Villaluz 1966; Escudero 1994). fish is a marine species but with euryhaline characteris- Fortunately, this species did not thrive well and is now tics that enable it to be cultured in a variety of aquatic considered nearly decimated in this lake. Another cy- environments, from marine cages to brackish-water prinid which has grown in importance to freshwater ponds to freshwater fish pens (Bagarinao 1999). The aquaculture, especially in Laguna de Bay, is the bighead commodity is continuously being produced in a wide 32 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

range of culture environments, including other lakes overfishing in the country’s reefs, not for food but for in the country, because this is a preferred food fish for the production of mother-of-pearl buttons. It has been Filipinos. declared as a threatened species in the country. Encour- Translocation may also be a method to conserve aging results in the translocation of wild juveniles of critically overexploited aquatic commodities, as in the Trochus niloticus into other sites proved to be a prom- case of the reef gastropod Trochus niloticus in the Phil- ising strategy for the conservation of this endangered ippines. This species’ population has dwindled due to species (Dolorosa, Grant, and Gill 2013). PHYSICAL IMPACTS 4

4.1 Environmental Impacts

4.1.1 Loss of Ecosystem Services Due to Conversion of Mangroves to Aquaculture Ponds It is estimated that 50 percent of mangrove loss is attributable to its conversion to fishponds. Figure 37 illustrates the relationship between the loss of mangroves and the growth of brackish-water ponds in the Philippines until 1990. According to a review by Primavera (1995), the conversion of mangroves into ponds proceeded at a slow pace of about 760–1,200 ha/year up to 1940 since there

Figure 37: The loss of mangrove areas and the development of brackish-water ponds in the Philippines

60 ha)

3 50

10 Mangrove/Pond area (x 10 0 1920 1940 1945 1950 1955 1960 1965 1970 1975 1980 1985 1990

Culture Pond: Gov’t. – Leased Privately – Owned

Source: Primavera 1991; Primavera 1995. 34 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

was no active government support. Upon the creation of 4.1.2 Eutrophication the BFAR in the late 1940s, funds for pond construction Eutrophication results from the heavy inputs of nutri- became available (mainly through international loans). ents in the aquatic environment, mainly from uncon- Mangroves were considered ‘valueless land’ (as quoted sumed feeds, aquatic animal wastes, and other inputs from Carbin 1948 as cited by Primavera 1995) at that into the aquatic system to boost production. A study time and conversion to brackish-water milkfish pond was on nitrogen and phosphorus utilization of formulated deemed a more useful alternative. Thus began the accel- feeds under controlled laboratory conditions shows erated conversion of mangroves to brackish-water ponds that an equivalent of only 33 percent of nitrogen and at a rate of 5,000 ha/year in the 1950s and 1960s. Con- 29 percent of phosphorus is retained in fish (as bio- version slowed down to 800 ha/year in the 1970s when mass) and the rest is lost through fecal and urinary mangrove areas were placed under the joint jurisdiction of excretion (Cuvin-Aralar 2003). Since this was done in the fisheries and forestry bureaus and there was a move to- the laboratory, the feed ration was visibly consumed by ward conservation. As the technology for shrimp culture the fish with some unquantified, but considered, minor developed, more mangroves were converted into ponds. nutrient losses through leaching. The host of ecosystem services provided by man- Feed conversion rates vary with species, feeding groves which turned out to be far more valuable was left strategy, and feeding management. Overfeeding results in unaccounted for during the initial period of conversion high feed conversion ratios (FCRs) with excess nutrients into ponds. It was only with the establishment of set entering the culture environment as organic sediments or parameters for valuation of various ecosystem services dissolved nutrients in the water column. Nitrogen and that it now has become apparent that mangroves, left phosphorus loading rates from one ton of shrimp harvest as is, have far more economic, environmental, and bio- have ranged from 10 to 117 kg of nitrogen and 9 to 46 kg logical benefits than converting them to fishponds, and of phosphorous, depending on FCR (White et al. 2008). not the ‘valueless land’ they were deemed to be. Table 13 shows model estimates of amounts of nitrogen Mangrove ecosystem-derived services include and phosphorus released to the aquatic environment (a) interception of land-derived nutrients, pollutants, from aquaculture as a function of FCR. and suspended matter before these reach deeper water David et al. (2009) documented the increasing (Tam and Wong 1999); (b) export of materials that nutrient flux in sediment cores from aquaculture activi- support nearshore food webs including shrimps (Sase- ties in a number of marine aquaculture sites in the Phil- kumar et al. 1992); (c) protection of vulnerable coastal ippines: Honda Bay and Malampaya Bay in Palawan, areas from storm surges that have recently destroyed local communities in the country (Kathiresan and Ra- jendran 2005; Alongi 2008); (d) prevention of coast- Table 13: Estimated organic matter and nutrient loading for one ton of al erosion through sediment stabilization (Marshall harvested shrimp released at 1994); and (e) nursery and spawning areas for a variety different FCRs of commercially important fish, shellfish, and molluscs (Sasekumar et al. 1992). With the loss of mangroves, Organic matter Nitrogen Phosphorus important subsidies to subsistence uses and ecological, FCR kg/ton kg/ton kg/ton economic, and conservation uses are also lost. It is in- 1 500 26 13 teresting to note that the decrease in mangrove areas in 1.5 875 56 21 various countries is inversely correlated with an increase 2 1,250 87 28 in GDP but not generally correlated with population 2.5 1,625 117 38 (Valiela, Bowen, and York 2001). Source: Asian Shrimp Culture Council 1993, as cited by White et al. 2008. Physical Impacts 35

Table 14: Comparison of phosphorus An indirect impact of eutrophication is mass fish values from marine aquaculture kill. Mass fish kill is a common occurrence in aqua- sites in the Philippines culture operations in the Philippines and has incurred huge financial losses for the aquaculture investor. In La- Site Characteristics P-range, ppm guna de Bay, 60 percent of mass fish mortalities record- Malampaya Capture fisheries; shellfish 15–85 ed between the 1970s and the late 1990s were attribut- Sound culture ed to low dissolved oxygen, secondary to massive algal Honda Bay Less aquaculture development 22 (average) Manila Bay 39 km2 of fish cages 20–60 bloom due to eutrophication (Cuvin-Aralar 2001). The cause of massive algal bloom is excess nutrients in the Bolinao Bay 1,100 fish cages (milkfish) 20–90 lake, which in turn is due to eutrophication as has been Milagros Bay Developing aquaculture site; 15–40 mainly shellfish discussed in the previous section. More recent incidents Baseline Value 15–20 of mass fish kills in different regions of the country were Source: David et al. 2009. also documented by the BFAR from 2005 to 2014 (Bantaya, pers.comm.). Of the more than 300 incidents of mass fish kills, almost 40 percent were because Manila Bay, Bolinao in Pangasinan, and Milagros Bay of poor water quality due to dissolved oxygen depletion in Masbate. The sites have varying degrees of aquacul- and elevated ammonia. A number of instances of oxy- ture activity. Results show a narrow concentration range gen depletion were due to algal blooms. Interestingly, a for nitrogen from older core samples when compared few incidents of mass fish mortalities were also reported to newer ones. On the other hand, phosphorus showed as being caused by agricultural pollution run-offs into significantly higher levels in younger or more recently inland waters with aquaculture activities. In Bolinao, deposited sediments. Sediments deposited years ago and Pangasinan, an important site for milkfish aquaculture, older had 20 ppm phosphorous. On the other hand, a the site has experienced environmental changes due to 2–3-fold increase in phosphorous levels was noted in these mariculture activities which release organic mat- sediments deposited within the last 15 years. Phospho- ter from unconsumed feed and fecal material that ac- rous sediment profiles reflected the intensity of aqua- cumulate in the sediment. A massive fish kill incident culture activities in the different sites. Honda Bay and in 2002 occurred in the area associated with the bloom Malampaya Sound in Palawan are sites where aquacul- of a dinoflagellate, accompanied by a <2 mg/l dissolved ture activities had lower aquaculture intensity. Manila oxygen level. Increase in nutrient levels over a 10-year Bay has about 39 km2 of fish cages which are adjacent to period (1995–2005) in the area has been reported (Mc- urban centers. Bolinao has more than 1,100 fish cages, Glone et al. 2008). Ammonia has reportedly increased mainly milkfish (Chanos chanos), and Milagros Bay is by 56 percent, nitrite by 35 percent, nitrate by 90 per- a developing aquaculture site with shellfish as the ma- cent, and phosphate by 67 percent as the waters became jor product. Phosphorous concentrations in these sites increasingly eutrophic. ranged from 10 to 90 ppm. Table 14 summarizes the Taal Lake has multiple uses and benefits such as phosphorous values obtained for the study sites. for open water fisheries, commercial aquaculture, recre- A study is currently being undertaken by the ational activities, navigation routes, and water source. National Fisheries Research and Development Institute Of particular interest are immense aquaculture activities (NFRDI) on nutrient buildup from aquaculture ponds in the lake that started in the 1980s through which ti- in the provinces of Bulacan, Bataan, Cavite, and Pam- lapia (Oreochromis niloticus) and milkfish (Chanos cha- panga and the National Capital Region, all surround- nos) culture was introduced (Papa and Mamaril 2011). ing Manila Bay. The proliferation of fish pens and cages has affected the 36 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

water quality of the lake. It is estimated that 64 percent erodes the thermal stratification of the water column of the nitrogen and 81 percent of the phosphorus con- (Balistrieri et al. 2006; Caliro et al. 2008; Marti-Car- tents of fish feed are released into the lake environment dona et al. 2008). In combination with the pressure of (Edwards 1993). Yambot (2000) calculated that for ev- strong winds, mixing of water occurs. This transports ery 1.5 tons of fish feed given, 16 kg of phosphorus is the low dissolved oxygen and reduced chemical sub-

released into Taal Lake waters. Further, the excess fish stances such as hydrogen sulfide (H2S), nitrite (NO2),

feed and fish feces contribute to the increased organic and ammonia (NH3) from the lake bottom to the wa- material that settles at the bottom of the lake. Decom- ter surface, as well as mixes them in localized portions position of this organic matter releases hydrogen sulfide of the lake. The lake then goes into a state of hypoxia

(H2S) and other toxic gases (White et al. 2008). characterized by low dissolved oxygen, that is, below Significant fish kill occurrences in Taal Lake 2 mg/L. This undesirable water quality subsequent to have created major economic setbacks in the area. One lake overturn triggers fish kills in Taal Lake. noteworthy incident was the 2011 massive fish kill that disrupted the socioeconomic activities in the lake, with recorded losses of approximately PHP 140 million. The 4.1.3 Contamination from Toxic and event was attributed to an interplay of factors such as Hazardous Substances of Aquatic lake overturn, water pollution, change in season (that Products is, from summer to rainy season), changes in wind A survey of specifically selected antibiotic and pesticide stress, and intermittent rainfall (BFAR 2011). residues in Philippine aquaculture and fishery prod- From 1998 to 2011, lake overturn and pollution ucts was conducted recently by Coloso, Catacutan, and are the major causes of reported fish kill in Taal Lake Arnaiz (2015) from samples of tilapia, milkfish, sea bass, (Figure 38) (Magcale-Macandog et al. 2013). Increase snapper, grouper, rabbitfish, carp, catfish, silver perch, in wind turbulence and low atmospheric temperature tiger shrimp, white shrimp, and freshwater prawn. Some cools the lake water surface layer (epilimnion) and of the sampled fish tested positive for the antibiotic

Figure 38: Occurrences of fish kill in Taal Lake due to various factors including lake overturn, population, oxygen depletion, sulfur upwelling, and timud infestation based on BFAR announcements and reports from 1998 to 2011

200 3.0 180 160 2.5 140 2.0 120 100 1.5 80 60 1.0 40 Wind velocity (mps) Wind direction (degrees) 0.5 20 0 0 0 5 0 15 20 25 30 35 40 45 50 55 60 Wind direction Fish kill due to pollution Wind velocity Fish kill due to lake overturn Fish kill due to timud infestation Fish kill due to oxygen depletion Fish kill due to sulfur upwelling

Sources: BFAR and PAGASA; Graph by Magcale-Macandog et al. 2013. Physical Impacts 37

OTC and oxalinic acid (OXA) as well as for organo- MRL (0.005). Endrin ketone (0.02582 ppm) was also chlorine pesticides (OCP) for both high-value and low- detected from the same prawn sample, although no PEL value fish commodities. OXA and OTC were the most and MRL is as yet established (Table 15). common antibiotic residues found and methoxychlor for OCP from Luzon, Visayas and Mindanao. OXA in Penaeus vannamei sample from Mindanao was found 4.2 Impact of Diversification of Culture to exceed the maximum residue limit (MRL, based on Commodities through Species Japan Food Chemical Research) and Permissible Expo- Introductions sure Limit (PEL, based on the Occupational Safety and Health Administration based in the United States). In 4.2.1 Effects on Biodiversity one sample of freshwater prawn Macrobrachium species Introduction and/or translocation of aquatic organisms from Luzon, the level of Endosulfan I (0.0144 ppm) primarily affect biodiversity in localities of introduc- was considered harmful based on PEL (0.00642) and tion. There are examples of invasive species altering the

Table 15: Level of OTC, OXA, and OCP in fish samples from the Philippines

Residual Analysis Report No. of No. of (+) Aquatic Product Samples Samples OTC OXA OCP

Luzon Silver perch 1 1 No sample No sample 0.00074 (Heptachlor epoxide isomer B) 0.00093 (Endrin) Milkfish 10 1 — — 0.00680 (Methoxychlor) Manila sea catfish 1 1 — — 0.00353 (Endrin) (kanduli) 0.00255 (4-4’DDT) 0.03255 (Methoxychlor) Freshwater prawn 1 1 No sample No sample 0.014440 (Endosulfan (Endosulfan) (Macrobra-chium species) 0.02582 (Endrin ketone) Shrimp (Penaeus monodon) 1 1 — — 0.00124 (trans-Chlordane) Nile tilapia 9 1 — 0.00496 0.27146 (Methoxychlor) Red tilapia 2 1 — — 0.27425 (Methoxychlor) Visayas Milkfish 12 1 — 0.00830 0.01745 (Heptachlor) 0.03307 (Methoxychlor) Grouper 2 1 — 0.02004 — Shrimp (Penaeus monodon) 5 1 2.51844 — 0.00240 (Endosulfan II) 0.00345 (Endosulfan sulfate) Mindanao Milkfish 5 1 0.04046 0.01006 0.03828 (Methoxychlor) 0.00187 (Aldrin) Shrimp (Penaeus vannamei) 1 1 0.78121 — — Source: Modified from Coloso, Catacutan, and Arnaiz 2015. Notes: 1. Samples of goby, bighead carp, common carp, snakehead, and siganid from Luzon; sea bass, siganid, snapper, and tilapia from Visayas; sea bass, shrimp Penaeus monodon, siganid, snapper, and tilapia from Mindanao were negative for OTC, OXA, and OCP and were not included in the list. 2. Values in bold font exceed the PEL and MRL 38 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector evolutionary pathway of native species by competitive (Cuvin-Aralar 2014). Figure 38 illustrates the direct and exclusion, niche displacement, hybridization, introgres- indirect impact of introduced species on biodiversity. sion, predation, and ultimately extinction (Mooney and Cleland 2001). Introduction of new pathogens along with the exotic species is also a risk of species introduc- 4.2.2 Other Impacts of Introduced Species tion (Joshi 2006). Introduced invasive species are con- Aside from adverse impacts on biodiversity, introduced sidered the second leading cause of species extinction aquatic species have also adversely affected other envi- and endangerment worldwide, the first being habitat ronmental factors. Escapees from the ornamental fish destruction (Williams et al. 1989). trade like the South American sucker mouth catfish, In the case of the golden apple snail Pomacea locally known as janitor fish Pterygoplichthys pardalis canaliculata whose introduction was as alternative pro- and Pterygoplichthys disjunctivus, have become invasive tein source for Filipinos, its introduction to the country in many areas in Luzon, including Marikina River and has been blamed for the loss of the edible native snail Laguna de Bay (Chavez et al. 2006; Jumawan et al. 2011) Pila conica (Pagulayan 1997). The loss of most of the and Agusan Marsh in Mindanao (Hubilla, Kis, and Pri- endemic cyprinids in Lake Lanao, the third-largest lake mavera 2008). The fish with its hard armor-like cover- in the country, has been attributed to the introduction ing damaged the banks of the Marikina River due to its of the white goby Glossogobius giurus and the eleotrid burrowing habit and damaged aquaculture fish cages in Hypseleotris agilis (Juliano, Guerrero, and Ronquillo Laguna de Bay. Considerable expense has been incurred 1989). The introduction of the Thai catfish Clarias ba- from a ‘bounty system’ type of approach to eradicate tracus has resulted in the loss of the native catfish Clar- janitor fish wherein fishermen were paid to catch the ias macrocephalus in many inland water bodies in the janitor fish at PHP 5.00/kg, after which the caught fish country. SEAFDEC/AQD implemented research and are destroyed (Joshi 2006). The two introduced fresh- development activities to breed Clarias macrocephalus water cichlid species, the black chin tilapia Sarotherodon (Tan-Fermin et al. 2008) in the hope of restocking de- melanotheron and the Mayan cichlid Cichlasoma uroph- pleted inland water bodies, but difficulties in obtaining thalmus, have been caught in Manila Bay (Ordonez et wild brood stock for induced spawning activities ham- al. 2015). It is to be noted that the black chin tilapia has pered efforts. been reported as an introduced species in Laguna de Bay Introduced species have far-reaching adverse en- (Cuvin-Aralar 2014). It is possible that Sarotherodon vironmental impacts. Cuvin-Aralar (2014) compared melanotheron found its way to Manila Bay via the Pasig the fish biodiversity in an aquaculture and non-aqua- River from Laguna de Bay, in addition to escapees from culture site in Laguna de Bay, the largest inland water fishponds in adjacent areas. Both cichlids were reported body in the Philippines widely used for fish production. to have had competitive interactions with other fish spe- Results showed that fish biodiversity was significantly cies in Manila Bay (Ordonez et al. 2015). lower in the aquaculture site compared to the non-aqua- In the case of the golden apple snail (Pomacea culture site. There was a significantly higher predom- canaliculata), its introduction caused considerable inance of introduced species for culture (Nile tilapia, havoc not only to inland water bodies but many rice bighead carp, Tra catfish) compared to native species fields as well (Joshi 2006). To eradicate these snails, in the aquaculture site. The non-aquaculture site had molluscicides valued at US$23 million were import- significantly higher relative dominance of native spe- ed between 1998 and 2005, but had limited success; cies. Indices of biodiversity such as Shannon-Wiener the snails still remain a problem. The snails are also Index, Simpson Index, and Evenness all indicate signifi- vectors of a rat lungworm that also affects humans cantly higher fish biodiversity in non-aquaculture sites (Joshi 2006). Socioeconomic and Health Impacts of Fisheries and Aquaculture Practices 39

Figure 39: Schematic diagram of direct and indirect impacts of species introduction on biodiversity

Allen species

Predation Disease Ecological impacts Genetic changes

Competition with Reduction in native species; Habitat destruction Hybridization Introgression endangering species; at times native species leading to extinction Hybrid vigor; Reduction in native Outbreeding New and unusual increased population numbers; depression; selection on native fitness inbreeding depression; reduced species reduced fitness fitness Genetic changes in native species

Displacement of native species; Findangering; extinction; loss of Direct impacts Indirect impacts taxonomically distinct population/species

Source: de Silva et al. 2009.

SOCIOECONOMIC AND HEALTH IMPACTS 5 OF FISHERIES AND AQUACULTURE PRACTICES

5.1 Human Health Impacts

5.1.1 Use of Waste Products for Aquaculture The use of excretory waste products, from both animals and humans, has been a common practice in many aquaculture-producing countries in Asia. The Philip- pines does not traditionally use human waste as fertilizer in aquaculture ponds, but the use of animal waste is a common practice. In 1989, the World Health Organi- zation (WHO) estimated that at least two-thirds of the world’s aquaculture production of fish comes from ponds fertilized by human and animal waste (in Howgate 1998). Although the trend in the overall use of fecal wastes is declining worldwide, the Philippines still uses livestock manure as organic fertilizer in ponds. The use of animal (and human) waste as fertilizer in aquaculture may result in the transfer of excreted pathogens like bacteria, viruses, and helminths not only to the aquatic environment but also to the cultured organisms, which in turn results in transfer to human consumers of the fishery product. Although thus far there is no available documentation on actual transfer of pathogens from aquaculture products reared in ponds fertilized with excreta in the Philippines, other countries have documented 42 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector the bioaccumulation of pathogenic viruses and bacte- (mostly Vibrios) resistance to antibiotics in shrimp ria in the muscle tissue of shellfish exposed to animal ponds currently using antibiotics to those ponds that and human feces (Schwab et al. 1998). The potential used antibiotics before and ponds which did not use to infect humans through direct dermal contact (of antibiotics. Their results showed highest percentage aquaculture wastewater) or ingestion of an improperly of microbials with multiple antibiotic resistance from cooked contaminated fish product is a possibility (Sap- ponds which were using antibiotics (oxolinic acid) at kota et al. 2008). the time of the sampling, followed by those from ponds which used antibiotics before. The lowest incidence of antibiotic resistance was in ponds that have not used 5.1.2 Application of chemicals and antibiotics. Antibiotic resistance was shown for OTC, bioactive compounds to boost furazolidone, oxolinic acid, and chloramphenicol. Fur- aquaculture production poses ther, the study also showed no correlation between concern on their release to the resistance and the actual type of antibiotic used, with aquatic environment highest incidence of resistance to oxolinic acid and Aside from direct contamination of fish products as furazolidone. shown in the previous section, the use of antibiotics Since many antibiotics used in aquaculture are in aquaculture feed also poses a concern in terms of also used on humans, concerns on antibiotic resistance the release of these compounds through leaching and and other subsequent effects on human health have excretion of the aquatic animals, which in turn will been raised (Marshall and Levy 2011). However, con- contaminate the environment (water and sediment). crete evidence of any possible harm to humans by the This has resulted in the emergence of antibiotic-resis- use of veterinary drugs, including antibiotics, as used tant microbes in aquaculture environments, increase in aquaculture is difficult to document as the drugs in antibiotic resistance in fish pathogens, transfer of are often similar to those used on humans (Howgate resistance to microbes of land animals and to human 1998). Precaution should nevertheless be put in place pathogens, and a change in the bacterial population in that will require very low levels of residues of these the sediments and water (Cabello 2006). The presence therapeutants in fish and fishery products for human of these antibiotic residues exerts undue influence on consumption (Bernoth 1991). Figure 40 illustrates the the microflora in the water and sediment and modifies sources and pathways of how antibiotics are released to the diversity of the population of microorganisms not the environment. only in situ, but in other areas as well where the residues may be washed away. The use of antibiotics will inev- itably select for antibiotic-resistant bacteria, for exam- 5.2 Socioeconomic Impacts ple, those which may contain resistant genes (Marshall and Levy 2011). These resistant bacteria will be able 5.2.1 Beneficial Impacts of Fisheries and to spread their genes into water and sediment indig- Aquaculture enous microbes, which also contain resistance genes. The positive impact of fisheries and aquaculture on the As applied in aquaculture, the low-dose, extended use livelihood of fishers and fish farmers has been amply of antibiotics among food animals promotes the prop- demonstrated. In the case of 6 of the top-ranked agation of resistant strains through selective pressures 22 species in freshwater aquaculture in the world, more on other nonresistant strains which may compete with than 20 percent of the production occurs in areas out- the resistant ones. A study conducted by Tendencia and side of their natural range of distribution. From 2000 de la Peña (2001) compared the microbial population’s to 2004, 16 percent of global finfish production from Socioeconomic and Health Impacts of Fisheries and Aquaculture Practices 43

Figure 40: Sources and pathways of how antibiotics are released into the environment

Human and Veterinary medicine Industrial production Aquaculture Stock breeding Crop production

Waste water Animal manure

Waste water treatment

Irrigation water

Environment (soils, rivers, lakes)

Source: Wang et al. 2015, (c) John Wiley & Sons. Reproduced with permission from John Wiley & Sons; further permission required for reuse. Notes: Antibiotics reach the environment through multiple ways, the main pathways beginning from human and agricultural use are highlighted. The thickness of the arrows reflects the relative importance of the pathways.

aquaculture was alien freshwater species (de Silva et al. people directly employed in aquaculture in Laguna de 2006). In the Philippines, two of the top three cultured Bay area, not considering other members of the popu- fish species were either introduced (in the case of Nile lation who are in one way or another dependent on lake tilapia) or translocated (the case of milkfish). Nile tila- aquaculture through backward linkages in the input pia introduction to the Philippine aquaculture scene markets and forward linkages in marketing. is considered highly beneficial both from the point of view of food production and as a source of livelihood. In Laguna de Bay, milkfish is a top commodity in terms of production volume. Milkfish is a translocated spe- Table 16: Production value (in PHP, cies and constituted on average 6.43 percent of total thousands) of milkfish and tilapia as well as total cultured milkfish production in the Philippines and 0.41 per- fish production in Laguna de cent of total fish produced in the country from 1996 to Bay 2006 (Israel, Boni-Cortez, and Patambang 2008). Nile tilapia, on the other hand, is an exotic species intro- Year Milkfish Tilapia Total Production

duced for culture in the lake. This species constituted 1996 618,745 305,683 957,736 on average 9.01 percent of total tilapias produced in 1997 696,389 342,968 1,063,847 the country and 0.31 percent of total fish production 1998 676,000 340,825 1,109,181 (Israel, Boni-Cortez, and Patambang 2008). With 1999 814,269 377,916 1,404,635 regard to income generation, aquaculture enterprises 2000 732,608 573,393 1,566,844 in Laguna de Bay averaged almost PHP 1,373 million 2001 123,607 416,582 929,555 from 1996 to 2006, of which milkfish contributed 2002 305,752 437,538 975,536 more than PHP 657 million and tilapia PHP 496 mil- 2003 674,235 535,983 1,390,427 lion (Israel, Boni-Cortez, and Patambang 2008). Table 2004 953,007 654,359 1,930,427 16 shows the value of production of milkfish and tilapia 2005 905,638 737,472 1,977,269 in Laguna de Bay from 1996 to 2006, representing the 2006 729,764 739,472 1,798,761 gross income of producers of these commodities. Israel, Average 657,274 496,530 1,373,081 Boni-Cortez, and Patambang (2008) estimates 5,152 Source: BAS files as cited by Israel, Boni-Cortez, and Patambang 2008.

SOLUTIONS TO MITIGATE IMPACTS 6 OF AQUACULTURE POLLUTANTS

Aquaculture is considered a ‘polluting’ industry due to the heavy use of various chemicals as well as the waste produce from the production process itself. These issues also affect the sustainability of the enterprise. Various technological innovations as well as ‘reinvention’ and modification of traditional methods of fish farming have been developed or are in the process of development to mitigate the impacts of aquaculture not only in the environment but on human health as well.

6.1 Use of Eubiotics and Strategies to Improve Health of Aquatic Animals

There are a number of nontraditional feed ingredients that are currently in various stages of research and development for use in aquaculture, essentially to improve health and overall production without resorting to use of traditional chemicals used in aquaculture. The term eubiotics (eu=good; bios=life) has been coined to include under it probiotics and prebiotics.

6.1.1 Probiotics and Prebiotics Probiotics are live microorganisms which when administered in adequate amounts confer a health benefit to the fish (FAO/WHO 2001), while prebiotics 46 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Table 17: Probiotics used in shrimp (h) maintain balance among intestinal microflora brackish-water farms in the (De et al. 2009). Dietary probiotics primarily work Philippines through the competitive exclusion principle, either by competing for nutrients against pathogenic organisms Probiotic Amount Used Remarks or competitive binding to receptors on the gut of the BZT Waste 1–2 kg/ha Pond preparation cultured fish. Some probiotics may produce a specific Digester 150–800 g/ha 1–150 DOC (days of culture) antibacterial substance themselves, while others may BZT 300–500 g/ha 5–7 days prior to stocking reduce the production of toxic amines and decrease Aquaculture 50–200 g/ha 1–150 DOC the ammonia level in the gastrointestinal tract (De et Super PS 30–50 L/ha Pond preparation al. 2009). Some examples of probiotics added to feeds 5–8 L/ha Rearing phase, every 5–10 days are the addition of live Bacillus subtilis to Pacific white Super Biotic 6 kg/ha Rearing phase 1–90 DOC weekly shrimp Penaeus vannamei diets (Wang 2007) and 5–10 g/kg feed 3–30 DOC, 2–3 time/day Lactobacillus species to giant freshwater prawn Mac- 10 g/kg feed 31–60 DOC, 2–4 times/day robrachium rosenbergii diets (Venkat, Sahu, and Jain Zymetin 5–10 g/kg feed Rearing phase, 3–30 DOC 2004), where both species showed improved growth 10 g/kg feed 31–60 DOC Ecomarine 25 tablets/ha Pond preparation performance. NS-SPO 2–3 kg/ha/culture 7-day interval Aside from dietary inclusion, probiotics may Series also be applied to the pond water in shrimp farms. Ta- BYM 5–15 kg/ha Rearing phase ble 17 lists some commercial probiotics used in shrimp Biobase 10 kg/ha Pond preparation ponds in the Philippines. 17 kg/ha/week Rearing phase Prebiotics are also incorporated into the feeds Source: Cruz-Lacierda et al. 2008. but are the indigestible component of the diet that are metabolized by specific microorganisms that are helpful for the growth and health of the host (cul- are nondigestible oligosaccharides used to control tured fish) (Manning and Gibson 2004). The prebi- or manipulate microbial composition and/or activ- otic should be resistant to gastric acids, breakdown ity, thereby assisting in maintaining a beneficial gut by digestive enzymes in the gut, and gastrointestinal microflora (Zimmerman, Bauer, and Mosenthin absorption and fermentation by intestinal microflora 2001). Both probiotics and prebiotics are now com- (Ringo et al. 2010). Among the important character- monly used in aquaculture as an alternative to the use istics of prebiotics are the following: (a) are easy to in- of chemical products to promote good soil and water corporate in the feed; (b) regulate gut viscosity; (c) are quality in ponds as well as limit or minimize the use of noncarcinogenic; (d) are derived from dietary poly- antibiotics. saccharides; (e) are of low calorific value; (f) reduce Probiotics may be incorporated into the feed harmful microbial loads; (g) are effective at low con- or applied directly to the water. If the product is to centrations; (h) exert anti-adhesive properties against be incorporated as a feed ingredient, it has to have harmful gut microbes; (i) stimulate beneficial gut mi- the following characteristics: (a) resistant to low pH crobes; and (j) produce no residual effects (Ganguly, and bile acids; (b) have no pathogenicity; (c) viable Paul, and Mukhopadhayay 2010). Prebiotics work by and stable in storage and in the field; (d) survive and providing selective stimulation of the growth and/or potentially colonize the gut; (e) be cultivable on a activity of intestinal bacteria that contribute to the large scale; (f) able to adhere to the epithelial lining health and well-being of the fish; shifting gut microbi- of the gut; (g) affect cultured fish beneficially; and al population to one dominated by beneficial bacteria; Solutions to Mitigate Impacts of Aquaculture Pollutants 47 increasing disease resistance; and improving nutrient 6.1.2 Nutraceuticals, Immunostimulants digestibility. Among the prebiotics that have proven Nutraceuticals (nutrition + pharmaceutical) are naturally beneficial to fish are inulin, fructooligosaccharides occurring substances which may be found in some level (FOS), and mannanoligosaccharides (MOS) which in the natural diet of the cultured organisms. The term have been used in carp, shrimps, and tilapia (Ringo was coined in 1989 in response to the growing interest et al. 2010). in food and food supplements in human health (And- Another type of eubiotic added to feeds is or- lauer and Fürst 2002). When functional feeds also aid in ganic acid (OA). These may be in the form of short- the prevention/treatment of disease and disorders, it is chain fatty acids (C1-C7), volatile fatty acids, and called a nutraceutical (Alexander et al. 2011). Nutraceu- weak carboxylic acids. These acids are widely distrib- ticals are administered orally over an extended period. It uted in nature as normal constituents of plants or an- attempts to stimulate the immune system to compen- imal tissues. Unlike mineral acids, OAs are relatively sate for production-related immunosuppression. It is weak; they do not completely dissociate in water, but an alternative to antibiotics and other chemotherapeu- low molecular weight OAs are miscible in water. They tants for disease management. Nutraceuticals have been may be in the form of sodium, potassium, or calci- known to increase overall vigor as well as increase levels um salts. OAs added to feeds should be protected to of antioxidants (Trushenski, Kasper, and Kohler 2006). avoid dissociation in the intestine, particularly in the Immunostimulants is another group of naturally segments with relatively high pH, and reach far into occurring compound that modulates the immune sys- the gastrointestinal tract where the bulk of the bacte- tem by increasing host resistance against diseases caused rial population is located. OAs act as an antimicrobial by pathogens. As a feed additive, immunostimulants growth promoter without the associated public health enhance transitory disease resistance in fish (Ringo et concern. OAs work by (a) improving feed palatabil- al. 2012). Some immunostimulants tested for aquacul- ity and reducing diet pH; (b) acting as antimicrobi- ture are beta glucans, alginate, and ErgosanTM extracts al preservative of feeds; (c) reducing gastric pH and from algae and dietary nucleotides which have been enhancing pepsin activity; (d) stimulating beneficial tested in catfish, tilapia, eel, carp, snakehead, and sea intestinal flora and improving health; (e) increasing bass (Ringo et al. 2012). digestibility of nutrients and thus improving growth and feed conversion; and (f) reducing the risk of spread of microbial infection by lowering microbial 6.2 Legislations and Regulations on the load in feces (Elala and Ragaa 2014; Ng et al. 2009). Use of Chemicals and Fisheries and Some examples of OA used in aquaculture and live- Aquaculture stock feeds are formic acid, acetic acid, propionic acid, oxalic acid, lactic acid, and butyric acid. OAs in 6.2.1 Setting Up Standards the form of potassium diformate (KDF) and sodium The Philippine National Standards (PNS) for the code diformate (NDF) have been used in experimental di- of conduct for Good Aquaculture Practice (GAqP) ets in Nile tilapia and were shown to improve growth, was published in 2014 (PNS/BAFPS 2014). This is FCR, and disease resistance and lower fecal microbial part of the Philippine commitment to the Association load (Cuvin-Aralar et al, 2011; Ng et al. 2009; Ela- of Southeast Asian Nations (ASEAN) Roadmap for la and Ragaa 2014). Formic acid showed the highest ASEAN Community 2009–2015, seeking to enhance inhibitory effect, compared to propionic and butyric intra- and extra-ASEAN trade and long-term com- acid, on Vibrio harveyi in shrimp culture (Mine and petitiveness of ASEAN food, agriculture, and forestry Boopathy 2011). products and commodities. Before promulgation of the 48 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

GAqP, it underwent a series of reviews and consultations forms used in culturing any aquatic organisms such as, with stakeholders in various parts of the country and but not limited to, crustaceans, fish, and mollusks…. the Committee on Fisheries and Aquaculture (CFA) Custom-mixed feeds and feed products for aquaculture of the Philippine Council for Agriculture and Fisher- use are also covered.” Under this code, nutrient standards ies (PCAF). The Code of GAqP applies to aquaculture for feeds for various commodities and for different life farms and projects covering hatchery, nursery, fish cage/ stages have been put in place. Pellet quality and stabili- pen/pond, seaweed, and mollusk farms regardless of ty are also included in the standards. Another important ownership and “covers practices that aim to prevent or part of PNS for Aquaculture Feeds is the list of banned minimize the risk associated with aquaculture produc- veterinary drugs in aquaculture feed (Table 18) adopted tion (mariculture, coastal aquaculture/ brackish-water from the Philippine Veterinary Drug Directory. It is in- culture, and freshwater culture). This code covers the teresting to note that despite a ban on the use of antibi- following aspects of aquaculture production namely: otics like chloramphenicol as early as 1990, the drug was (a) food safety, (b) animal health and welfare, (c) envi- still in use when the survey was conducted by Cruz-Lac- ronmental integrity, and (d) socioeconomic” (PNS/ ierda et al. in 1995–1996 (refer back to Table 10). BAFPS 2014). Minimum compliance requirements PNS for selected capture fishery and aquaculture covering location, hygiene/sanitation, waste disposal/ products have also been established, but mainly adopt- removal, culture environment preparation including ed from international standards following those set by application/dispensing of chemical inputs and veteri- the FAO/WHO Codex Alimentarius Commission. Ta- nary drug, feed inputs and feed quality, water manage- ble 19 lists some of the PNS published for various fish ment, disease control and management, animal welfare, and fishery products. post-harvest, and transport are included in the code. Proper record keeping and inspection by a designated authority for compliance to the code is also covered. 6.2.2 Regular Monitoring of Fisheries and PNS for Aquaculture Feeds have also been final- Aquaculture Operations’ Use of ized and published (PNS/BAFPS 2010) and covers “the Chemicals preparation and formulation of nutritionally adequate The code for GAqP covers monitoring of aquaculture aquaculture feeds such as pellet, mash, and crumble feed operations to ensure compliance to the minimum

Table 18: Banned veterinary drugs in aquaculture feeds

Drug Administrative Order Subject Date

Clenbuterol, Salbutamol, No. 14, Series of 2003 Ban on the use in food animals of beta-agonist drugs May 12, 2003 Terbutaline, Pirbuterol (Department of Agriculture) used in humans as bronchodilators and tocolytic agents Furaltadone, Furazolidone, No. 2, Series of 2000 (Department of Declaring a ban/phase-out of the use of nitrofurans in August 17, 2000 Nitrofurazone Agriculture and Department of Health) food-producing animals Carbadox, Olaquindox No. 60, Series of 2000 (Department of Ban and withdrawal of olaquindox and carbadox from January 11, 2000 Agriculture) No. 4-A, Series of 2000 the market (Department of Health) Chloramphenicol No. 60, Series of 1990 (Department Declaring a ban on the use of chloramphenicol in food- April 30, 1990 of Agriculture) No. 91, Series of 1990 producing animals (Department of Health) Source: PNS/BAFPS 2010. Solutions to Mitigate Impacts of Aquaculture Pollutants 49

Table 19: PNS for various fishery products

Product PNS Reference Reference Standard

Milkfish, frozen PNS/BAFPS 66: 2008 a, Tilapia, frozen PNS/BAFPS 67:2008 a, b Shrimp and prawns, quick frozen PNS/BAFPS 70:2008 a, c Grouper, live and chilled/frozen PNS/BAFPS 73:2009 d, e Abalone, live and chilled PNS/BAFPS 72:2009 f, e Lobsters, quick frozen PNS/BAFPS 91:2011 g, h, e Cephalopods, fresh and frozen PNS BAFS 136:2014 h Tuna, fresh-chilled and fresh-frozen for sashimi PNS BAFS 137:2014 h, i Sea cucumber, dried PNS/BAFPS 128:2013 j Danggit, dried PNS/BAFPS 68:2008 k Note: a - International Commission on Microbiological Specifications for Food (ICMSF), 1986; b - FAO/WHO CAC/RCP, 1999; c - FAO/WHO CODEX STAN, 1995; d - FAO/WHO CAC/RCP 2005; e - FAO/WHO CAC CODEX STAN, 1995; f - FAO/WHO CL 2008; g - CODEX STAN 2004; h - CODEX STAN 2009; i - CODEX STAN 1995; j - CODEX STAN 2005; k - FAO/WHO CAC/RCP 1979.

requirements set by the code. The aquaculture opera- 6.2.3 Development and Adoption of tor should record the last two croppings specifying the National and Regional Guidelines on group of fish treated with veterinary drugs, the total the Use of Chemicals in Aquaculture quantity of the drugs used, the start and end date of and Designation of Competent treatment, completion of withdrawal period, and the National Government Authority for earliest date the fish is safe to be consumed. The code Regulation and Monitoring further states that the withdrawal period be verified by The ASEAN recently published the ‘Guidelines for conducting residue analysis on samples of treated fish. the Use of Chemicals in Aquaculture and Measures The MRL (maximum residue limit) for the particular to Eliminate the Use of Harmful Chemicals’ (ASEAN drug should fall within the acceptable level based on Secretariat 2013). The guidelines were developed to the standards set by Codex or trading partners (PNS/ help national regulators and stakeholders manage the BAFPS 2014). various chemicals used in aquaculture in ASEAN mem- Although the code for GAqP has been in exis- ber countries. The guidelines aim to provide the Com- tence for a number of years, compliance is not man- petent Authority (CA) of each ASEAN member state datory. Fish farms who need to be certified to enable in setting standards and regulating the use of chemicals produce from these farms to be exported are the only and aquaculture and implementing measures to elimi- ones who need to comply with GAqP. For most of the nate the use of harmful chemicals. The member states fish farmers selling their produce in local markets, there are encouraged to assess and review gaps within each is no need to be certified and thus no push to comply individual country regarding chemicals used in aqua- with GAqP. Limitations on the part of the Government culture in the region listed in the guidelines. Among the also exist, particularly in funds to enable the designat- classes of aquaculture chemicals listed in the guidelines ed certifying agency to conduct the necessary inspec- which are commonly used in ASEAN member states tions, monitoring, and analysis for farms that want to are (a) antibiotics/antimicrobials both for food fish and be certified. ornamentals; (b) disinfectants; (c) chemotherapeutants 50 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector for food fish and ornamentals; (d) piscicides for use in countries. Table 20 lists the current regulatory status pond preparation and early culture only; (e) hormones of various aquaculture chemicals for food fish in the both for food fish and ornamentals; (f) anesthetics; Philippines. (g) culture system preparation; and (h) banned chem- The ASEAN guidelines came about because icals. There are differences in the list of allowed and the use of drugs and chemicals in aquaculture opera- prohibited chemicals in each of the ASEAN member tions in the ASEAN region are not fully regulated and

Table 20: List of chemicals used in aquaculture and their status in the Philippines and other ASEAN member countries

Chemical Status Chemical Status

Antibiotics/Antimicrobials Chemotherapeutants Amoxicillin y, b Copper sulfate y, a Chlortetracycline* y, b Formaldehyde y, a Doxycycline y, b Hydrogen peroxide y, a Enrofloxacin* y, b Methylene blue y, a Erythromycin* y, b Potassium permanganate y, a Florfenicol y, b Praziquantel y, a Metronidazole/Dimetridazole n, b Sodium chloride y, a Nitrofuran n, b Trichlorfon y, b Norfloxacin y, b Trifluralin y, b Oxolinic acid* y, b Anesthetics OTC* y, b Eugenol, Aqui-S y, a Rifampicin y, b Phenoxy ethanol y, a Sulfadimethoxine + Trimetoprim* y, b Tricane methanesulfonate (TMS222) y, a Sulfamerazine y, b Disinfectants Sulfonamide* y, b Benzalkonium chloride y, a Tetracycline* y, b Calcium hypochlorite y, a Hormones Chloramine-T y, a 17” MT y, b Cypermethrin y, b HCG y, a Formalin y, a LHRHa y, a Hydrogen peroxide y, a Pituitary extract y, a Iodine y, a Culture system preparation Lime y, a Calcium chloride y, a Malachite green n, b Calcium hypochlorite y, a Methylene blue y, a Lime y, a Omnicide y, a Hormones Disinfectants Sodium thiosulfate y, a Potassium monopersulfate y, a Urea y, a Potassium permanganate y, a Zeolite y, a Sodium chloride y, a

(continued on next page) Solutions to Mitigate Impacts of Aquaculture Pollutants 51

Table 20: List of chemicals used in aquaculture and their status in the Philippines and other ASEAN member countries (continued)

Chemical Status Chemical Status

Piscicides Sodium hypochlorite y, a Organophosphates (dichlorvos; trichlorfon) y, a Trichlorfon y, a Rotenone y, a Banned Saponin y, a Beta-Agonist n, b Chloramphenicol n, b Clenbuterol n, b Crystal violet n, b Cypermethrin Diethylstilbestrol (Stilbene) n, b Dimetridazole (nitroimidazole) n, b Enrofloxacin Ipronidazole n, b Malachite green n, b Metronidazole (nitroimidazole) n, b Nitrofuran n, b Nitroimidazoles n, b Organochlorine n, b Organophosphates (selected) n, b Organotin n, b Ronidazole (nitroimidazole) n, b Trichlorfon (dipterex) y, b Trifluralin y, b Note: y - allowed in the Philippines; n - prohibited in the Philippines; a - allowed in other ASEAN member countries; b - prohibited in other ASEAN member countries. * - Chemicals with MRL.

controlled by their respective CA. Under these ASE- (d) approval and/or registration of third-party service AN guidelines, the BFAR is the designated CA for the provider (laboratory, quarantine facilities); (e) approv- regulation of chemicals used in aquaculture while the al and/or registration of manufacturers and traders of Food and Drug Administration of the Department chemicals and drugs for use in aquaculture; (f) estab- of Health (DOH) is the CA for veterinary drugs and lishment and regular update of a national list of chem- the Fertilizer and Pesticide Authority (FPA) is the CA icals for aquaculture purposes; (g) creating awareness for pesticides (Coloso, Catacutan, and Arnaiz 2015). among aquaculturists through extension and awareness The assignment as CAs of these agencies takes off from programs; (h) carrying out monitoring, inspection, and the existing regulatory structure in the Philippines. As surveillance activities; (i) regulating the import, manu- the CA, these institutions shall be responsible for the facture, and trade of chemicals and products; (j) evalu- following: (a) technical, diagnostic capacity and capa- ating and verifying the efficacy and safety of chemicals bility; (b) coordination with other relevant agencies; intended for use in aquaculture systems; and (k) carry- (c) approval and registration of aquaculture premises; ing out enforcement activities for non-compliance to 52 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector national practice and legislations. As agreed upon in the value. This type of aquaculture has received much ASEAN guidelines, these local CAs will be responsible attention in the past decade as a method of producing for notifying other ASEAN CAs and other relevant in- aquaculture products through the co-culture of compat- ternational organizations on current laws and regula- ible organisms. The principle is that waste product of tions regarding chemicals in aquaculture. This is in view one species (usually finfish as fed species) is utilized by of increasing trade among ASEAN member countries. another species, usually lower trophic levels such as seaweeds, mollusks, and other benthic invertebrates (Ren et al. 2012). IMTA produces fish biomass and at the same 6.3 Regulations on the introduction of time minimizes waste product from aquaculture opera- nonnative species for culture and tions. IMTA can be applied to open water or land-based protecting local species systems (aquaponics), marine or freshwater systems, as well as temperate or tropical systems. It is essentially not According to information on their website, the BFAR a new concept, since a form of IMTA was practiced in issued Fisheries Administrative Order 189 series of China in 2200 BC (NACA 1989). The use of extractive 1993 prohibiting the importation of live shrimp and species is a cost-effective way to mitigate the amount prawn of all stages. However, this ban was lifted to favor of nitrogen, phosphorus, carbon, and organic wastes the culture of the Pacific white shrimp Penaeus vanna- released from aquaculture. Important considerations mei through Fisheries Administrative Order 225, 225-1 for IMTA are (a) compatible combination of species; series of 2007, and Fisheries Administrative Order (b) appropriate habitat; (c) appropriate available culture 225-2, 225-3 series of 2008. This was to address the technologies for the commodity; (d) complementary demand for the entry of this shrimp into the country ecosystem functions of the cultured organisms; (e) cul- to save the ailing tiger shrimp (Penaeus monodon) that tured organisms being able to grow to a significant bio- has been devastated by various diseases. There are no mass for efficient mitigation of wastes; and (f) commer- other Fisheries Administrative Orders prohibiting the cial value of the cultured commodities (Chopin et al. introduction of other species for aquaculture in either 2010). In the Philippines, experimental trials on IMTA the food or ornamental fish industry. However, there with species such as milkfish as the ‘fed’ commodity and are numerous Fisheries Administrative Orders issued angel wing clam (Anodontia philippiana) and sand fish through the years mainly prohibiting or regulating the (Holothuria scabra) as the extractive species have been export of various fisheries commodities as well as estab- conducted (Lebata-Ramos, pers. comm). lishing fish sanctuaries in various parts of the country.

6.4.2 Aquasilviculture 6.4 Technologies to Reduce Nutrients Aquasilviculture is the integration of aquaculture with from Aquaculture mangroves. It is an environment-friendly system which promotes harmonious coexistence between fisheries 6.4.1 Integrated Multitrophic production and mangrove systems in a semi-enclosed Aquaculture System and Integrated environment. This culture method promotes harmoni- Agriculture-Aquaculture ous use of mangrove areas for aquaculture production, Integrated Multitrophic Aquaculture (IMTA) involves without destroying the mangrove forests. The Philip- cultivating fed species with extractive species that use pine government through the BFAR and the Commis- wastes from aquaculture for their growth, with the sion on Higher Education (CHED) in collaboration advantage of all species in the system having economic with academic institutions and local governments are Solutions to Mitigate Impacts of Aquaculture Pollutants 53 implementing the ‘Philippine National Aquasilvicul- Therefore, the aquaponics system is an efficient way to ture Program’. A memorandum of agreement has been upcycle nutrients from aquaculture to crop production, signed between the two institutions as principals. The thus avoiding eutrophication problems associated with program involves reforestation of denuded mangrove aquaculture wastes. areas and use of these reforested areas and existing man- Rice-fish-vegetable integrated production is groves for the culture of fish and other fishery products widely practiced in many Asian countries like China, without cutting down a single tree. Abandoned areas Vietnam, India, and Bangladesh. However, there is covered by fishpond lease agreements (FLAs) as deter- limited adoption in the Philippines. This type of pro- mined jointly by the Department of Environment and duction system is ideally suited for small farmholdings Natural Resources (DENR), Department of Agricul- in rural communities. This type of farming provides ture (DA), and the LGUs shall also be restored to their several advantages: (a) maximize use of land and water original mangrove state (Flores, et al. 2014). resources over a limited area; (b) integrated pest management system by reducing the use of pesticides since fish feed on larvae and juveniles of pests in rice fields; 6.4.3 Integrated Agri-Aquaculture System (c) minimize the use of fertilizer in rice since fish waste Integrated Agri-Aquaculture (IAA) combines the pro- is a source of nutrients for the growing rice and other duction of crops, livestock, and aquatic animals in a crops; and (d) improve resource utilization by diversi- limited system and is conducive for small farmholding fying crops produced in a limited area. The BFAR has by maximizing production in a small area and using the been promoting the integrated culture of rice and fresh- different waste components from each product. water prawn (Macrobrachium rosenbergii) through pilot One type of such integrated production system demonstration sites in the province of Laguna using is aquaponics. It is the integration of recirculating fish just 1,000 m2 of rice fields, with 10 percent devoted production systems with hydroponic plant production to prawn and the rest to rice. Figure 39 illustrates the to use the fertilizers efficiently. The integration of these layout of the farm. Cost and return analysis for this set- two systems leads to the removal of nutrients (primarily up proved to be significantly better for the integrated nitrates and phosphates) from the system, omitting the rice-prawn system compared to monoculture of rice need for water changes and thus conserving water. How- (Casbadillo, unpublished). Figure 41 shows the cost ever, water is needed to fill the initial system. Aquapon- and return for this simple setup. ic systems recirculate water to use nutrients efficiently, IAA is not as widely popular in the Philippines thus producing food in a sustainable manner with little as in other Asian countries. For instance, rice-fish cul- environmental impact. Removal of nutrients from fish ture poses problems in synchronizing harvest of the two effluent through plant nutrient uptake is an efficient main crops. Many rice farmers feel that digging deeper and productive method of filtration (Licamele 2009). ditches in specific areas in the rice field limits the area An aquaponics system is a symbiotic joining of aqua- devoted to rice. Since the primary crop is rice and the culture and hydroponics. The nutrient wastes produced side crop is fish, traditional rice farmers have to learn by fish are circulated to the plant growing component the technology of fish culture in tandem with their rice and used by plants as fertilizers. Instead of building up production effort. Although the BFAR promotes this, in the aquaculture system, nutrients generated from fish the agencies responsible for rice production do not. It is waste serve as liquid fertilizer to hydroponically grown mainly the ‘fish’ people who are promoting integration plants. The hydroponic component serves as a biofil- with crops. Another hindrance to the adoption of IAA ter so that the water can be circulated back to the fish is the limitation in the use of traditional agricultural culture component of the system (White et al. 2008). chemicals such as pesticides since these are toxic to fish. 54 An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector

Figure 41: Schematic diagram of farm Figure 42: Cost and return for rice layout (top-top view; bottom- monoculture and rice-prawn cross-sectional view) of rice- integrated culture for a prawn culture in Laguna based 1,000 m2 plot from pilot studies on a 1,000 m2 area of the BFAR

14,000 12,000 10,000 Are planted to rice 8,000 Irrigation PhP

Are for Prawn 6,000 4,000 2,000 Irrigation 0 canal 0.5 m Rice Mono Rice + Prawn Prawn Cost Gross income Net income Dike area Dike Source: Casbadillo unpublished. 1 m Planted to rice pond (Bolivar, Jimenez, and Brown 2006) and lake- Pipe with net cover based cages (Cuvin-Aralar et al. 2012). FCRs were significantly lowered, but no reduction in growth was observed. The improved performance attained by the skip feeding strategy may be a result of reduced feed Many farmers find it difficult to veer away from pesti- waste either through more complete feed consumption cides and fertilizer use in their rice field, despite the fact by fish and/or improved nutrient absorption. Skip feed- that one of the significant features of IAA is integrated ing or alternate day feeding is both an economical and pest management: using fish to control rice pests and ecologically sound alternative to Nile tilapia culture in weeds. Moreover, the use of fertilizers is also minimized both ponds and lake-based culture systems. since fish excretory products are sources of nutrients for Another feeding management strategy that has the growing rice. shown to be effective in reducing feed wastage and improving feed efficiency is the use of maintenance feeding (MF) and submaximum feeding (SF). Exper- 6.4.4 Feeding Management System which imental studies using this type of feed management Involves Improvement of Feeding where the fish are given MF and subsequently SF gave Practices for Cultured Aquatic 30 percent less feed wastage, as measured by fecal out- Animals put, compared to control (given full daily feed ration). Proper feed management results in efficient use of Mean FCR of fish given the MF/SF ration was only feed with reduced feed wastage, resulting in high feed 0.8, which is significantly lower than 1.6 for fish given efficiency (low FCR). In the Philippines, it has been the full ration. Growth rates of fish also did not differ shown that skip feeding or alternate day feeding strat- and full catch-up growth occurred in the MF/SF ra- egy for Nile tilapia is effective and efficient in both tion. This study shows that feeding fish in cycles of MF Solutions to Mitigate Impacts of Aquaculture Pollutants 55 followed by SF may be an applicable feed management technique actually ‘upcycles’ by closing the nutrient strategy to reduce feed costs and at the same time im- loop. Hence, water exchange can be decreased with- prove effluent quality of the aquaculture water without out deterioration of water quality and, consequently, affecting growth (Ali et al. 2010). Studies on this type the total amount of nutrients discharged into adjacent of feed management in local aquaculture commodities water bodies may be decreased (Lezama-Cervantes & should also be conducted to determine if it can be ad- Paniagua-Michel 2010). opted locally. BFT gained prominence as a sustainable method to control water quality, with the added value of producing proteinaceous feed in situ from a combina- 6.4.5 Biofloc Technology tion of plankton and heterotrophic bacteria (Crab et al. Biofloc Technology (BFT) is considered an environ- 2012) that are able to provide nutrients to the cultured ment-friendly and efficient system to produce aquacul- species. The technology has been used in the culture ture products, since nutrients could continuously be of various species like Nile tilapia (Avnimelech 2007) recycled and reused. The sustainable approach of such and marine shrimps (Ballester et al. 2010; Emeren- a system is based on the growth of microorganism in ciano, Ballester, and Cavalli 2011; Emerenciano et al. the culture medium, benefited by the minimum or zero 2012; Brito et al. 2014), with positive results in terms water exchange. These microorganisms (biofloc) have of better growth and survival but with differences in the two major roles: (a) maintenance of water quality, by degree of the beneficial effect of BFT among the differ- the uptake of nitrogen compounds generating ‘in situ’ ent species. In the BFT culture system, the floc makes microbial protein and (b) nutrition, increasing cul- the water turbid. Most fish farmers have the idea of ture feasibility by reducing FCR and decreasing feed clear water being much better than turbid water, thus costs (Emerenciano, Gaxiola, and Cuzon 2013). As a BFT goes against what fish farmers expect (Avnimelech closed system, BFT has the advantage of minimizing 2009). One of the issues against BFT is the require- the release of effluents into water bodies as opposed to ment for vigorous aeration in the system to enable the traditional culture systems where water drained from floc to remain in the water column, or else the system ponds and tanks in the course of the grow out results will not function. Oxygen requirement in BFT typi- in eutrophication of receiving water bodies. In BFT, cally ranges from 5 to 8 mg oxygen per liter per hour, ‘waste’-nitrogen from uneaten feed and cultured organ- another reason for the need for aeration (Hargreaves isms is converted into proteinaceous feed available 2013). Electricity cost, needed to provide the aeration for those same organisms. Instead of ‘downcycling’, a required, in the Philippines is quite prohibitive, thus phenomenon often found in an attempt to recycle, the limiting the adoption of BFT.

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