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Page 1: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

An Overview of Agricultural Pollution in the PhilippinesThe Fisheries Sector2016

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Page 2: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and
Page 3: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

An Overview of Agricultural Pollution in the Philippines The Fisheries Sector2016

Submitted to

The World Bank’s Agriculture and Environment & Natural Resources Global Practices

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© 2016 International Bank for Reconstruction and Development / The World Bank 1818 H Street NWWashington DC 20433Telephone: 202-473-1000

Internet: www.worldbank.org

This work is a product of the staff of The World Bank. The findings, interpretations, and conclusions expressed in this work do not necessarily reflect the views of The World Bank, its Board of Executive Directors, or the governments they represent.

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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.

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CONTENTS

Abbreviations and Acronyms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .vii

Foreword . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix

1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.1 History of Capture Fisheries and Aquaculture in the Philippines . . . . . 11.2 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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152.1 Population Pressure to Increase Fish Production from

Capture Fisheries and Aquaculture . . . . . . . . . . . . . . . . . . . . . . . . . . 152.2 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 . . . . . . . . . . . . . . . . . . 213.1 Conversion of Land and Water Resources for Aquaculture . . . . . . . . 213.2 Practices to Prepare and Improve Culture Environment . . . . . . . . . . 243.3 Practices to Improve Production . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263.4 Practices to Improve Aquatic Animal Health . . . . . . . . . . . . . . . . . . . 293.5 Practice to Diversity Cultured Commodities . . . . . . . . . . . . . . . . . . . 30

4 Physical Impacts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 334.1 Environmental Impacts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 334.2 Impact of Diversification of Culture Commodities

through Species Introductions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sectoriv

5 Socioeconomic and Health Impacts of Fisheries and Aquaculture Practices . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 415.1 Human Health Impacts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 415.2 Socioeconomic Impacts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42

6 Solutions to Mitigate Impacts of Aquaculture Pollutants . . . . . . . . . . . . . . . . . 456.1 Use of Eubiotics and Strategies to Improve Health of Aquatic Animals . . . . . . . . . . . . . . . 456.2 Legislations and Regulations on the Use of Chemicals and Fisheries and Aquaculture . . . . 476.3 Regulations on the introduction of nonnative species for

culture and protecting local species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526.4 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 . . . . . . . 4Figure 3: Trend of fisheries production in the Philippines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4Figure 4: Average change in volume of production in Philippine fisheries from

1980 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5Figure 5: Capture fisheries data for the Philippines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5Figure 6: Average change in volume of production in Philippine capture fisheries

from 1980 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5Figure 7: Marine and inland capture fisheries data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6Figure 8: Average change in volume of production in Philippine marine capture fisheries

from 1980 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6Figure 9: Average volume of production in Philippine marine capture fisheries

from 1980 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6Figure 10: Average volume of production in Philippine inland capture fisheries

from 1980 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7Figure 11: Average change in volume of production in Philippine inland capture fisheries

from 1980 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7Figure 12: Aquaculture production in marine, freshwater, and brackish-water

culture environments (excluding aquatic plants) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8Figure 13: Average volume of production in Philippine brackish-water aquaculture

from 1996 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8Figure 14: Average change in volume of production in Philippine brackish-water aquaculture

from 1996 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9Figure 15: Average volume of production in Philippine freshwater aquaculture

from 1996 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9Figure 16: Average change in volume of production in Philippine freshwater aquaculture

from 1996 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9Figure 17: Top aquaculture fishery commodities in Philippine aquaculture . . . . . . . . . . . . . . . . 10Figure 18: Average volume of production in Philippine marine aquaculture

from 1996 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

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vContents

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 . . . . . . . . . . . . . . . 11Figure 21: Average change in volume of production in Philippine peneid shrimp

aquaculture from 1996 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11Figure 22: Average volume of production in Philippine peneid shrimp aquaculture

from 1996 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12Figure 23: Average volume of production in Philippine tilapia aquaculture

from 1996 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13Figure 24: Average change in volume of production in Philippine tilapia aquaculture

from 1996 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13Figure 25: Average change in volume of production in Philippine milkfish aquaculture

from 1996 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13Figure 26: Average volume of production in Philippine milkfish aquaculture

from 1996 to 2014 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14Figure 27: Philippine population growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16Figure 28: Value of fisheries production in Philippine pesos from 1980 to 2014 . . . . . . . . . . . . . 17Figure 29: Contribution of fisheries to the Philippines’ GDP . . . . . . . . . . . . . . . . . . . . . . . . . . . 17Figure 30: Contribution of fisheries to GVA at constant prices . . . . . . . . . . . . . . . . . . . . . . . . . . 18Figure 31: Comparison of value of exports and imports of fisheries products . . . . . . . . . . . . . . . 18Figure 32: Import dependency ratio of three major fish culture commodities . . . . . . . . . . . . . . . 19Figure 33: Production cost, farm gate price, and profit margins for milkfish culture . . . . . . . . . . 19Figure 34: Process of establishment of MPs in the Philippines . . . . . . . . . . . . . . . . . . . . . . . . . . 22Figure 35: Site of MPs for establishment in the Philippines . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23Figure 36: Number of aquatic animal species introductions in the Philippines

in the various decades . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30Figure 37: The loss of mangrove areas and the development of brackish-water ponds

in the Philippines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33Figure 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 . . . . . . . . 43Figure 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 . . . . . . . . . . . . . . . . . . . . . 54Figure 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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23Table 3: Groups of chemicals and additives used in aquaculture . . . . . . . . . . . . . . . . . . . . . . . 24Table 4: Application of inorganic fertilizer in shrimp Penaeus monodon and milkfish

Chanos chanos ponds for the period surveyed in 1995–1996 and 2006–2007 . . . . . . 26Table 5: Summary of organic fertilizers used in milkfish and shrimp ponds and

in polyculture of these two commodities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27

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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 . . . . . 29Table 11: Disinfectants used in black tiger shrimp brackish-water farms

in the Philippines in 2006–2008* . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30Table 12: Partial list of invasive and potentially invasive introduced species to

the Philippines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31Table 13: Estimated organic matter and nutrient loading for one ton of harvested shrimp

released at different FCRs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34Table 14: Comparison of phosphorus values from marine aquaculture sites

in the Philippines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35Table 15: Level of OTC, OXA, and OCP in fish samples from the Philippines . . . . . . . . . . . . 37Table 16: Production value (in PHP, thousands) of milkfish and tilapia as well as total

cultured fish production in Laguna de Bay . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43Table 17: Probiotics used in shrimp brackish-water farms in the Philippines . . . . . . . . . . . . . . . 46Table 18: Banned veterinary drugs in aquaculture feeds. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48Table 19: PNS for various fishery products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49Table 20: List of chemicals used in aquaculture and their status in the Philippines and

other ASEAN member countries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50

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ABBREVIATIONS AND ACRONYMS

AFMA Agriculture and Fisheries Modernization ActASEAN Association of Southeast Asian Nations BFAR Bureau of Fisheries and Aquatic ResourcesBFT Biofloc TechnologyBW Body WeightCA Competent AuthorityCFA Committee on Fisheries and AquacultureCHED Commission on Higher EducationDA Department of AgricultureDENR Department of Environment and Natural ResourcesDOH Department of HealthFAO Food and Agriculture OrganizationFCR Feed Conversion RatioFLA Fishpond Lease AgreementFOS FructooligosaccharidesFPA Fertilizer and Pesticide AuthorityGAqP Good Aquaculture PracticeGDP Gross Domestic ProductGVA Gross Value AddedHCG Human Chorionic GonadotropinIAA Integrated Agri-AquacultureICMSF International Commission on Microbiological Specifications

for FoodIMTA Integrated Multitrophic AquacultureKDF Potassium DiformateLGU Local Government UnitLHRHa Luteinizing Hormone Releasing Hormone-AnalogMOS MannanoligosaccharidesMF Maintenance Feeding

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MP Mariculture ParkMRL Maximum Residue LimitMT MethyltestosteroneNDF Sodium DiformateNPK Nitrogen, Phosphorus and

PotassiumOA Organic AcidPCAF Philippine Council for Agriculture

and Fisheries PEL Permissible Exposure Limit

PNS Philippine National StandardsOCP Organochlorine PesticidesOTC OxytetracyclineOXA Oxalinic AcidSEAFDEC/AQD Southeast Asian Fisheries Devel-

opment Center, Aquaculture Department

SF Submaximum FeedingWHO World Health Organization

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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 aquacul-ture; (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.

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INTRODUCTION

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 riv-ers 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

1

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector2

is a consequence of rapid population growth accompa-nied by increased demand for fish and fishery products since production from capture fisheries has become in-creasingly unable to meet the demand due to a variety of factors, foremost of which are over exploitation and the depletion of natural stocks (Sapkota et al. 2008).

In Southeast Asia, the early development of aquaculture first started in the 15th century in Indo-nesia with brackish-water culture and spread to neigh-boring countries. The Philippines being an archipelago, with more water than land like Indonesia, followed suit.

Expansion of the aquaculture industry in the Philippines was further stimulated with the establish-ment of the Bureau of Fisheries and Aquatic Resources (BFAR) in the late 1940s. The BFAR established and implemented schemes to promote aquaculture through the construction of ponds (Primavera 1995). Since then, aquaculture has evolved in the country with a di-verse list of species cultured in a variety of ecosystems. The bulk of the production is from aquatic plants (sea-weeds), milkfish, tilapia, shrimp, carp, and bivalves like oyster and mussel. Like capture fisheries, aquaculture has significantly contributed to food security and rural livelihood. The Philippines ranked 4th with regard to aquaculture production in 1997, but dropped to 12th place by 2012 (FAO 2014) and moved slightly to 11th place in 2013 (FAO FishStat 2015).

Milkfish was the primary coastal aquaculture commodity cultured in brackish-water ponds, with Food and Agriculture Organization (FAO) records dat-ing back to 1950. The culture of this euryhaline species spread to freshwater and by the 1990s to marine cages. Hand in hand with developments in the technology of milkfish culture and success in the captive breeding of the commodity pioneered by the Southeast Asian Fish-eries Development Center/Aquaculture Department (SEAFDEC/AQD) (Marte and Lacanilao 1986; Juario et al. 1984) coupled with the promotion of the culture of the commodity by the locals, the production of the commodity spread to other areas of the country.

The culture of peneid shrimps, mainly the black tiger shrimp Penaeus monodon, evolved from

and some areas into fish port and fish landing areas sup-porting large-scale commercial fishing.

Capture fisheries technology in the Philippines also evolved through time. Early trades with China and the settlement of Chinese communities resulted in the introduction of some capture fisheries gears by this eth-nic group, such as the large lever net or ‘salambaw’ as well as gill and casting nets (Rasalan 1952, as cited by Spoehr 1984). The capture fishing industry during the Spanish colonial times was relatively static from a tech-nological standpoint. In the late 1800s, Tagalog inno-vations such as a type of round haul seine ‘sapiao’ and a deepwater fish corral spread to the archipelago (Um-ali 1950, as cited by Spoehr 1984). In pelagic fishing, more innovations such as a type of purse seine, gill net, and lift net were adopted. Japanese commercial fish-ing innovations such as the beam trawl and ‘muro-ami’ were introduced. With these innovations, the Philip-pines’ capture fisheries transformed from a broad-spec-trum, small-scale type to more capital-intensive and highly specialized fish-catching methods. The period since World War II has seen the greatest technological advances in capture fisheries in the country than any other period before that (Spoehr 1984).

Details on the early history of aquaculture are unclear, although people have been farming fish for thousands of years based on evidence of fish farming in the Arab Republic of Egypt and China in 2500 BC and 1100 BC, respectively (Landau 1992). In South-east Asia, brackish-water pond culture can be traced from Indonesia almost 600 years ago (Schuster 1952, as cited by Primavera 1995). This gradually spread to other Southeast Asian countries. In the Philippines, the earliest fishpond record was in Rizal Province in 1863 (Philippine Census of 1921 in Siddall, Atchue, and Murray 1985). At the turn of the century, there were reports of pond culture in the Manila area (Radcliffe 1912, as cited by Primavera 1993).

Traditional aquaculture involved minimal in-puts, small farm size, and low stocking density. This type of fish farming has been practiced in many parts of the world for centuries. Intensification of aquaculture

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Introduction 3

traditional, to extensive, to semi-intensive, and finally to an intensive farming system (Primavera 1991). From being a by-product (from accidental entries into ponds) of milkfish aquaculture, the tiger shrimp industry de-veloped as a separate and important aquaculture com-modity. Traditional and extensive culture shrimp farm-ing systems relied on tidal water exchange and available natural productivity since stocking rates are quite low from less than 1 prawn/m2 (traditional) to 1–3 prawns/m2 (extensive) and maybe in polyculture with milkfish.

1.2 Capture Fisheries and Aquaculture Development in the Philippines

The Philippines’ fisheries production, capture and aquaculture combined, has steadily increased since the 1950s. From 0.230 million tons in 1950, the produc-tion steadily increased to 5.158 million tons, an equiv-alent average growth of 22.4-fold. However, there was a slight decrease in total production from 2011 to 2013 (Figure 1).

The percentage contribution of the Philippines’ fisheries to world production ranged from 1.2 percent in 1950 to 3.1 percent in 2010. The country’s world ranking also improved with its percentage contribution,

from 17 in 1950–1965 to 5 in 2010. In 2013, the country ranked eighth in the world (Figure 2).

The contribution of aquaculture to the coun-try’s production has increased dramatically from just 10.7 percent (25,649 tons) in 1950 to 50.4 percent (4,708,790 tons) in 2013, including aquatic plants (Figure 3). Despite advances in aquaculture, there was −4 percent growth in the fisheries sector for the peri-od 2013 to 2014 compared to 1.2 percent growth in the agriculture and forestry sector for the same period (PSA 2015).

Among the 81 provinces in the country, Pala-wan exhibited the fastest increase in production in the last 34 years. Palawan set an average annual increase of 14,000 tons in production from the years 1980 to 2014. This is way higher when compared to the 1980s’ top producer, Laguna, which rather suffered from an average annual decrease of 5,000 tons in production for the same period (Figure 4).

1.2.1 Capture FisheriesThe average growth of the Philippine marine capture fisheries from 2003 to 2012 is just 4.6 percent. This is low in comparison to China (13.6 percent), Indonesia (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

Prod

uctio

n, to

ns (x

1,0

00,0

00);

Phil.

Pro

duct

ion,

tons

(x 1

00,0

00)

1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010 2011 2012 2013

200

Philippine productionWorld production

0

80100120

604020

140160180

Source: FAO FishStat 2015.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector4

period. Myanmar with 121.4 percent has the highest growth in the world (FAO 2014).

Based on FAO FishStat (2015), total capture fish-eries in the Philippines peaked in 2010 with 2,615,801 tons, equivalent to a more than 12-fold increase from 213,227 tons in 1950 (Figure 5).

In 2014, the total production declined to 2,351,479 tons. This corresponds to about 10 percent decrease in production relative to the 2010s. At the

provincial level, Laguna exhibited the fastest decline in production from 1980 to 2014 (Figure 5).

On the other hand, South Cotabato achieved an average annual increase of 7,000 tons in production for the same period, making it the highest contributor in capture fisheries.

Ninety percent of the total production in cap-ture fisheries is attributed to marine commodities and the remaining 10 percent to inland capture fisheries

Figure 3: Trend of fisheries production in the Philippines

Capture Aquaculture Total

Volu

me

of P

rodu

ctio

n,m

illio

n of

met

ric to

ns

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

6

0

1

2

3

4

5

Source: FAO FishStat 2015.

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

Cont

ribut

ion

to W

orld

Pro

duct

ion

1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010 2011 2012 2013

3.5%

World RankContribution, %

0%

0.5%

1.0%

1.5%

2.0%

2.5%

3.0%

Wor

ld R

anki

ng

1

17

15

13

11

9

7

5

3

Source: FAO FishStat 2015.

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Introduction 5

based on the data of FAO FishStat from 1950 to 2013 (Figure 7).

The major provinces contributing to marine capture fisheries are shown in Figure 8.

Laguna Province is one of the main players in inland capture fisheries. In 2014, the province con-tributed 19 percent to the total production in inland capture fisheries next to Rizal (28 percent), mainly due to production from the country’s largest inland water body, Laguna de Bay, bounded by these two provinc-es (Figure 10). However, it is in this specific subsector that Laguna had the fastest decline in total production in capture fisheries from 1980 to 2014 as shown in Figure 11.

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

Source: Based on PSA 2015 data.

Figure 5: Capture fisheries data for the Philippines

Volu

me

of P

rodu

ctio

n,m

illio

n of

met

ric to

ns

1950

1955

1960

1965

1970

1975

1980

1985

1990

1995

2000

2005

2010

2015

3.0

0

0.5

1.0

1.5

2.0

2.5

Source: FAO FishStat 2015.

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

Source: Based on PSA 2015 data.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector6

1.2.2 AquacultureFrom the 1950s to 1970s, brackish-water aquacul-ture dominated the fish culture scene, contributing to 87 percent of total production while the remaining was mainly from freshwater aquaculture (Figure 12).

Figure 7: Marine and inland capture fisheries data

Volu

me

of P

rodu

ctio

n,m

illio

n of

met

ric to

ns

1950

1955

1960

1965

1970

1975

1980

1985

1990

1995

2000

2005

2010

2015

Inland

3.0

0

0.5

1.0

1.5

2.0

2.5

Marine

Source: FAO FishStat 2015.

Figure 8: Average change in volume of production in Philippine marine capture fisheries from 1980 to 2014

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.

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Introduction 7

In 2014, 15 percent of the 322,668 tons of pro-duction in brackish-water aquaculture came from Pam-panga (Figure 13). In line with this, it was reported to have an average annual increase of 1,000 tons in pro-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 (main-ly fishponds) or about the same as the combined produc-tion 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 com-pared 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 gener-ally confined to seaweeds and other aquatic plants up until the early 1970s. However, since then marine fish aquacul-ture grew in volume and by 2014, marine fish production from aquaculture contributed almost 125,000 tons com-pared to a measly 38 tons in 1972 (Figure 17). Seventy-six

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

Source: Based on PSA 2015 data.

Figure 11: Average change in volume of production in Philippine inland capture fisheries from 1980 to 2014

Source: Based on PSA 2015 data.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector8

In addition, small-farm reservoirs are also pres-ent in the country, which produced almost 100 tons of cultured fish annually. These mainly came from Quiri-no and North Cotabato (Figure 19).

percent of this came from Pangasinan alone. As the top contributor in marine fish aquaculture, Pangasinan had an average annual increase of 5,000 tons in production from 1996 to 2014 (Figure 18).

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

Volu

me

of P

rodu

ctio

n,m

illio

n of

met

ric to

ns

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

0.9

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

Brackish Freshwater Marine

Source: FAO FishStat 2015.

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

Source: Based on PSA 2015 data.

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Introduction 9

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

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.

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

Source: Based on PSA 2015 data.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector10

Dominant fish species cultured are peneid shrimps (mainly tiger shrimps), tilapias (mainly Nile ti-lapia), and milkfish. These three commodities comprised 77 percent of fish aquaculture production by 2013 at a

total volume of 730,000 tons and at an estimated total value of US$1.8 million (Figure 20).

From these three commodities, with the devel-opment of aquaculture technologies for other aquatic

Figure 17: Top aquaculture fishery commodities in Philippine aquaculture

Volu

me

of P

rodu

ctio

n,m

illio

n of

met

ric to

ns

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

0.9

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

Shrimps Milkfish TilapiasOthers

Source: FAO FishStat 2015.

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

Source: Based on PSA 2015 data.

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Introduction 11

food species, the list of aquaculture commodities ex-panded by the 1980s to include crabs and snappers. By 2013, the list included groupers and siganids.

Peneid shrimps were produced in brackish-wa-ter 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 pro-duction. 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 peneid shrimps in 2014 (Figure 21).

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

Source: Based on PSA 2015 data.

Figure 20: Volume of production in Philippine small-farm reservoir in 2014

Source: Based on PSA 2015 data.

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

Source: Based on PSA 2015 data.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector12

the strains developed in the Philippines. A few of these technologies and strains are now being used in other tilapia-producing countries. (Macaranas et al. 1995; Bolivar et al. 1993).

Milkfish (Chanos chanos) on the other hand is a commodity with wide salinity tolerance, making it ideal for culture in all three aquaculture environments: ma-rine, brackish, and freshwater farming systems. From 1950 to the mid-1990s, based on FAO records (Fish-Stat), milkfish was cultured mainly in brackish-water ponds with about a tenth of total production from freshwater aquaculture. The culture of milkfish in fish pens in Laguna de Bay, the largest inland water body in the country, started in the early 1970s (Delmendo and Gedney 1976) and gradually spread to other in-land water bodies like Taal Lake (Tan, Garcia, and Tan 2011) (Figure 25). By 2013, total milkfish production in the three culture environments was at its highest at over 401,000 tons, in which 25 percent came from Pangasinan alone (Figure 26).

But then again, the country’s production gradu-ally picked up. As of 2014, however, it has not yet fully recovered with just 51,000 tons of production valued at US$500,000. This increase can primarily be attributed to Pampanga, which produced 20,000 tons (39 per-cent) of peneid shrimps in 2014. This is followed by Lanao del Norte with 10,000 tons (21 percent) of pro-duction as presented in Figure 22.

In line with this, Pampanga also surpassed 80 oth-er provinces in the country by producing 100,000 tons of tilapia. It is equivalent to 41 percent of the total tilapia produced in 2014. It is 50 percent higher when compared to the second-highest producer, Batangas (Figure 23).

Tilapia culture started off with the Mossambique tilapia (Oreochromis mossambicus) and was gradually re-placed by Nile tilapia (Oreochromis niloticus) (Gupta and Acosta 2004). A number of genetic improvement programs for Nile tilapia have been undertaken by var-ious government institutions as well as universities. The GIFT, Get Excel, FAST, and GMT are just a few of

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

Source: Based on PSA 2015 data.

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Introduction 13

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

Source: Based on PSA 2015 data.

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

Source: Based on PSA 2015 data.

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

Source: Based on PSA 2015 data.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector14

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

Source: Based on PSA 2015 data.

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INCREASED POPULATION AND 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.

2

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector16

In 1965, fish consumption of Filipinos was at 23.09 kg/capita/year. This increased to 31.58 kg/cap-ita/year by 2013, with the highest consumption of 35.64 kg/capita in 2010 (Table 1). This translates to a total fish consumption of 3.1 tons in 2013 and 3.3 tons in 2010. If the country’s population grows as expect-ed, with a population projection of 110.97 million in 2020, fish consumption would reach 3.5 tons using the

average consumption for the last four decades which is close to 32 kg/capita/year.

With regard to self-sufficiency in fish produc-tion compared with fish consumption, there was a defi-cit from 1961 to 1975. To address the deficit in fish supply for local consumption, various programs to improve capture fisheries and aquaculture production were undertaken by the Government’s BFAR through

Figure 27: Philippine population growth

Mill

ion

1969 1980 1991 2002 2013

120

20

40

60

80

100

Source: Trading Economics 2015.

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

YearPer Capita Fish

Consumption, kg/yearTotal Fish Consumption,

tonsTotal Fish Production,

tonsSurplus/Deficit,

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).

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Increased Population and Drive For Economic Growth Pushed For Increasing Fisheries Production In The Philippines 17

its Ginintuang Masaganang Ani for Fisheries Program for 2002–2004, with specific developmental road maps for various commodities (BFAR 2015).

2.2 Contribution of Capture Fisheries and Aquaculture in Philippine Economy

The fisheries sector contributed almost PHP 242 mil-lion in 2014 to the country’s economy (Figure 28).

This translates to 1.9 percent in 2013, down from a peak of 4.9 percent in 1987 at constant prices, 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).

With regard to gross value added (GVA) contribu-tion, the fisheries sector contributed 18.5 percent in 2013, with a high of 24.4 percent in 2009 (since 1988) and an average of 20 percent at constant prices (Figure 30).

On the other hand, fishery exports far exceeded imports with a balance of trade of US$1,086 million

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

Valu

e of

Pro

duct

ion,

mill

ion

PhP

19861980 1982 1984 1988 1990

Aquaculture Capture Fisheries Total

1992 1994 1996 1998 2000 2002 2004 2006 2008 2010 2012 2014

300

0

50

100

150

200

250

Source: PSA 2015.

Figure 29: Contribution of fisheries to the Philippines’ GDP

GDP

at C

onst

ant P

rice

19851978 1980 1982 1988 1990 1992 1994 1996 1998 2000 2003 2005 2007 2009 2011 2013

6

0

1

2

3

4

5

Source: BFAR 1978 to 2013.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector18

in 2013 (Figure 31). Major exports in terms of val-ue are tuna, seaweeds, crabs, and shrimps, equivalent of 28.91 percent, 9.48 percent, 3.65 percent, and 2.86 percent, respectively, as of 2013 (BFAR 2013).

Of the three top fish commodities cultured, im-port dependency ratio is relatively high for shrimps and prawns and low for milkfish and tilapia (Figure 32).

In the last three decades, employment or engage-ment in the fisheries and aquaculture sector has grown faster than the world’s population and employment in traditional agriculture. Eighty-six percent of fishers and

fish farmers worldwide live in Asia. China, India, Indo-nesia, the Philippines, and Vietnam have a significant number of fishers and fish farmers (FAO 2008). Most fishers and fish farmers are small-scale, artisanal fishers, operating on coastal and inland fishery resources. In the Philippines, about a million people are employed in the fisheries and fish farming sector. Available census data show that in the 1990s, 990,872 people were under this sector, which is estimated at 5 percent of the country’s population. Fishermen in the municipal fisheries sec-tor consisted 68 percent (675,677). Those involved in

Figure 30: Contribution of fisheries to GVA at constant prices

GVA

at C

onst

ant P

rice,

%

1991

1988

1989

1990

1992

1993

1995

1994

1996

1997

1999

1998

2000

2002

2004

2006

2008

2010

2012

2003

2005

2007

2009

2011

2013

25

0

5

10

15

20

Source: BFAR 1988 to 2013.

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

Valu

e, b

illio

n Ph

P

45

0

25

15

20

10

5

30

35

40

19831977 1979 1981 1985 1987 1989 1991

Exports Imports

1993 1995 1997 1999 2000 2001 2003 2005 2007 2009 2011 2013

Source: BFAR 1977 to 2013.

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Increased Population and Drive For Economic Growth Pushed For Increasing Fisheries Production In The Philippines 19

aquaculture and commercial fisheries sectors comprise 26 percent (258,480) and 6 percent (56,715), respec-tively (BFAR 19977–2014). In the 2002 census, the number of people involved in fisheries increased to more than 1.6 million. There was a marked increase in the number of people employed in the municipal fisheries sector at close to 1.4 million people (85 per-cent), while aquaculture was slightly down to 226,195 (14 percent) and the commercial sector further reduced to just 16,498 (1 percent) (BFAR 1977–2014).

Those engaged in the culture of milkfish know the profitability of this enterprise. Milkfish aquaculture profit margins averaged 110 percent and were in the range of 63 to 153 percent between 2001 and 2013 (Figure 33). Production cost remained fairly constant from 2001 in the range of PHP 23.5–39.2 per kilo-gram, while farm gate price tended to increase from a low PHP 53.5 per kilogram to a high PHP 87.7 per kilogram.

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

Impo

rt D

epen

denc

y Ra

tion

Milk

fish

and

Tila

pia

Impo

rt D

epen

denc

yRa

tion

Shrim

ps

0.18

0

0.10

0.06

0.08

0.04

0.02

0.12

0.14

0.16

9

0

5

3

4

2

1

6

7

8

19961990 1992 1994 1998 2000 2002 2004

Milkfish Tilapia

2006 2008 2010 2012 2014

Shimps and Prawns

Source: PSA 2015.

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

Cost

, PhP

Profi

t, %

100

0

60

4050

30

1020

708090

200

50

100

150

20072001 2003 2005 2009 2011 201320042002

Profit, %Farmgate price per Kg, PhP

2006 2008 2010 2012

Production cost per Kg, Ph

Source: PSA 2015.

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APPROACHES TO IMPROVE FISHERIES 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.

3

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector22

infrastructure and equipment that will allow fisherfolk and investors to operate in a cost-effective and secure manner; and (d) promote environment-friendly inputs and farm management practices.

A ‘mariculture highway’ in the eastern and west-ern seaboard of the country was envisioned to provide a sustainable strategy to ensure food security from aqua-culture and to contribute to the country’s economic growth. These planned MPs will prevent the unregu-lated establishment of mariculture facilities across the country without regard for the overall sustainability of the industry. Figure 34 shows the process for establish-ing an MP in a designated area.

Careful site evaluation is done before a site is con-sidered for MP development. If the site is found suitable, the local Sanguniang Bayan or Sanguniang Panlungsod enacts an ordinance declaring the area as an MP. If the BFAR and the local government unit (LGU) involved agree, a memorandum of agreement is signed by the BFAR and the LGU to develop and co-manage the MP. An Executive Management Council manages the MP.

The first MP in the Philippines was established in 2001 in the Island Garden City of Samal in Davao. Since then a number of mariculture areas have been de-veloped (Figure 35).

Table 2 shows the operation of two MPs, one in Panabo and another in San Juanico. Aside from the production and economic benefits of these two MPs,

3.1.1 Conversion of Mangroves to Fishponds

At least 35 percent of the world’s mangrove forests have been lost in the last two decades, which far exceeds the loss of two other significantly threatened environments: tropical rain forests and coral reefs (Valiela, Bowen, and York 2001).

Mangrove areas in the Philippines were around 400,000 to 500,000 ha at the turn of the century (Brown and Fisher 1918, as cited by Primavera and Agbayani 1997). This declined to 132,000 ha by 1990 (Auburn University 1993, as cited by Primavera and Agbayani 1997). The decrease in mangrove area in the last few decades has been traced back to the conver-sion of these areas into milkfish and shrimp ponds. There was only around 61,000 ha of fishponds in the 1940s. This expanded to 223,000 ha by 1990 (Prima-vera 1994) at the peak of fishpond construction from mangrove areas, between 1988 and 1990 alone. Initial-ly, milkfish monoculture dominated the brackish-water pond system, but the development of culture technol-ogies for the peneid shrimp Penaeus monodon, or black tiger shrimp, transformed many of these converted mangrove areas to the culture of this high-value com-modity with excellent export potential.

3.1.2 Establishment of Mariculture ParksThe Philippines’ BFAR spearheaded the establishment of MPs in selected coastal areas of the country. The concept of an MP is similar to the establishment of an industrial estate on land where the Government in partnership with the local Government and private sec-tor puts up the facilities for a managed marine aquacul-ture enterprise. The rationale behind the establishment of MPs is to address issues such as declining capture fisheries due to over exploitation, destructive fishing methods, pollution, and habitat deterioration. The MP project aims to (a) generate employment and alle-viate poverty in the countryside; (b) promote marine fish culture as an alternative livelihood for marginal-ized fisherfolk; (c) develop an area with appropriate

Figure 34: Process of establishment of MPs in the Philippines

An ExecutiveManagement

Council managesthe MP

Initial environmentassessment

If site issuitable

If LGU andBFAR agree

SanguniangBayan/Panglunsod

enacts an ordinancedeclaring the area as MP

BFAR and LGU sign aMOA to develop andco-manage the MP

Source: Adora 2009.

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Approaches to Improve Fisheries Production 23

fisherfolk in the area noted increased fish recruitment and reduction, if not elimination, in unregulated, il-legal, and destructive fishing in the area, probably due to active management of the MP and its surrounding areas. The total area planned for MP development is 50,150 ha, but only a small portion of this has been fully established (Salayo et al. 2012).

3.1.3 Establishment of Inland Water Aquaculture Facilities

The declining fish catch in the Philippines’ largest lake, Laguna de Bay, provided the impetus for the intro-duction of milkfish culture in fish pens in this lake. Heretofore, milkfish has been primarily cultured in

brackish-water ponds. Milkfish was thought to be an ideal species to utilize the eutrophic lake’s primary pro-ductivity 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.

The infrastructure of fish cages and pens in in-land water bodies for aquaculture had adverse impacts on the environment. Cage and pen structures affect water bodies since (a) they take up space which es-sentially competes with other uses of the inland water body; (b) they alter flow regimes and circulation pat-tern which in turn affects oxygen, sediment, as well as plankton and fish larvae; and (c) they adversely alter the aesthetic quality of the area (Beveridge 1984).

Enclosures such as pens and cages are a more open-type of fish rearing system than land-based fa-cilities such as ponds, tanks, and raceways; thus, there is a greater degree of interaction between cages and penned fish and the outside environment (Beveridge 1984). Nutrients from unconsumed feeds, excreta, and the inevitable mortalities inside the pens/cages may di-rectly affect the aquatic environment, often resulting in eutrophication.

Figure 35: Site of MPs for establishment in the Philippines

Source: BFAR website.

Table 2: Performance of two MPs

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 industry, no.

61 178

Year of data covered 2006 to 2009 2004 to 2009

Source: Adora 2009.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector24

3.2 Practices to Prepare and Improve Culture Environment

With the intensification of aquaculture, the use of chemicals and other products during different phases of production has become inevitable. Fertilizers, water and soil treatment chemicals, disinfectants, antibiotics, and pesticides (molluscicides, piscicides, algicides) are among the most common groups of compounds used in aquaculture. Table 3 lists these various compounds used in Philippine aquaculture.

Table 3: Groups of chemicals and additives used in aquaculture

Group Compound/Product Reference

Inorganic fertilizers Ammonium phosphate a, c

Ammonium sulfate a, c

Calcium nitrate a

Diammonium phosphate c

Nitrogen, phosphorus and potassium (NPK)

a

Organic fertilizers Horse manure c

Chicken manure a, c

Cow manure a, c

Molasses (sugar waste) c

Pig manure a, c

Urea a, c

Water and sediment Calcium carbonate a, b, c

Treatment compound Calcium hydroxide a, c

Dolomite a, c

Sodium thiosulfate a

Zeolite a

Pesticides Fungicides

Fentin acetate c

Malachite green a

Trifluralin a

Herbicides

2,4-Dichlorophenoxyacetic acid

a

Insecticides

Organochlorine

Endosulfan a, c

Organophosphate

Table 3: Groups of chemicals and additives used in aquaculture

Group Compound/Product Reference

Azinphos-methyl a

Diazinon a

Trichlorfon c

Piscicides

Nicotine a, c

Rotenone a

Saponin (teaseed cake) a, b, c

Disinfectants Benzalkonium chloride a

Calcium hypochlorite a, c

Calcium sulfite a

Copper complex solution a

Formaldehyde b, c

Iodine a

Potassium monopersulfate a

Potassium permanganate a

Sodium cyanide c

Sodium hypochlorite a

Antibiotics Macrolides

Erythromycin a, b, f, g

Nitrofurans

Furazolidone a, b, c, f

Nifurpirinol a

Quinolones

Oxolinic acid a, b, f, d, g

Sulfonamides

Sulfamethoxazole a

Sulfamerazine a

Sulfadimethoxine a

Tetracyclines

Tetracycline a

Doxycycline a

Oxytetracycline (OTC) a, b

Others

Chloramphenicol a, b, e, f, g

Nalidixic acid a

Rifampicin a

Trimethoprim a

Source: Rico et al. 2012, © Wiley Publishing Asia Pty Ltd; Sapkota et al. 2008, (c) Elsevier. Reproduced with permission from publishers; further permission required for reuse.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 Bengtsson 2001; f - Primavera 1993; g - Primavera et al. 1993.

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Approaches to Improve Fisheries Production 25

3.2.1 Application of Fertilizers and Other Chemicals

Asia has a long history of organic and inorganic fertil-izer use in pond culture. Often, in extensive systems, fertilizers are the only input, most especially in small-scale, single pond operation. Almost all extensive and semi-intensive aquaculture, with few exceptions, rely on fertilizers and manure (de Silva and Hassan 2007). The Philippines imports most of its fertilizer needs as self-sufficient supply is only available for diammonium phosphate. Chicken manure is the most readily avail-able and therefore the most commonly used organic fertilizer. Low-cost, unprocessed organic fertilizers are preferred by Philippine aquaculture operations, but the use of compost has also become popular. The Phil-ippine Government has strongly supported the fertil-izer industry with its deregulation in 1986 to encour-age the entry of more traders. Quality assurance and monitoring, price control, and incentives are being implemented in line with the Agriculture and Fisheries Modernization Act (AFMA) under Republic Act 843C (Sumagaysay-Chavoso 2007).

In pond culture, inorganic and organic fertiliz-ers are applied in extensive and semi-intensive systems to stimulate growth of natural food. In extensive pro-duction systems, application of fertilizers allows for the growth of natural food in sufficient quantity to com-pletely do away with commercial feeds. Extensive sys-tems require heavy inputs of fertilizers since the growth of natural food should be sufficient to support fish growth, while semi-intensive and intensive systems re-quire less fertilizers since the cultured fish are provid-ed with formulated feeds (Cruz-Lacierda et al. 2008). Monoammonium phosphate (16-20-0), diammonium phosphate (18-46-0), urea (46-0-0), and ammonium sulfate (21-0-0) are the most widely used fertilizers in Philippine aquaculture. In combination with lime, am-monium sulfate is also used to kill unwanted species as part of pond preparation before stocking. Table 4 shows the use of various organic fertilizers in milkfish (Chanos chanos) and peneid shrimp (Penaeus monodon) ponds in the Philippines based on results of surveys in 1995–1996

(Cruz-Lacierda, de La Pena, and Lumanlan-Mayo 2000) and in 2006–2007 (Cruz-Lacierda et al. 2008).

Organic fertilizers, mainly animal manure, is also widely used in Philippine aquaculture. A wide va-riety of animal waste and their combination is used. Chicken manure is the most widely used and as per survey results between 2006 and 2007, 85 percent of the 39 respondents use this organic fertilizer for their milkfish ponds while none of the 40 respondents en-gaged in shrimp culture use this organic fertilizer. Cow and carabao manure are also used by 3 percent of respondents for milkfish and 13 percent of respon-dents for shrimp culture. Horse manure is used by only 3 percent of the respondents for shrimp culture while pig manure is used by 5 percent of respondents for the polyculture of milkfish and shrimp (Cruz-Lacierda et al. 2008). Table 5 shows a summary of the organic fer-tilizers used in aquaculture from two survey periods: 1996–1997 (Cruz-Lacierda, de La Pena, and Luman-lan-Mayo 2000) and 2006–2007 (Cruz-Lacierda et al. 2008). With regard to use of organic fertilizers, there is a large increase in the rate of application for both the pond preparation phase based, for example, for chicken manure, from 0.5 to 3 tons/ha in 1995–1996 to 1–10 tons/ha in 2006–2007 for milkfish culture.

Aside from fertilizers, there are other chemicals used in the preparation of ponds before stocking to improve soil and water quality. These chemicals act as soil or water conditioner. Lime is applied to adjust the pH of the pond soil to neutral or alkaline to promote volatilization of ammonia. Lime is also a disinfec-tant. Application is broadcasting on dried and caked pond bottom. Commonly used types of lime in pond preparation are agricultural lime (CaCO3), hydrated lime (Ca(OH)2), and dolomite (MgCO3). For soils with very low pH and for new ponds, hydrated lime is the choice, while agricultural lime is for old ponds (Cruz-Lacierda et al. 2008). To a limited extent some farmers even use liming to kill potential pests and predators. To remove ammonia and other nitrogenous compounds, zeolite is applied (Rico et al. 2012). Many of these water and soil conditioning chemicals have

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector26

short environmental life and are relatively harmless, al-though they do affect water quality. Table 6 shows the application rates for some of these chemicals in pond preparation.

3.2.2 Application of Piscicides and Molluscicides

Typical for pond preparation before stocking any com-modity for culture is the eradication of other fish species and molluscs which may prey on the cultured species or compete for food, oxygen, and space in the culture environment. As a routine part of pond preparation,

chemical agents are applied to kill fish and molluscs in the pond bottom. Table 7 shows some of the common piscicides and molluscicides in aquaculture ponds.

3.3 Practices to Improve Production

3.3.1 Use of Hormones and Growth Promoters

Exogenous hormones, particularly gonadotropins, have been used for years to induce final maturation of captive female broodfish. Hormone products such as lutein-izing hormone releasing hormone-analog (LHRHa),

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 (every 15 days till harvest)

20–100 kg/ha

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 (every 15 days till harvest)

5–100 kg/ha

Solophos (0-20-0) Shrimp/pond preparation 3–20 kg/ha —

Shrimp/rearing phase 5–10 kg/ha —

Ammonium sulfate (21-0-0)Calcium nitrate

Shrimp/pond preparation 100–500 kg/ha 10–100 kg/ha

Shrimp/pond preparation (broadcast) 3–50 kg/ha —

Shrimp/rearing phase (broadcast) 5–10 kg/ha —

Source: Cruz-Lacierda, de La Pena, and Lumanlan-Mayo 2000; Cruz-Lacierda et al. 2008.

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Approaches to Improve Fisheries Production 27

human chorionic gonadotropin (HCG), and other hormone containing products such as OvatideTM and OvaprimTM (both are a combination of gonadotropin and a dopamine antagonist). Hormones such as these

have been used in the Philippines for commodities such as milkfish, sea bass, bighead carp, catfish, grou-pers, and many other species (Kungvankij et al. 1986; Tan-Fermin and Emata 1993; Liao et al. 1979; Marte et

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 (pond preparation, broadcast

100–3,000 kg/ha (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/pig manure)

— 1,000 kg/ha (pond preparation; tea bags) —

2006–2007 Chicken manure 1–10 tons/ha (pond preparation)

— 0.5–10 tons/ha (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.

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 (CaCO3)

0.2–6 tons/ha 1–10 tons/ha; 200–300 kg/ha (rearing phase)

1–5 tons/ha; 140–400 kg/ha (rearing phase)

Hydrated lime (Ca(OH)2)

0.2–2 tons/ha 0.4–2 tons/ha; 50–200 kg/ha (rearing phase)

0.75–1.5 tons/ha; 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)

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector28

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.

Another use of hormones in aquaculture is for sex reversal, either for masculinization or feminization. The culture of monosex fish has been shown to improve growth compared to mixed sex culture since a greater portion of energy in feed is channeled toward somatic

growth rather than reproduction (Chakraborty et al. 2011). The hormones 17-α-methyltestosterone (MT) and estradiol-17β are the most common hormones for masculinization and feminization, respectively (Pan-dian and Sheela 1995). In the Philippines, the most common species that undergo sex reversal through hormone treatment of MT are tilapia. Since the mid-1980s commercial-scale sex reversal, mainly masculin-ization, through MT treatment has been practiced in many tilapia-producing countries including the Philip-pines (Popma and Green 1990). Diets are mixed with MT at 10 mg/kg at a rate of 15–20 percent of BW per day of tilapia for 20–30 days (Popma and Green 1990; Chakraborty et al. 2011). After this method, 97–100 percent phenotypically male tilapia can be achieved and ready for grow-out.

3.3.2 Use of AnestheticsAnesthetics are employed in fisheries and aquaculture in instances when the fish need to be transported or han-dled, which is stressful to the fish. Stress can result in immunosuppression, physical injury, and even death to the fish. During transport, anesthetics are used to

Table 8: Sample of hormone dosage used for induced spawning of the Asian catfish Clarias microcephalus and bighead carp Aristichthys nobilis

Hormone Catfish Bighead Carp

HCG 4 IU/g body weight (BW)

2,000 IU/kg BW (female); 1,000 IU/kg BW (for male)

LHRHa 0.05 μg/g BW 20–50 μ g/kg BW (female); 10–25 μ g/kg BW (male)

OvaprimTM 0.5 μ L/g BW 0.5 ml/kg BW (female); 0.25 ml/kg BW (male)

OvatideTM 0.2 μ L/g BW 0.5 ml/kg BW (female); 0.25 ml/kg BW (male)

Source: Tan-Fermin et al. 2008; Gonzal et al. 2001.Note: OvaprimTM and OvatideTM are commercial preparations containing LHRHa and domperidone.

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.

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Approaches to Improve Fisheries Production 29

reduce metabolism which in turn reduces oxygen con-sumption and excretion rates (Coyle, Durborow, and Tidwell 2004; Strange and Shreck 1978). Immersion in anesthetic bath is the most common way anesthetics are applied to fish and crustaceans. For large-size fish, the anesthetic solution may be sprayed to the gills. The anes-thetic is absorbed through the gills and enters the blood stream to take effect on the fish. Table 9 is a list of com-mon anesthetics and their dosage for various aquaculture commodities. Environmental and human safety regula-tions on the use of anesthetics in aquaculture are not yet in place in the Philippines. In the United States, only

MS-222 is registered for use in food fish and requires a 21-day withdrawal period (Coyle, Durborow, and Tidwell 2004). Thus far, there is no such list of approved anesthetics for use in aquaculture in the Philippines.

3.4 Practices to Improve Aquatic Animal Health

3.4.1 Use of Antibiotics and AntimicrobialsAntibiotics and antimicrobials are generally substances that kill or suppress the growth of microorganisms.

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);0.5 ml/Lc (brood stock)

125 mg/Ld

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.

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 5–7 days

1–2.5 g/kg feed20 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.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector30

Antibiotics are substances produced by or derived from specific microorganisms and can destroy or inhibit the growth of pathogenic organisms and prevent or treat infection. The use of antibacterial treatment in aqua-culture became widespread in the 1970s when bacterial pathogens became increasingly prevalent in aquacul-ture. However, antibacterial chemotherapy has been in practice for over 60 years, using sulphonamides to treat furunculosis in trout and tetracyclines against gram-negative pathogens (Inglis 2000). Method of dosing of these antibiotics may be through (a) immer-sion or water bath; (b) injection; (c) topical applica-tion; or (d) incorporation as a feed ingredient. The last is the more common approach particularly for shrimp culture. With the intensification of shrimp culture, fueled by its attractive price not only locally but more so in the international market, problems with shrimp diseases causing high mortalities need to be addressed to maintain production volume. Antibiotics and anti-microbial agents became the drug of choice to address disease problems.

3.4.2 Use of Chemotherapeutants As aquaculture operations intensified, disease occur-rence from pathogenic organisms became a threat to production. These chemicals or drugs are selectively toxic to the causative agent of the disease. For instance, in shrimp culture, the prevalence of the luminous bacte-ria Vibrio has resulted in the devastation of many farms in the country, eventually resulting in the sharp decline in shrimp production not only in the Philippines but

also in other shrimp-producing countries. To address the problem of Vibrio infection, it has become a prac-tice to disinfect inflowing water in some shrimp farms. Chlorine (as calcium hypochlorite) or formalin is used to treat the water in reservoirs before use in the shrimp ponds (Cruz-Lacierda et al. 2008). Table 11 shows the dosage of disinfectants used in monoculture shrimp ponds and in polyculture with milkfish.

3.5 Practice to Diversity Cultured Commodities

3.5.1 Introduction of Exotic Aquatic Species

New aquatic species from other countries are introduced to boost both capture fisheries and aquaculture produc-tion. Figure 36 shows the recorded number of intro-duced exotic species in the Philippines since the early 1900s. An estimated 45 percent of fish introductions are for aquaculture (food fish) purposes and 42 percent for the ornamental fish industry, 6 percent for recreational fishing, 6 percent for mosquito control (Guerrero 2014), and the remaining are probably incidental introductions

Table 11: Disinfectants used in black tiger shrimp brackish-water farms in the Philippines in 2006–2008*

Chemical Shrimp (n = 40) Polyculture (n = 21)

Calcium hypochlorite 5–100 ppm (33%) 25–50 ppm (10%)

Formalin 5–20 ppm (10%) —

Source: Cruz-Lacierda et al. 2008.Note: * Values in parenthesis are percentage of farms surveyed; n=number of farms surveyed.

Figure 36: Number of aquatic animal species introductions in the Philippines in the various decades

Num

ber o

f Exo

tic S

peci

esIn

trod

uced

with

Rec

ords

1900

s

1910

s

1920

s

1930

s

1940

s

1950

s

1960

s

1970

s

1980

s

1990

s

2000

s

60

0

10

20

30

40

50

Source: Cagauan 2007.

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Approaches to Improve Fisheries Production 31

as ‘tag-along’ species. The peak of introduction of exotic fish species in the country was in the 1970s with more than 50 species introduced (Cagauan 2007).

Introduction of exotic species is the second lead-ing cause for the loss of biodiversity, after habitat de-struction (Williams et al. 1989; IUCN 1999). Many fish species introduced for aquaculture have proven to be economically beneficial to many farming communi-ties in the world, including the Philippines. Among the top freshwater species being farmed in the Philippines is an introduced species, the Nile tilapia Oreochromis niloticus. Although many countries consider the intro-duction of this species as a nuisance and consider the species to be invasive (Linde-Arias et al. 2008; Angien-da et al. 2011), many more countries have accepted this species as an important aquaculture commodity.

One of the early records of fish introduction to the Philippines was in 1915 with the release of com-mon carp (Cyprinus carpio) from Hong Kong in Lake Lanao in Mindanao (Villaluz 1966; Escudero 1994). Fortunately, this species did not thrive well and is now considered nearly decimated in this lake. Another cy-prinid which has grown in importance to freshwater aquaculture, especially in Laguna de Bay, is the bighead

carp, Aristichthys nobilis, introduced from Taiwan in 1968 (Guerrero 2014). Table 12 shows a list of some species introduced to the Philippines, either as food fish or for the ornamental fish industry, that have become invasive or have the potential to become invasive.

3.5.2 Translocation of Aquatic SpeciesEven native fish species are not immune from being introduced to other bodies of water where they are not part of the native population. The translocation of native species from one drainage system to another in the same country is a widely accepted method for enhancement of many natural waters around the world (Innal and Erk’akan 2006). This may either be inten-tional or unintentional. Translocation may be a way of enhancing fisheries productivity. An example of inten-tional introduction is the case of milkfish Chanos chanos in Laguna de Bay for the fish pen culture industry. Milk-fish is a marine species but with euryhaline characteris-tics that enable it to be cultured in a variety of aquatic environments, from marine cages to brackish-water ponds to freshwater fish pens (Bagarinao 1999). The commodity is continuously being produced in a wide

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.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector32

range of culture environments, including other lakes in the country, because this is a preferred food fish for Filipinos.

Translocation may also be a method to conserve critically overexploited aquatic commodities, as in the case of the reef gastropod Trochus niloticus in the Phil-ippines. This species’ population has dwindled due to

overfishing in the country’s reefs, not for food but for the production of mother-of-pearl buttons. It has been declared as a threatened species in the country. Encour-aging results in the translocation of wild juveniles of Trochus niloticus into other sites proved to be a prom-ising strategy for the conservation of this endangered species (Dolorosa, Grant, and Gill 2013).

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PHYSICAL IMPACTS

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

Man

grov

e/Po

nd a

rea

(x 1

03 ha)

1920

1940

1945

1950

1955

1960

1965

1970

1975

1980

1985

1990

60

0

10

20

30

40

50

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

Source: Primavera 1991; Primavera 1995.

4

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector34

was no active government support. Upon the creation of the BFAR in the late 1940s, funds for pond construction became available (mainly through international loans). Mangroves were considered ‘valueless land’ (as quoted from Carbin 1948 as cited by Primavera 1995) at that time and conversion to brackish-water milkfish pond was deemed a more useful alternative. Thus began the accel-erated conversion of mangroves to brackish-water ponds at a rate of 5,000 ha/year in the 1950s and 1960s. Con-version slowed down to 800 ha/year in the 1970s when mangrove areas were placed under the joint jurisdiction of the fisheries and forestry bureaus and there was a move to-ward conservation. As the technology for shrimp culture developed, more mangroves were converted into ponds.

The host of ecosystem services provided by man-groves which turned out to be far more valuable was left unaccounted for during the initial period of conversion into ponds. It was only with the establishment of set parameters for valuation of various ecosystem services that it now has become apparent that mangroves, left as is, have far more economic, environmental, and bio-logical benefits than converting them to fishponds, and not the ‘valueless land’ they were deemed to be.

Mangrove ecosystem-derived services include (a) interception of land-derived nutrients, pollutants, and suspended matter before these reach deeper water (Tam and Wong 1999); (b) export of materials that support nearshore food webs including shrimps (Sase-kumar et al. 1992); (c) protection of vulnerable coastal areas from storm surges that have recently destroyed local communities in the country (Kathiresan and Ra-jendran 2005; Alongi 2008); (d) prevention of coast-al erosion through sediment stabilization (Marshall 1994); and (e) nursery and spawning areas for a variety of commercially important fish, shellfish, and molluscs (Sasekumar et al. 1992). With the loss of mangroves, important subsidies to subsistence uses and ecological, economic, and conservation uses are also lost. It is in-teresting to note that the decrease in mangrove areas in various countries is inversely correlated with an increase in GDP but not generally correlated with population (Valiela, Bowen, and York 2001).

4.1.2 EutrophicationEutrophication results from the heavy inputs of nutri-ents in the aquatic environment, mainly from uncon-sumed feeds, aquatic animal wastes, and other inputs into the aquatic system to boost production. A study on nitrogen and phosphorus utilization of formulated feeds under controlled laboratory conditions shows that an equivalent of only 33 percent of nitrogen and 29 percent of phosphorus is retained in fish (as bio-mass) and the rest is lost through fecal and urinary excretion (Cuvin-Aralar 2003). Since this was done in the laboratory, the feed ration was visibly consumed by the fish with some unquantified, but considered, minor nutrient losses through leaching.

Feed conversion rates vary with species, feeding strategy, and feeding management. Overfeeding results in high feed conversion ratios (FCRs) with excess nutrients entering the culture environment as organic sediments or dissolved nutrients in the water column. Nitrogen and phosphorus loading rates from one ton of shrimp harvest have ranged from 10 to 117 kg of nitrogen and 9 to 46 kg of phosphorous, depending on FCR (White et al. 2008). Table 13 shows model estimates of amounts of nitrogen and phosphorus released to the aquatic environment from aquaculture as a function of FCR.

David et al. (2009) documented the increasing nutrient flux in sediment cores from aquaculture activi-ties in a number of marine aquaculture sites in the Phil-ippines: Honda Bay and Malampaya Bay in Palawan,

Table 13: Estimated organic matter and nutrient loading for one ton of harvested shrimp released at different FCRs

FCROrganic matter

kg/tonNitrogenkg/ton

Phosphoruskg/ton

1 500 26 13

1.5 875 56 21

2 1,250 87 28

2.5 1,625 117 38

Source: Asian Shrimp Culture Council 1993, as cited by White et al. 2008.

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Physical Impacts 35

Manila Bay, Bolinao in Pangasinan, and Milagros Bay in Masbate. The sites have varying degrees of aquacul-ture activity. Results show a narrow concentration range for nitrogen from older core samples when compared to newer ones. On the other hand, phosphorus showed significantly higher levels in younger or more recently deposited sediments. Sediments deposited years ago and older had 20 ppm phosphorous. On the other hand, a 2–3-fold increase in phosphorous levels was noted in sediments deposited within the last 15 years. Phospho-rous sediment profiles reflected the intensity of aqua-culture activities in the different sites. Honda Bay and Malampaya Sound in Palawan are sites where aquacul-ture activities had lower aquaculture intensity. Manila Bay has about 39 km2 of fish cages which are adjacent to urban centers. Bolinao has more than 1,100 fish cages, mainly milkfish (Chanos chanos), and Milagros Bay is a developing aquaculture site with shellfish as the ma-jor product. Phosphorous concentrations in these sites ranged from 10 to 90 ppm. Table 14 summarizes the phosphorous values obtained for the study sites.

A study is currently being undertaken by the National Fisheries Research and Development Institute (NFRDI) on nutrient buildup from aquaculture ponds in the provinces of Bulacan, Bataan, Cavite, and Pam-panga and the National Capital Region, all surround-ing Manila Bay.

An indirect impact of eutrophication is mass fish kill. Mass fish kill is a common occurrence in aqua-culture operations in the Philippines and has incurred huge financial losses for the aquaculture investor. In La-guna de Bay, 60 percent of mass fish mortalities record-ed between the 1970s and the late 1990s were attribut-ed to low dissolved oxygen, secondary to massive algal bloom due to eutrophication (Cuvin-Aralar 2001). The cause of massive algal bloom is excess nutrients in the lake, which in turn is due to eutrophication as has been discussed in the previous section. More recent incidents of mass fish kills in different regions of the country were also documented by the BFAR from 2005 to 2014 (Bantaya, pers.comm.). Of the more than 300 inci-dents of mass fish kills, almost 40 percent were because of poor water quality due to dissolved oxygen depletion and elevated ammonia. A number of instances of oxy-gen depletion were due to algal blooms. Interestingly, a few incidents of mass fish mortalities were also reported as being caused by agricultural pollution run-offs into inland waters with aquaculture activities. In Bolinao, Pangasinan, an important site for milkfish aquaculture, the site has experienced environmental changes due to these mariculture activities which release organic mat-ter from unconsumed feed and fecal material that ac-cumulate in the sediment. A massive fish kill incident in 2002 occurred in the area associated with the bloom of a dinoflagellate, accompanied by a <2 mg/l dissolved oxygen level. Increase in nutrient levels over a 10-year period (1995–2005) in the area has been reported (Mc-Glone et al. 2008). Ammonia has reportedly increased by 56 percent, nitrite by 35 percent, nitrate by 90 per-cent, and phosphate by 67 percent as the waters became increasingly eutrophic.

Taal Lake has multiple uses and benefits such as for open water fisheries, commercial aquaculture, recre-ational activities, navigation routes, and water source. Of particular interest are immense aquaculture activities in the lake that started in the 1980s through which ti-lapia (Oreochromis niloticus) and milkfish (Chanos cha-nos) culture was introduced (Papa and Mamaril 2011). The proliferation of fish pens and cages has affected the

Table 14: Comparison of phosphorus values from marine aquaculture sites in the Philippines

Site Characteristics P-range, ppm

Malampaya Sound

Capture fisheries; shellfish culture

15–85

Honda Bay Less aquaculture development 22 (average)

Manila Bay 39 km2 of fish cages 20–60

Bolinao Bay 1,100 fish cages (milkfish) 20–90

Milagros Bay Developing aquaculture site; mainly shellfish

15–40

Baseline Value 15–20

Source: David et al. 2009.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector36

water quality of the lake. It is estimated that 64 percent of the nitrogen and 81 percent of the phosphorus con-tents of fish feed are released into the lake environment (Edwards 1993). Yambot (2000) calculated that for ev-ery 1.5 tons of fish feed given, 16 kg of phosphorus is released into Taal Lake waters. Further, the excess fish feed and fish feces contribute to the increased organic material that settles at the bottom of the lake. Decom-position of this organic matter releases hydrogen sulfide (H2S) and other toxic gases (White et al. 2008).

Significant fish kill occurrences in Taal Lake have created major economic setbacks in the area. One 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 event was attributed to an interplay of factors such as lake overturn, water pollution, change in season (that is, from summer to rainy season), changes in wind stress, and intermittent rainfall (BFAR 2011).

From 1998 to 2011, lake overturn and pollution are the major causes of reported fish kill in Taal Lake (Figure 38) (Magcale-Macandog et al. 2013). Increase in wind turbulence and low atmospheric temperature cools the lake water surface layer (epilimnion) and

erodes the thermal stratification of the water column (Balistrieri et al. 2006; Caliro et al. 2008; Marti-Car-dona et al. 2008). In combination with the pressure of strong winds, mixing of water occurs. This transports the low dissolved oxygen and reduced chemical sub-stances such as hydrogen sulfide (H2S), nitrite (NO2), and ammonia (NH3) from the lake bottom to the wa-ter surface, as well as mixes them in localized portions of the lake. The lake then goes into a state of hypoxia characterized by low dissolved oxygen, that is, below 2 mg/L. This undesirable water quality subsequent to lake overturn triggers fish kills in Taal Lake.

4.1.3 Contamination from Toxic and Hazardous Substances of Aquatic Products

A survey of specifically selected antibiotic and pesticide residues in Philippine aquaculture and fishery prod-ucts was conducted recently by Coloso, Catacutan, and Arnaiz (2015) from samples of tilapia, milkfish, sea bass, snapper, grouper, rabbitfish, carp, catfish, silver perch, tiger shrimp, white shrimp, and freshwater prawn. Some 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

Win

d di

rect

ion

(deg

rees

)

Win

d ve

loci

ty (m

ps)

200

0

120

80100

604020

140160180

3.0

0

1.0

0.5

1.5

2.0

2.5

150 5 0 20 25 30 35 40 45 50 55 60

Wind direction Wind velocityFish kill due to pollution Fish kill due to lake overturnFish 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.

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Physical Impacts 37

OTC and oxalinic acid (OXA) as well as for organo-chlorine pesticides (OCP) for both high-value and low-value fish commodities. OXA and OTC were the most common antibiotic residues found and methoxychlor for OCP from Luzon, Visayas and Mindanao. OXA in Penaeus vannamei sample from Mindanao was found to exceed the maximum residue limit (MRL, based on Japan Food Chemical Research) and Permissible Expo-sure Limit (PEL, based on the Occupational Safety and Health Administration based in the United States). In one sample of freshwater prawn Macrobrachium species from Luzon, the level of Endosulfan I (0.0144 ppm) was considered harmful based on PEL (0.00642) and

MRL (0.005). Endrin ketone (0.02582 ppm) was also detected from the same prawn sample, although no PEL and MRL is as yet established (Table 15).

4.2 Impact of Diversification of Culture Commodities through Species Introductions

4.2.1 Effects on BiodiversityIntroduction and/or translocation of aquatic organisms primarily affect biodiversity in localities of introduc-tion. There are examples of invasive species altering the

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

Aquatic ProductNo. of

SamplesNo. of (+) Samples

Residual Analysis Report

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 (kanduli)

1 1 — — 0.00353 (Endrin)0.00255 (4-4’DDT)0.03255 (Methoxychlor)

Freshwater prawn (Macrobra-chium species)

1 1 No sample No sample 0.014440 (Endosulfan (Endosulfan)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

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector38

evolutionary pathway of native species by competitive exclusion, niche displacement, hybridization, introgres-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-tion (Joshi 2006). Introduced invasive species are con-sidered the second leading cause of species extinction and endangerment worldwide, the first being habitat destruction (Williams et al. 1989).

In the case of the golden apple snail Pomacea canaliculata whose introduction was as alternative pro-tein source for Filipinos, its introduction to the country has been blamed for the loss of the edible native snail Pila conica (Pagulayan 1997). The loss of most of the endemic cyprinids in Lake Lanao, the third-largest lake in the country, has been attributed to the introduction of the white goby Glossogobius giurus and the eleotrid Hypseleotris agilis (Juliano, Guerrero, and Ronquillo 1989). The introduction of the Thai catfish Clarias ba-tracus has resulted in the loss of the native catfish Clar-ias macrocephalus in many inland water bodies in the country. SEAFDEC/AQD implemented research and development activities to breed Clarias macrocephalus (Tan-Fermin et al. 2008) in the hope of restocking de-pleted inland water bodies, but difficulties in obtaining wild brood stock for induced spawning activities ham-pered efforts.

Introduced species have far-reaching adverse en-vironmental impacts. Cuvin-Aralar (2014) compared the fish biodiversity in an aquaculture and non-aqua-culture site in Laguna de Bay, the largest inland water body in the Philippines widely used for fish production. Results showed that fish biodiversity was significantly lower in the aquaculture site compared to the non-aqua-culture site. There was a significantly higher predom-inance of introduced species for culture (Nile tilapia, bighead carp, Tra catfish) compared to native species in the aquaculture site. The non-aquaculture site had significantly higher relative dominance of native spe-cies. Indices of biodiversity such as Shannon-Wiener Index, Simpson Index, and Evenness all indicate signifi-cantly higher fish biodiversity in non-aquaculture sites

(Cuvin-Aralar 2014). Figure 38 illustrates the direct and indirect impact of introduced species on biodiversity.

4.2.2 Other Impacts of Introduced SpeciesAside from adverse impacts on biodiversity, introduced aquatic species have also adversely affected other envi-ronmental factors. Escapees from the ornamental fish trade like the South American sucker mouth catfish, locally known as janitor fish Pterygoplichthys pardalis and Pterygoplichthys disjunctivus, have become invasive in many areas in Luzon, including Marikina River and Laguna de Bay (Chavez et al. 2006; Jumawan et al. 2011) and Agusan Marsh in Mindanao (Hubilla, Kis, and Pri-mavera 2008). The fish with its hard armor-like cover-ing damaged the banks of the Marikina River due to its burrowing habit and damaged aquaculture fish cages in Laguna de Bay. Considerable expense has been incurred from a ‘bounty system’ type of approach to eradicate janitor fish wherein fishermen were paid to catch the janitor fish at PHP 5.00/kg, after which the caught fish are destroyed (Joshi 2006). The two introduced fresh-water cichlid species, the black chin tilapia Sarotherodon melanotheron and the Mayan cichlid Cichlasoma uroph-thalmus, have been caught in Manila Bay (Ordonez et al. 2015). It is to be noted that the black chin tilapia has been reported as an introduced species in Laguna de Bay (Cuvin-Aralar 2014). It is possible that Sarotherodon melanotheron found its way to Manila Bay via the Pasig River from Laguna de Bay, in addition to escapees from fishponds in adjacent areas. Both cichlids were reported to have had competitive interactions with other fish spe-cies in Manila Bay (Ordonez et al. 2015).

In the case of the golden apple snail (Pomacea canaliculata), its introduction caused considerable havoc not only to inland water bodies but many rice fields as well (Joshi 2006). To eradicate these snails, molluscicides valued at US$23 million were import-ed between 1998 and 2005, but had limited success; the snails still remain a problem. The snails are also vectors of a rat lungworm that also affects humans (Joshi 2006).

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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

Reduction in native species;endangering species; at times

leading to extinction

Habitat destructionCompetition withnative species

Hybridization

Reduction in nativepopulation numbers;

inbreeding depression;reduced fitness

New and unusualselection on native

species

Hybrid vigor;increased

fitness

Outbreedingdepression;

reducedfitness

Genetic changesin native species

Displacement of native species;Findangering; extinction; loss of

taxonomically distinct population/speciesIndirect impactsDirect impacts

Introgression

Disease Ecological impacts Genetic changes

Source: de Silva et al. 2009.

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SOCIOECONOMIC AND HEALTH IMPACTS OF FISHERIES AND AQUACULTURE PRACTICES

5.1 Human Health Impacts

5.1.1 Use of Waste Products for AquacultureThe 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 produc-tion 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

5

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector42

the bioaccumulation of pathogenic viruses and bacte-ria in the muscle tissue of shellfish exposed to animal and human feces (Schwab et al. 1998). The potential to infect humans through direct dermal contact (of aquaculture wastewater) or ingestion of an improperly cooked contaminated fish product is a possibility (Sap-kota et al. 2008).

5.1.2 Application of chemicals and bioactive compounds to boost aquaculture production poses concern on their release to the aquatic environment

Aside from direct contamination of fish products as shown in the previous section, the use of antibiotics in aquaculture feed also poses a concern in terms of the release of these compounds through leaching and excretion of the aquatic animals, which in turn will contaminate the environment (water and sediment). This has resulted in the emergence of antibiotic-resis-tant microbes in aquaculture environments, increase in antibiotic resistance in fish pathogens, transfer of resistance to microbes of land animals and to human pathogens, and a change in the bacterial population in the sediments and water (Cabello 2006). The presence of these antibiotic residues exerts undue influence on the microflora in the water and sediment and modifies the diversity of the population of microorganisms not 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-ple, those which may contain resistant genes (Marshall and Levy 2011). These resistant bacteria will be able to spread their genes into water and sediment indig-enous microbes, which also contain resistance genes. As applied in aquaculture, the low-dose, extended use of antibiotics among food animals promotes the prop-agation of resistant strains through selective pressures on other nonresistant strains which may compete with the resistant ones. A study conducted by Tendencia and de la Peña (2001) compared the microbial population’s

(mostly Vibrios) resistance to antibiotics in shrimp ponds currently using antibiotics to those ponds that used antibiotics before and ponds which did not use antibiotics. Their results showed highest percentage of microbials with multiple antibiotic resistance from ponds which were using antibiotics (oxolinic acid) at 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 antibiotics. Antibiotic resistance was shown for OTC, furazolidone, oxolinic acid, and chloramphenicol. Fur-ther, the study also showed no correlation between resistance and the actual type of antibiotic used, with highest incidence of resistance to oxolinic acid and furazolidone.

Since many antibiotics used in aquaculture are also used on humans, concerns on antibiotic resistance and other subsequent effects on human health have been raised (Marshall and Levy 2011). However, con-crete evidence of any possible harm to humans by the use of veterinary drugs, including antibiotics, as used in aquaculture is difficult to document as the drugs are often similar to those used on humans (Howgate 1998). Precaution should nevertheless be put in place that will require very low levels of residues of these therapeutants in fish and fishery products for human consumption (Bernoth 1991). Figure 40 illustrates the sources and pathways of how antibiotics are released to the environment.

5.2 Socioeconomic Impacts

5.2.1 Beneficial Impacts of Fisheries and Aquaculture

The positive impact of fisheries and aquaculture on the livelihood of fishers and fish farmers has been amply demonstrated. In the case of 6 of the top-ranked 22 species in freshwater aquaculture in the world, more than 20 percent of the production occurs in areas out-side of their natural range of distribution. From 2000 to 2004, 16 percent of global finfish production from

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Socioeconomic and Health Impacts of Fisheries and Aquaculture Practices 43

aquaculture was alien freshwater species (de Silva et al. 2006). In the Philippines, two of the top three cultured fish species were either introduced (in the case of Nile tilapia) or translocated (the case of milkfish). Nile tila-pia introduction to the Philippine aquaculture scene 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-cies and constituted on average 6.43 percent of total milkfish production in the Philippines and 0.41 per-cent of total fish produced in the country from 1996 to 2006 (Israel, Boni-Cortez, and Patambang 2008). Nile tilapia, on the other hand, is an exotic species intro-duced for culture in the lake. This species constituted on average 9.01 percent of total tilapias produced in the country and 0.31 percent of total fish production (Israel, Boni-Cortez, and Patambang 2008). With regard to income generation, aquaculture enterprises in Laguna de Bay averaged almost PHP 1,373 million from 1996 to 2006, of which milkfish contributed more than PHP 657 million and tilapia PHP 496 mil-lion (Israel, Boni-Cortez, and Patambang 2008). Table 16 shows the value of production of milkfish and tilapia in Laguna de Bay from 1996 to 2006, representing the gross income of producers of these commodities. Israel, Boni-Cortez, and Patambang (2008) estimates 5,152

people directly employed in aquaculture in Laguna de Bay area, not considering other members of the popu-lation who are in one way or another dependent on lake aquaculture through backward linkages in the input markets and forward linkages in marketing.

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

Human and Veterinary medicine

Waste water

Irrigation water

Environment (soils, rivers, lakes)

Waste watertreatment

Animal manure

Industrial production Aquaculture Stock breeding Crop production

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.

Table 16: Production value (in PHP, thousands) of milkfish and tilapia as well as total cultured fish production in Laguna de Bay

Year Milkfish Tilapia Total Production

1996 618,745 305,683 957,736

1997 696,389 342,968 1,063,847

1998 676,000 340,825 1,109,181

1999 814,269 377,916 1,404,635

2000 732,608 573,393 1,566,844

2001 123,607 416,582 929,555

2002 305,752 437,538 975,536

2003 674,235 535,983 1,390,427

2004 953,007 654,359 1,930,427

2005 905,638 737,472 1,977,269

2006 729,764 739,472 1,798,761

Average 657,274 496,530 1,373,081

Source: BAS files as cited by Israel, Boni-Cortez, and Patambang 2008.

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SOLUTIONS TO MITIGATE IMPACTS 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 inno-vations 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 PrebioticsProbiotics are live microorganisms which when administered in adequate amounts confer a health benefit to the fish (FAO/WHO 2001), while prebiotics

6

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are nondigestible oligosaccharides used to control or manipulate microbial composition and/or activ-ity, thereby assisting in maintaining a beneficial gut microflora (Zimmerman, Bauer, and Mosenthin 2001). Both probiotics and prebiotics are now com-monly used in aquaculture as an alternative to the use of chemical products to promote good soil and water quality in ponds as well as limit or minimize the use of antibiotics.

Probiotics may be incorporated into the feed or applied directly to the water. If the product is to be incorporated as a feed ingredient, it has to have the following characteristics: (a) resistant to low pH and bile acids; (b) have no pathogenicity; (c) viable and stable in storage and in the field; (d) survive and potentially colonize the gut; (e) be cultivable on a large scale; (f ) able to adhere to the epithelial lining of the gut; (g) affect cultured fish beneficially; and

(h) maintain balance among intestinal microflora (De et al. 2009). Dietary probiotics primarily work through the competitive exclusion principle, either by competing for nutrients against pathogenic organisms or competitive binding to receptors on the gut of the cultured fish. Some probiotics may produce a specific antibacterial substance themselves, while others may reduce the production of toxic amines and decrease the ammonia level in the gastrointestinal tract (De et al. 2009). Some examples of probiotics added to feeds are the addition of live Bacillus subtilis to Pacific white shrimp Penaeus vannamei diets (Wang 2007) and Lactobacillus species to giant freshwater prawn Mac-robrachium rosenbergii diets (Venkat, Sahu, and Jain 2004), where both species showed improved growth performance.

Aside from dietary inclusion, probiotics may also be applied to the pond water in shrimp farms. Ta-ble 17 lists some commercial probiotics used in shrimp ponds in the Philippines.

Prebiotics are also incorporated into the feeds 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-tured fish) (Manning and Gibson 2004). The prebi-otic should be resistant to gastric acids, breakdown by digestive enzymes in the gut, and gastrointestinal absorption and fermentation by intestinal microflora (Ringo et al. 2010). Among the important character-istics of prebiotics are the following: (a) are easy to in-corporate in the feed; (b) regulate gut viscosity; (c) are noncarcinogenic; (d) are derived from dietary poly-saccharides; (e) are of low calorific value; (f ) reduce harmful microbial loads; (g) are effective at low con-centrations; (h) exert anti-adhesive properties against harmful gut microbes; (i) stimulate beneficial gut mi-crobes; and (j) produce no residual effects (Ganguly, Paul, and Mukhopadhayay 2010). Prebiotics work by providing selective stimulation of the growth and/or activity of intestinal bacteria that contribute to the health and well-being of the fish; shifting gut microbi-al population to one dominated by beneficial bacteria;

Table 17: Probiotics used in shrimp brackish-water farms in the Philippines

Probiotic Amount Used Remarks

BZT Waste Digester

1–2 kg/ha Pond preparation

150–800 g/ha 1–150 DOC (days of culture)

BZT Aquaculture

300–500 g/ha 5–7 days prior to stocking

50–200 g/ha 1–150 DOC

Super PS 30–50 L/ha Pond preparation

5–8 L/ha Rearing phase, every 5–10 days

Super Biotic 6 kg/ha Rearing phase 1–90 DOC weekly

5–10 g/kg feed 3–30 DOC, 2–3 time/day

10 g/kg feed 31–60 DOC, 2–4 times/day

Zymetin 5–10 g/kg feed Rearing phase, 3–30 DOC

10 g/kg feed 31–60 DOC

Ecomarine 25 tablets/ha Pond preparation

NS-SPO Series

2–3 kg/ha/culture 7-day interval

BYM 5–15 kg/ha Rearing phase

Biobase 10 kg/ha Pond preparation

17 kg/ha/week Rearing phase

Source: Cruz-Lacierda et al. 2008.

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Solutions to Mitigate Impacts of Aquaculture Pollutants 47

increasing disease resistance; and improving nutrient digestibility. Among the prebiotics that have proven beneficial to fish are inulin, fructooligosaccharides (FOS), and mannanoligosaccharides (MOS) which have been used in carp, shrimps, and tilapia (Ringo et al. 2010).

Another type of eubiotic added to feeds is or-ganic acid (OA). These may be in the form of short-chain fatty acids (C1-C7), volatile fatty acids, and weak carboxylic acids. These acids are widely distrib-uted in nature as normal constituents of plants or an-imal tissues. Unlike mineral acids, OAs are relatively weak; they do not completely dissociate in water, but low molecular weight OAs are miscible in water. They may be in the form of sodium, potassium, or calci-um salts. OAs added to feeds should be protected to avoid dissociation in the intestine, particularly in the segments with relatively high pH, and reach far into the gastrointestinal tract where the bulk of the bacte-rial population is located. OAs act as an antimicrobial growth promoter without the associated public health concern. OAs work by (a) improving feed palatabil-ity and reducing diet pH; (b) acting as antimicrobi-al preservative of feeds; (c) reducing gastric pH and enhancing pepsin activity; (d) stimulating beneficial intestinal flora and improving health; (e) increasing digestibility of nutrients and thus improving growth and feed conversion; and (f ) reducing the risk of spread of microbial infection by lowering microbial load in feces (Elala and Ragaa 2014; Ng et al. 2009). Some examples of OA used in aquaculture and live-stock feeds are formic acid, acetic acid, propionic acid, oxalic acid, lactic acid, and butyric acid. OAs in the form of potassium diformate (KDF) and sodium diformate (NDF) have been used in experimental di-ets in Nile tilapia and were shown to improve growth, FCR, and disease resistance and lower fecal microbial load (Cuvin-Aralar et al, 2011; Ng et al. 2009; Ela-la and Ragaa 2014). Formic acid showed the highest inhibitory effect, compared to propionic and butyric acid, on Vibrio harveyi in shrimp culture (Mine and Boopathy 2011).

6.1.2 Nutraceuticals, ImmunostimulantsNutraceuticals (nutrition + pharmaceutical) are naturally occurring substances which may be found in some level in the natural diet of the cultured organisms. The term was coined in 1989 in response to the growing interest in food and food supplements in human health (And-lauer and Fürst 2002). When functional feeds also aid in the prevention/treatment of disease and disorders, it is called a nutraceutical (Alexander et al. 2011). Nutraceu-ticals are administered orally over an extended period. It attempts to stimulate the immune system to compen-sate for production-related immunosuppression. It is an alternative to antibiotics and other chemotherapeu-tants for disease management. Nutraceuticals have been known to increase overall vigor as well as increase levels of antioxidants (Trushenski, Kasper, and Kohler 2006).

Immunostimulants is another group of naturally occurring compound that modulates the immune sys-tem by increasing host resistance against diseases caused by pathogens. As a feed additive, immunostimulants enhance transitory disease resistance in fish (Ringo et al. 2012). Some immunostimulants tested for aquacul-ture are beta glucans, alginate, and ErgosanTM extracts from algae and dietary nucleotides which have been tested in catfish, tilapia, eel, carp, snakehead, and sea bass (Ringo et al. 2012).

6.2 Legislations and Regulations on the Use of Chemicals and Fisheries and Aquaculture

6.2.1 Setting Up Standards The Philippine National Standards (PNS) for the code of conduct for Good Aquaculture Practice (GAqP) was published in 2014 (PNS/BAFPS 2014). This is part of the Philippine commitment to the Association of Southeast Asian Nations (ASEAN) Roadmap for ASEAN Community 2009–2015, seeking to enhance intra- and extra-ASEAN trade and long-term com-petitiveness of ASEAN food, agriculture, and forestry products and commodities. Before promulgation of the

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GAqP, it underwent a series of reviews and consultations with stakeholders in various parts of the country and the Committee on Fisheries and Aquaculture (CFA) of the Philippine Council for Agriculture and Fisher-ies (PCAF). The Code of GAqP applies to aquaculture farms and projects covering hatchery, nursery, fish cage/pen/pond, seaweed, and mollusk farms regardless of ownership and “covers practices that aim to prevent or minimize the risk associated with aquaculture produc-tion (mariculture, coastal aquaculture/ brackish-water culture, and freshwater culture). This code covers the following aspects of aquaculture production namely: (a) food safety, (b) animal health and welfare, (c) envi-ronmental integrity, and (d) socioeconomic” (PNS/BAFPS 2014). Minimum compliance requirements covering location, hygiene/sanitation, waste disposal/removal, culture environment preparation including application/dispensing of chemical inputs and veteri-nary drug, feed inputs and feed quality, water manage-ment, disease control and management, animal welfare, 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.

PNS for Aquaculture Feeds have also been final-ized and published (PNS/BAFPS 2010) and covers “the preparation and formulation of nutritionally adequate aquaculture feeds such as pellet, mash, and crumble feed

forms used in culturing any aquatic organisms such as, but not limited to, crustaceans, fish, and mollusks…. Custom-mixed feeds and feed products for aquaculture use are also covered.” Under this code, nutrient standards for feeds for various commodities and for different life stages have been put in place. Pellet quality and stabili-ty are also included in the standards. Another important part of PNS for Aquaculture Feeds is the list of banned veterinary drugs in aquaculture feed (Table 18) adopted from the Philippine Veterinary Drug Directory. It is in-teresting to note that despite a ban on the use of antibi-otics like chloramphenicol as early as 1990, the drug was still in use when the survey was conducted by Cruz-Lac-ierda et al. in 1995–1996 (refer back to Table 10).

PNS for selected capture fishery and aquaculture products have also been established, but mainly adopt-ed from international standards following those set by the FAO/WHO Codex Alimentarius Commission. Ta-ble 19 lists some of the PNS published for various fish and fishery products.

6.2.2 Regular Monitoring of Fisheries and Aquaculture Operations’ Use of Chemicals

The code for GAqP covers monitoring of aquaculture operations to ensure compliance to the minimum

Table 18: Banned veterinary drugs in aquaculture feeds

Drug Administrative Order Subject Date

Clenbuterol, Salbutamol, Terbutaline, Pirbuterol

No. 14, Series of 2003 (Department of Agriculture)

Ban on the use in food animals of beta-agonist drugs used in humans as bronchodilators and tocolytic agents

May 12, 2003

Furaltadone, Furazolidone, Nitrofurazone

No. 2, Series of 2000 (Department of Agriculture and Department of Health)

Declaring a ban/phase-out of the use of nitrofurans in food-producing animals

August 17, 2000

Carbadox, Olaquindox No. 60, Series of 2000 (Department of Agriculture) No. 4-A, Series of 2000 (Department of Health)

Ban and withdrawal of olaquindox and carbadox from the market

January 11, 2000

Chloramphenicol No. 60, Series of 1990 (Department of Agriculture) No. 91, Series of 1990 (Department of Health)

Declaring a ban on the use of chloramphenicol in food-producing animals

April 30, 1990

Source: PNS/BAFPS 2010.

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requirements set by the code. The aquaculture opera-tor should record the last two croppings specifying the group of fish treated with veterinary drugs, the total quantity of the drugs used, the start and end date of treatment, completion of withdrawal period, and the earliest date the fish is safe to be consumed. The code further states that the withdrawal period be verified by conducting residue analysis on samples of treated fish. The MRL (maximum residue limit) for the particular drug should fall within the acceptable level based on the standards set by Codex or trading partners (PNS/BAFPS 2014).

Although the code for GAqP has been in exis-tence for a number of years, compliance is not man-datory. Fish farms who need to be certified to enable produce from these farms to be exported are the only ones who need to comply with GAqP. For most of the fish farmers selling their produce in local markets, there is no need to be certified and thus no push to comply with GAqP. Limitations on the part of the Government also exist, particularly in funds to enable the designat-ed certifying agency to conduct the necessary inspec-tions, monitoring, and analysis for farms that want to be certified.

6.2.3 Development and Adoption of National and Regional Guidelines on the Use of Chemicals in Aquaculture and Designation of Competent National Government Authority for Regulation and Monitoring

The ASEAN recently published the ‘Guidelines for the Use of Chemicals in Aquaculture and Measures to Eliminate the Use of Harmful Chemicals’ (ASEAN Secretariat 2013). The guidelines were developed to help national regulators and stakeholders manage the various chemicals used in aquaculture in ASEAN mem-ber countries. The guidelines aim to provide the Com-petent Authority (CA) of each ASEAN member state in setting standards and regulating the use of chemicals and aquaculture and implementing measures to elimi-nate the use of harmful chemicals. The member states are encouraged to assess and review gaps within each individual country regarding chemicals used in aqua-culture in the region listed in the guidelines. Among the classes of aquaculture chemicals listed in the guidelines which are commonly used in ASEAN member states are (a) antibiotics/antimicrobials both for food fish and ornamentals; (b) disinfectants; (c) chemotherapeutants

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.

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for food fish and ornamentals; (d) piscicides for use in pond preparation and early culture only; (e) hormones both for food fish and ornamentals; (f ) anesthetics; (g) culture system preparation; and (h) banned chem-icals. There are differences in the list of allowed and prohibited chemicals in each of the ASEAN member

countries. Table 20 lists the current regulatory status of various aquaculture chemicals for food fish in the Philippines.

The ASEAN guidelines came about because the use of drugs and chemicals in aquaculture opera-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)

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controlled by their respective CA. Under these ASE-AN guidelines, the BFAR is the designated CA for the regulation of chemicals used in aquaculture while the Food and Drug Administration of the Department of Health (DOH) is the CA for veterinary drugs and the Fertilizer and Pesticide Authority (FPA) is the CA for pesticides (Coloso, Catacutan, and Arnaiz 2015). The assignment as CAs of these agencies takes off from the existing regulatory structure in the Philippines. As the CA, these institutions shall be responsible for the following: (a) technical, diagnostic capacity and capa-bility; (b) coordination with other relevant agencies; (c) approval and registration of aquaculture premises;

(d) approval and/or registration of third-party service provider (laboratory, quarantine facilities); (e) approv-al and/or registration of manufacturers and traders of chemicals and drugs for use in aquaculture; (f ) estab-lishment and regular update of a national list of chem-icals for aquaculture purposes; (g) creating awareness among aquaculturists through extension and awareness programs; (h) carrying out monitoring, inspection, and surveillance activities; (i) regulating the import, manu-facture, and trade of chemicals and products; (j) evalu-ating and verifying the efficacy and safety of chemicals intended for use in aquaculture systems; and (k) carry-ing out enforcement activities for non-compliance to

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

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.

(continued)

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national practice and legislations. As agreed upon in the ASEAN guidelines, these local CAs will be responsible for notifying other ASEAN CAs and other relevant in-ternational organizations on current laws and regula-tions regarding chemicals in aquaculture. This is in view of increasing trade among ASEAN member countries.

6.3 Regulations on the introduction of nonnative species for culture and protecting local species

According to information on their website, the BFAR issued Fisheries Administrative Order 189 series of 1993 prohibiting the importation of live shrimp and prawn of all stages. However, this ban was lifted to favor the culture of the Pacific white shrimp Penaeus vanna-mei through Fisheries Administrative Order 225, 225-1 series of 2007, and Fisheries Administrative Order 225-2, 225-3 series of 2008. This was to address the demand for the entry of this shrimp into the country to save the ailing tiger shrimp (Penaeus monodon) that has been devastated by various diseases. There are no other Fisheries Administrative Orders prohibiting the introduction of other species for aquaculture in either the food or ornamental fish industry. However, there are numerous Fisheries Administrative Orders issued through the years mainly prohibiting or regulating the export of various fisheries commodities as well as estab-lishing fish sanctuaries in various parts of the country.

6.4 Technologies to Reduce Nutrients from Aquaculture

6.4.1 Integrated Multitrophic Aquaculture System and Integrated Agriculture-Aquaculture

Integrated Multitrophic Aquaculture (IMTA) involves cultivating fed species with extractive species that use wastes from aquaculture for their growth, with the advantage of all species in the system having economic

value. This type of aquaculture has received much attention in the past decade as a method of producing aquaculture products through the co-culture of compat-ible organisms. The principle is that waste product of one species (usually finfish as fed species) is utilized by another species, usually lower trophic levels such as sea-weeds, mollusks, and other benthic invertebrates (Ren et al. 2012). IMTA produces fish biomass and at the same time minimizes waste product from aquaculture opera-tions. IMTA can be applied to open water or land-based systems (aquaponics), marine or freshwater systems, as well as temperate or tropical systems. It is essentially not a new concept, since a form of IMTA was practiced in China in 2200 BC (NACA 1989). The use of extractive species is a cost-effective way to mitigate the amount of nitrogen, phosphorus, carbon, and organic wastes released from aquaculture. Important considerations for IMTA are (a) compatible combination of species; (b) appropriate habitat; (c) appropriate available culture technologies for the commodity; (d) complementary ecosystem functions of the cultured organisms; (e) cul-tured organisms being able to grow to a significant bio-mass for efficient mitigation of wastes; and (f ) commer-cial value of the cultured commodities (Chopin et al. 2010). In the Philippines, experimental trials on IMTA with species such as milkfish as the ‘fed’ commodity and angel wing clam (Anodontia philippiana) and sand fish (Holothuria scabra) as the extractive species have been conducted (Lebata-Ramos, pers. comm).

6.4.2 AquasilvicultureAquasilviculture is the integration of aquaculture with mangroves. It is an environment-friendly system which promotes harmonious coexistence between fisheries production and mangrove systems in a semi-enclosed environment. This culture method promotes harmoni-ous use of mangrove areas for aquaculture production, without destroying the mangrove forests. The Philip-pine government through the BFAR and the Commis-sion on Higher Education (CHED) in collaboration with academic institutions and local governments are

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implementing the ‘Philippine National Aquasilvicul-ture Program’. A memorandum of agreement has been signed between the two institutions as principals. The program involves reforestation of denuded mangrove areas and use of these reforested areas and existing man-groves for the culture of fish and other fishery products without cutting down a single tree. Abandoned areas covered by fishpond lease agreements (FLAs) as deter-mined jointly by the Department of Environment and Natural Resources (DENR), Department of Agricul-ture (DA), and the LGUs shall also be restored to their original mangrove state (Flores, et al. 2014).

6.4.3 Integrated Agri-Aquaculture SystemIntegrated Agri-Aquaculture (IAA) combines the pro-duction of crops, livestock, and aquatic animals in a limited system and is conducive for small farmholding by maximizing production in a small area and using the different waste components from each product.

One type of such integrated production system is aquaponics. It is the integration of recirculating fish production systems with hydroponic plant production to use the fertilizers efficiently. The integration of these two systems leads to the removal of nutrients (primarily nitrates and phosphates) from the system, omitting the need for water changes and thus conserving water. How-ever, water is needed to fill the initial system. Aquapon-ic systems recirculate water to use nutrients efficiently, thus producing food in a sustainable manner with little environmental impact. Removal of nutrients from fish effluent through plant nutrient uptake is an efficient and productive method of filtration (Licamele 2009). An aquaponics system is a symbiotic joining of aqua-culture and hydroponics. The nutrient wastes produced by fish are circulated to the plant growing component and used by plants as fertilizers. Instead of building up in the aquaculture system, nutrients generated from fish waste serve as liquid fertilizer to hydroponically grown plants. The hydroponic component serves as a biofil-ter so that the water can be circulated back to the fish culture component of the system (White et al. 2008).

Therefore, the aquaponics system is an efficient way to upcycle nutrients from aquaculture to crop production, thus avoiding eutrophication problems associated with aquaculture wastes.

Rice-fish-vegetable integrated production is widely practiced in many Asian countries like China, Vietnam, India, and Bangladesh. However, there is limited adoption in the Philippines. This type of pro-duction system is ideally suited for small farmholdings in rural communities. This type of farming provides several advantages: (a) maximize use of land and water resources over a limited area; (b) integrated pest man-agement system by reducing the use of pesticides since fish feed on larvae and juveniles of pests in rice fields; (c) minimize the use of fertilizer in rice since fish waste is a source of nutrients for the growing rice and other crops; and (d) improve resource utilization by diversi-fying crops produced in a limited area. The BFAR has been promoting the integrated culture of rice and fresh-water prawn (Macrobrachium rosenbergii) through pilot demonstration sites in the province of Laguna using just 1,000 m2 of rice fields, with 10 percent devoted to prawn and the rest to rice. Figure 39 illustrates the layout of the farm. Cost and return analysis for this set-up proved to be significantly better for the integrated rice-prawn system compared to monoculture of rice (Casbadillo, unpublished). Figure 41 shows the cost and return for this simple setup.

IAA is not as widely popular in the Philippines as in other Asian countries. For instance, rice-fish cul-ture poses problems in synchronizing harvest of the two main crops. Many rice farmers feel that digging deeper ditches in specific areas in the rice field limits the area devoted to rice. Since the primary crop is rice and the side crop is fish, traditional rice farmers have to learn the technology of fish culture in tandem with their rice production effort. Although the BFAR promotes this, the agencies responsible for rice production do not. It is mainly the ‘fish’ people who are promoting integration with crops. Another hindrance to the adoption of IAA is the limitation in the use of traditional agricultural chemicals such as pesticides since these are toxic to fish.

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An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector54

Many farmers find it difficult to veer away from pesti-cides and fertilizer use in their rice field, despite the fact that one of the significant features of IAA is integrated pest management: using fish to control rice pests and weeds. Moreover, the use of fertilizers is also minimized since fish excretory products are sources of nutrients for the growing rice.

6.4.4 Feeding Management System which Involves Improvement of Feeding Practices for Cultured Aquatic Animals

Proper feed management results in efficient use of feed with reduced feed wastage, resulting in high feed efficiency (low FCR). In the Philippines, it has been shown that skip feeding or alternate day feeding strat-egy for Nile tilapia is effective and efficient in both

pond (Bolivar, Jimenez, and Brown 2006) and lake-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 waste either through more complete feed consumption by fish and/or improved nutrient absorption. Skip feed-ing or alternate day feeding is both an economical and ecologically sound alternative to Nile tilapia culture in both ponds and lake-based culture systems.

Another feeding management strategy that has shown to be effective in reducing feed wastage and improving feed efficiency is the use of maintenance feeding (MF) and submaximum feeding (SF). Exper-imental studies using this type of feed management where the fish are given MF and subsequently SF gave 30 percent less feed wastage, as measured by fecal out-put, compared to control (given full daily feed ration). Mean FCR of fish given the MF/SF ration was only 0.8, which is significantly lower than 1.6 for fish given the full ration. Growth rates of fish also did not differ and full catch-up growth occurred in the MF/SF ra-tion. This study shows that feeding fish in cycles of MF

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

Irrig

atio

n

Irrigationcanal

PrawnareaDike Dike

0.5 m

1 m

Are

for P

raw

n

Are planted to rice

Planted to rice

Pipe with netcover

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

PhP

Rice Mono Rice + Prawn

14,000

0

4,000

2,000

6,000

8,000

10,000

12,000

Cost Net incomeGross income

Source: Casbadillo unpublished.

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Solutions to Mitigate Impacts of Aquaculture Pollutants 55

followed by SF may be an applicable feed management strategy to reduce feed costs and at the same time im-prove effluent quality of the aquaculture water without affecting growth (Ali et al. 2010). Studies on this type of feed management in local aquaculture commodities should also be conducted to determine if it can be ad-opted locally.

6.4.5 Biofloc TechnologyBiofloc Technology (BFT) is considered an environ-ment-friendly and efficient system to produce aquacul-ture products, since nutrients could continuously be recycled and reused. The sustainable approach of such a system is based on the growth of microorganism in the culture medium, benefited by the minimum or zero water exchange. These microorganisms (biofloc) have two major roles: (a) maintenance of water quality, by the uptake of nitrogen compounds generating ‘in situ’ microbial protein and (b) nutrition, increasing cul-ture feasibility by reducing FCR and decreasing feed costs (Emerenciano, Gaxiola, and Cuzon 2013). As a closed system, BFT has the advantage of minimizing the release of effluents into water bodies as opposed to traditional culture systems where water drained from ponds and tanks in the course of the grow out results in eutrophication of receiving water bodies. In BFT, ‘waste’-nitrogen from uneaten feed and cultured organ-isms is converted into proteinaceous feed available for those same organisms. Instead of ‘downcycling’, a phenomenon often found in an attempt to recycle, the

technique actually ‘upcycles’ by closing the nutrient loop. Hence, water exchange can be decreased with-out deterioration of water quality and, consequently, the total amount of nutrients discharged into adjacent water bodies may be decreased (Lezama-Cervantes & Paniagua-Michel 2010).

BFT gained prominence as a sustainable meth-od to control water quality, with the added value of producing proteinaceous feed in situ from a combina-tion of plankton and heterotrophic bacteria (Crab et al. 2012) that are able to provide nutrients to the cultured species. The technology has been used in the culture of various species like Nile tilapia (Avnimelech 2007) and marine shrimps (Ballester et al. 2010; Emeren-ciano, Ballester, and Cavalli 2011; Emerenciano et al. 2012; Brito et al. 2014), with positive results in terms of better growth and survival but with differences in the degree of the beneficial effect of BFT among the differ-ent species. In the BFT culture system, the floc makes the water turbid. Most fish farmers have the idea of clear water being much better than turbid water, thus BFT goes against what fish farmers expect (Avnimelech 2009). One of the issues against BFT is the require-ment for vigorous aeration in the system to enable the floc to remain in the water column, or else the system will not function. Oxygen requirement in BFT typi-cally ranges from 5 to 8 mg oxygen per liter per hour, another reason for the need for aeration (Hargreaves 2013). Electricity cost, needed to provide the aeration required, in the Philippines is quite prohibitive, thus limiting the adoption of BFT.

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REFERENCES

Adora, G. 2009. “Food Security through Sustainable Mariculture Park Projects in the Philippines.” East Asian Seas Congress Presentation. http://www.pem-sea.org/eascongress/ international-conference/presentation_t5-1_adora.pdf.

Alexander, C., M. S. Akhtar, P. Das, and S. C. Mandal. 2011. “Nutri-Biotechno-logical Interventions for Maximization of Growth in Carps of India.” World Aquaculture 42 (2): 6.

Ali, M., R. S. Hayward, P. G. Bajer, and G. W. Whitledge. 2010. “Maintenance/Sub-maximum Feeding Schedules for Reducing Solid Wastes and Improving Feed Conversion in Aquaculture.” Journal of World Aquaculture Society 41: 319–331

Almendras, J. M., C. Duenas, J. Nacario, N. M. Sherwood, and L. W. Crim. 1988. “Sustained Hormone Release. III. Use of Gonadotropin Releasing Hormone Analogues to Induce Multiple Spawnings in Sea Bass, Lates calcarifer.” Aqua-culture 74: 97–111.

Alongi, D. M. 2008. “Mangrove Forests: Resilience, Protection from Tsunamis, and Responses to Global Climate Change.” Estuarine, Coastal and Shelf Sci-ence 76: 1–13.

Andlauer, W., and P. Fürst. 2002. “Nutraceuticals: A Piece of History, Present Sta-tus, and Outlook.” Food Research International 35: 171–176

Angienda, P. O., H. J. Lee, K. R. Elmer, R. Abila, E. N. Waindi, and A. Meyer. 2011. “Genetic Structure and Gene Flow in an Endangered Native Tila-pia Fish (Oreochromis esculentus) compared to invasive Nile Tilapia (Oreo-chromis niloticus) in Yala Swamp, East Africa.” Conservation Genetics 12 (1): 243–255.

ASEAN (Association of Southeast Asian Nations) Secretariat. 2013. “Guidelines for the Use of Chemicals in Aquaculture and Measures to Eliminate the Use of Harmful Chemicals.” Jakarta, Indonesia.

Avnimelech, Y. 2007. “Feeding with Microbial Flocs by Tilapia in Minimal Dis-charge Bioflocs Technology Ponds.” Aquaculture 264: 140–147.

Page 70: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector58

_______. 2009. Biofloc Technology – A Practical Guide-book. Baton Rouge, Louisiana: The World Aqua-culture Society.

Bagarinao, T. U. 1999. Ecology and Farming of Milkfish. Iloilo, Philippines: SEAFDEC/AQD.

Ballester, E. L. C., P. C. Abreu, R. O. Cavalli, M. Emer-enciano, L. Abreu, W. Wasielesky. 2010. “Effect of Practical Diets with Different Protein Levels on the Performance of Farfantepenaeus paulensis Juveniles Nursed in a Zero Exchange Suspended Microbial Flocs Intensive System.” Aquaculture Nutrition 16:163–172.

Balistrieri, L. S., Tempel, R. N., Stillings, L. L., & Shevenell, L. A. (2006). Modeling spatial and temporal variations in temperature and salinity during stratification and overturn in Dexter Pit Lake, Tuscarora, Nevada, USA.Applied Geo-chemistry, 21(7), 1184-1203.

Bergquist, D. 2007. “Sustainability and Local People’s Participation in Coastal Aquaculture: Region-al Differences and Historical Experiences in Sri Lanka and the Philippines.” Environmental Management 40 (5): 787–802.

Bernoth, E. M. 1991. “Possible Hazards Due to Fish Drugs.” Bulletin of the European Association of Fish Pathologists 11: 17–21

Beveridge, M. C. M. 1984. “Cage and Pen Fish Farming. Carrying Capacity Models and Environmental Impact.” FAO Fisheries Technical Paper No. 255.

BFAR (Bureau of Fisheries and Aquatic Resources). “Mariculture Zones and Parks.” http://www.bfar.da.gov.ph/uegis.jsp?id=4.

BFAR. 2011. Press Release Taal Lake Fish kill. http://www.bfar.da.gov.ph/ newsarchives.jsp?id=226

_______. 1977–2014. Philippine Fisheries Profile. Que-zon City, Philippines: BFAR.

_______. 2015. “Ginintuang Masaganang Ani for Fish-eries Program 2002–2004.” Accessed November 15, 2015. http://bfar.da.gov.ph/program.

Bolivar, R. B., A. E. Eknath, H. L. Bolivar, and T. A. Abella. 1993. “Growth and Reproduction of Individually Tagged Nile Tilapia (Oreochromis

niloticus) of Different Strains.” Aquaculture 111: 159–169.

Bolivar, R. B., E. B. T. Jimenez, and C. L. Brown. 2006. “Alternate-Day Feeding Strategy for Nile Tilapia Grow Out in the Philippines: Marginal Cost-Revenue Analyses.” North American Jour-nal of Aquaculture 68 (2): 192–197.

Brito, L. O., L. A. V. Arana, R. B. Soares, W. Severi, R. H. Miranda, S. M. B. C. da Silva, M. R. M. Co-imbra, and A. O. Galvez. 2014. “Water Quality, Phytoplankton Composition and Growth of Li-topenaus vannamei (Boone) in an Integrated Bio-floc system with Gracilaria birdiae (Greville) and Gracillaria domingensis (Kutzing).” Aquaculture International 22: 1649–1664.

Cabello, F. C. 2006. “Heavy Use of Prophylactic An-tibiotics in Aquaculture: A Growing Problem for Human and Animal Health and for the Environment.” Environmental Microbiology 8: 1137–1144.

Cagauan, A. G. 2007. “Exotic Aquatic Species Intro-duction in the Philippines for Aquaculture–A Threat to Biodiversity or a Boon to the Econ-omy?” Environmental Science and Management 10: 48–62.

Caliro, S., Chiodini, G., Izzo, G., Minopoli, C., Si-gnorini, A., Avino, R., & Granieri, D. (2008). Geochemical and biochemical evidence of lake overturn and fish kill at Lake Averno, It-aly. Journal of volcanology and geothermal re-search, 178(2), 305-316.

Chakraborty, S. B., D. Mazumdar, U. Chatterji, and S. Banerjee. 2011. “Growth of Mixed-Sex and Monosex Nile Tilapia in Different Culture Sys-tems.” Turkish Journal Fisheries and Aquatic Sci-ences 11: 131–138.

Chavez, J. M., R. M. De La Paz, S. K. Manohar, R. C. Pa-gulayan, and J. R. Carandang. 2006. “New Phil-ippine Record of South American Sailfin Catfishes (Pisces: Loricariidae).” Zootaxa 1109: 57–68.

Chopin, T., M. Troell, G. Reid, D. Knowler, S. M. C. Robinson, A. Neori, A. H. Buschman, and S.

Page 71: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

REFERENCES 59

J. Pang. 2010. “Integrated Multi-Trophic Aqua-culture. Part II. Increasing IMTA Adoption.” Global Aquaculture Advocate November/Decem-ber: 17–19.

CODEX STAN 36-1981, Rev.1-1995. “Standard for Quick Frozen Finfish, Uneviscerated and Eviscer-ated.” Codex Alimentarius Commission. Rome, Italy: FAO/WHO. www.codexalimentarius.org.

CODEX STANh 95-1981, Rev.2-2004. “Codex Stan-dard for Quick Frozen Lobsters.” Codex Alimen-tarius Commission. Rome, Italy: FAO/WHO.

CODEX STAN 167-1989, Rev. 2-2005. “Standard for Salted Fish and Dried Salted Fish of the Gadidae Family of Fishes.” Codex Alimentarius Commis-sion. Rome, Italy: FAO/WHO.

CODEX/STAN 193-1995, Rev.4-2009, Amend.2-2010. “Codex General Standard for Contamination and Toxins in Foods.” Codex Alimentarius Commis-sion. Rome, Italy: FAO/WHO.

Coloso, R. M., M. R. Catacutan, and M. T. Arnaiz. 2015. Important Findings and Recommendations on Chemical Use in Aquaculture in Southeast Asia. Tigbauan, Iloilo, Philippines: SEAFDEC/AQD.

Coyle, S. D, R. M. Durborow, and J. H. Tidwell. 2004. “Anesthetics in Aquaculture.” Publication 3900, Stoneville, Mississippi: Southern Regional Aquaculture Center.

Crab, R., T. Defoirdt, P. Bossier, and W. Verstraete. 2012. “Biofloc Technology in Aquaculture: Ben-eficial Effects and Future Challenges.” Aquacul-ture 356: 351–356.

Cruz-Lacierda, E. R., L. D. de La Pena, and S. Luman-lan-Mayo. 2000. The Use of Chemicals in Aqua-culture in the Philippines. Use of Chemicals in Aquaculture in Asia. Iloilo: Southeast Asian Fish-eries Development Center, 155–184.

Cruz-Lacierda, E. R., V. L. Corre, J. A. Yamamoto, J. Koyama, and T. Matsuoka. 2008. “Current Status on the Use of Chemicals and Biological Products and Health Management Practices in Aquaculture Farms in the Philippines.” Mem. Fac. Fish. Kagoshima Univ. 57: 37–45.

Cuvin-Aralar, M. L. A. 2003. “Influence of Three Ni-trogen:Phosphorus Ratios on the Growth and Chemical Composition of Microalgae and its Utilization by Nile Tilapia, Oreochromis ni-loticus (L.).” Stuttgart, Beuren, Germany: Ver-lag Grauer. (Doctoral Dissertation, Universi-ty of Hohenheim, Stuttgart, Germany, ISBN 3-86186-428-2).

_______. 2014. “Fish Biodiversity and Incidence of Invasive Fish Species in an Aquaculture and Non-Aquaculture Site in Laguna de Bay, Phil-ippines.” In Lakes: The Mirrors of the Earth- Bal-ancing Ecosystem Integrity and Human Well-be-ing, edited by C. Chiara Biscarini, A. Pierleoni, and L. Naselli-Flores, 53–57. Proceedings of the 15th World Lake Conference, Perugia, Italy. Ita-ly: Science4press.

Cuvin-Aralar, M. L. A., P. Gibbs, A. Palma, A. An-dayog, and L. Noblefranca. 2012. “Skip Feed-ing as an Alternative Strategy in the Production of Nile Tilapia Oreochromis niloticus (Linn.) in Cages in Selected Lakes in the Philippines.” The Philippine Agricultural Scientist 95: 378–385.

Cuvin-Aralar, M. L. A., C. Luckstadt, K. Schroeder, and K. Kuhlmann. 2011. “Effect of Dietary Or-ganic Acid Salts, Potassium Diformate and So-dium Diformate on the Growth Performance of Male Nile Tilapia Oreochromis niloticus.” Bulle-tin of Fish Biology 13: 33–40.

Cuvin-Aralar, M. L. A., A. E. Santiago, A. C. Gonzal, C. B. Santiago, M. R. Romana-Eguia, S. F. Baldia, and Palisoc F Jr. 2001. “Incidence and Causes of Mass Fish Kill in a Shallow Tropical Eutrophic Lake (Laguna de Bay, Philippines).” 9th Interna-tional Conference on the Conservation and Man-agement of Lakes Proceedings, Session 5, Octo-ber 1-4, 2001, Shiga Prefecture, Japan, 233–236.

David, C. P. C., Y. Y. Maria, F. P. Siringan, J. M. Reoti-ta, P. B. Zamora, C. L. Villanoy, E.Z. Sombrito and R. V. Azanza. 2009. “Coastal Pollution Due to Increasing Nutrient Flux in Aquaculture Sites.” Environmental Geology 58 (2): 447–454.

Page 72: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector60

De, D., T. K. Ghoshal, A. Pramanik, and S. Ganguly. 2009. “Isolation, Identification and Methods of Use of Different Beneficial Microbes as Probi-otics in Aquafeed.” CIBA (ICAR) Spec. Publ. for Kakdwip Research Centre’s Training Manual on Brackishwater Aquaculture 41: 173–175.

De Silva, S. S., and M. R. Hasan. 2007. “Feeds and Fertilizers: The Key to Long-Term Sustainability of Asian Aquaculture.” In Study and Analysis of Feeds and Fertilizers for Sustainable Aquaculture Development, edited by M. R. Hasan, T. Hecht, S. S. De Silva and A. G. J. Tacon, 19–47. FAO Fisheries Technical Paper No. 497. Rome: FAO.

De Silva, S. S., T. T. T. Nguyen, G. M. Turchini, U. S. Amarasinghe, and N. W. Abery. 2009. “Alien Species in Aquaculture and Biodiversity: A Par-adox in Food Production.” Ambio 38: 24–28.

Delmendo, M. N. (1987). Milkfish culture in pens: an assessment of its contribution to overall fishery production of Laguna de Bay. ASEAN/UNDP/FAO Regional Small-Scale Coastal Fisheries De-velopment Project.

Delmendo, M. N., and R. H. Gedney. 1976. “Lagu-na De Bay Fish Pen Aquaculture Development – Philippines.” Proceedings of the Annual Meet-ing – World Mariculture Society 7: 257–265.

Dolorosa, R. G., A. Grant, and J. A. Gill. 2013. “Trans-location of Wild Trochus niloticus: Prospects for Enhancing Depleted Philippine Reefs.” Reviews in Fisheries Science 21: 403–413.

Edwards, P. (1993). Environmental issues in integrated agriculture-aquaculture and wastewater-fed fish culture systems. In Environment and aquacul-ture in developing countries. ICLARM Confer-ence Proceedings (Vol. 31, pp. 139–170).

Elala, N. M. A., and N. M. Ragaa. 2014. “Eubiotic Ef-fect of a Dietary Acidifier (Potassium Diformate) on the Health Status of cultured Oreochromis ni-loticus.” Journal of Advanced Research 6: 621–629.

Emerenciano, M., E. L. C. Ballester, and R. O. Ca-valli. 2011. “Effect of Biofloc Technology (BFT) on the Early Postlarval Stage of Pink Shrimp

Farfantepenaeus paulensis: Growth Performance, Floc Composition and Salinity Stress.” Aquacul-ture International 19: 891–901.

Emerenciano, M., E. L. C. Ballester, R. O. Cavalli, and W. Wasielewsky. 2012. “Biofloc Technology Ap-plication as a Food Source in a Limited Water Exchange Nursery System for Pink Shrimp Far-fantapeneus brasiliensis (Latreille, 1817).” Aqua-culture Research 43: 447–457.

Emerenciano, M., G. Gaxiola, and G. Cuzon. 2013. “Biofloc Technology (BFT): A Review for Aqua-culture Application and Animal food industry.” In Biomass Now-Cultivation and Utilization, In-Tech Publishing, Texas, USA. 301–328.

Escudero, P. E. 1994. “Lake Lanao Fisheries: Problems and Recommendations.” Philippine Biota 27: 8–18.

FAO (Food and Agriculture Organization of the Unit-ed Nations). 2008. State of World Fisheries and Aquaculture 2008. Rome: FAO.

_______. 2014. State of World Fisheries and Aquaculture 2014. Rome: FAO.

_______. 2015. “Global Capture Production.” Fish-ery Statistical Collection. http://www.fao.org/fishery/statistics/global-capture-production/en.

FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization). 2001. “Health and Nutritional Properties of Probiotics in Food including Powder Milk with Live Lactic Acid Bacteria.” FAO, WHO, United Nations. http://www.fao.org/3/a-a0512e.pdf

FAO/WHO CAC/RM42-1969. Sampling Plans for Pre-packaged Foods. Food and Agriculture Or-ganization/World Health Organization Codex Alimentarius Commission. Rome, Italy.

FAO/WHO CAC/RCP 1-69, Rev. 3-1997, Amd. 1999. “Recommended International Code of Practice: General Principles of Food Hygiene.” Codex Ali-mentarius Commission. Rome, Italy: FAO/WHO.

FAO/WHO CAC/RCP 26-1979. “Recommended International Code of Practice for Salted Fish.” Codex Alimentarius Commission. Rome, Italy: FAO/WHO.

Page 73: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

REFERENCES 61

FAO/WHO CAC/RCP 52-2003, Rev. 2-2005. “Code of Practice for Fish and Fishery Products.” Co-dex Alimentarius Commission. Rome Italy: FAO/WHO.

FAO/WHO CACf. CODEX STAN 192-1995. “Gen-eral Standard for Food Additives. Food Cate-gory 09.2.1: Frozen Fish, Fish Fillets, and Fish Products, Including Mollusks, Crustaceans, and Echinoderms.” Codex Alimentarius Commis-sion. Rome Italy: FAO/WHO.

FAO/WHO CODEX STAN 92 – 1981, Rev. 1 – 1995. “Codex Standard for Quick Frozen Shrimps or Prawns.” FAO/WHO.

FAO/WHO CL 2008/14-FFP. “Proposed Draft Stan-dard for Live Abalone and for Raw Fresh Chilled or Frozen Abalone for Direct Consumption or for Further Processing.” Codex Alimentarius Commission. Rome Italy: FAO/WHO.

Fermin, A. C. 1991. “LHRH-a and Domperidone-In-duced Oocyte Maturation and Ovulation in Bighead Carp, Aristichthys nobilis (Richardson).” Aquaculture 93: 87–94.

Flores, R. C., F. E. Tungol, A. S. Antonio, E. L. Me-dairos, and J. M. Salas. 2014. “BFAR-CHED Philippine National Aquasilviculture Program in Bataan: A Strategy Towards Fisheries Sustain-ability and Excellence.” Paper presented at the “Innovations and Good Practices in Higher Ed-ucation Workshop for SUCs,” Angat, Bulacan.

Ganguly, S., I. Paul, and S. K. Mukhopadhayay. 2010. “Application and Effectiveness of Immunostim-ulants, Probiotics, and Prebiotics in Aquacul-ture: A Review.” The Israeli Journal of Aquacul-ture - Bamidgeh 62: 130–138.

Gonzal, A. C., C. B. Santiago, A. C. Fermin, and E. V. Aralar. 2001. “Induced Breeding and Seed Production of Bighead Carp Aristichthys nobilis (Richardson).” Aquaculture Extension Manual No. 33. Tigbauan, Iloilo, Philippines: SEAF-DEC Aquaculture Department.

Graslund, S., and B. Bengstsson. 2001. “Chemicals and Biological Products Used in South-East Asian

Shrimp Farming and Their Potential Impact on the Environment – A Review.” Science of the To-tal Environment 280: 93–131.

_______. 2014. “Impacts of Introduced Freshwater Fishes in the Philippines (1905–2013): A Re-view and Recommendations.” Philippine Journal of Science 143: 49–59.

Gupta, M., and B. O. Acosta. 2004. “A Review of Global Tilapia Farming Practices.” Aquaculture Asia IX: 7–12.

Hargreaves, J. A. 2013. Biofloc Production Systems for Aquaculture. Publication 4503. Stoneville, Mis-sissippi: Southern Regional Aquaculture Center.

Howgate, P. 1998. “Review of the Public Heath Safe-ty of Products from Aquaculture.” International Journal of Food Science & Technology 33: 99–125.

Hubilla, M., F. Kis, and J. Primavera. 2008. “Janitor fish Pterygoplichthys disjunctivus in the Agusan Marsh: A Threat to Freshwater Biodiversity.” Journal of Environmental Science and Manage-ment 10 (1):10–23.

ICMSF (International Commission on Microbiologi-cal Specifications for Food), 1986.

Inglis, V., S. Z. Abdullah, S. L. Angka, S. Chinabut, B. R. Chowdhury, E. M. Leano, I. H. MacRae, A. Sasongko, T. Somsiri, and A. V. Yambot. 1997. “Survey of Resistance to Antibacterial Agents Used in Aquaculture in Five South East Asian countries.” In Diseases in Asian aquaculture III, 331–337. Manila, Philippines: Fish Health Sec-tion, Asian Fisheries Society.

Innal, D., and F. Erk’akan. 2006. “Effects of Exotic and Translocated Fish Species in the Inland Waters of Turkey.” Reviews in Fish Biology and Fisheries 16: 39–50.

Inglis, V. 2000. Antibacterial chemotherapy in aquacul-ture: review of practice, associated risks and need for action. In Use of Chemicals in Aquaculture in Asia: Proceedings of the Meeting on the Use of Chemicals in Aquaculture in Asia 20–22 May 1996, Tigbauan, Iloilo, Philippines (pp. 7–22). SEAFDEC Aquaculture Department.

Page 74: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector62

Israel, D. C., M. C. Boni-Cortez, M. E. Patambang. 2008. Aquacutlure Development in Laguna de Bay: An Economic Analysis. Terminal Report. Tigbauan, Iloilo, Philippines: SEAFDEC Aqua-culture Department.

IUCN/SSC (International Union for Conservation of Nature/Species Survival Commission) Criteria Review Working Group. 1999. “IUCN Red List Criteria Review Provisional Report: Draft of the Proposed Changes and Recommendations.”

Joshi, R. C. 2006. “Invasive Alien Species (IAS): Con-cerns and Status in the Philippines.” Accessed October 22, 2015. www.agnet.org/activities/sw/2006/589543823/paper-729213301.pdf.

Juario, J. V., M. N. Duray, V. M. Duray, J. F. Nacario, and J. M. Almendras. 1984. “Induced Breeding and Larval Rearing Experiments with Milkfish Chanos chanos (Forskal) in the Philippines.” Aquaculture 36: 61–70.

Juliano, R. O., R. D. Guerrero III, and I. Ronquil-lo. 1989. “The Introduction of Exotic Aquatic Species in the Philippines.” In Exotic Aquatic Organisms in Asia, edited by S.S. de Silva, 83–90. Proceedings of the Workshop on Introduc-tion of Exotic Organisms in Asia. Special Pub-lication 3, Manila, Philippines: Asian Fisheries Society.

Jumawan, J. C., B. M. Vallejo, A. A. Herrera, C. C. Buerano, and I. K. C. Fontanilla. 2011. “DNA Barcodes of the Suckermouth Sailfin Catfish Pterygoplichthys (Siluriformes: Loricariidae) in the Marikina River System, Philippines: Molec-ular Perspective of an Invasive Alien Fish Spe-cies.” Philippine Science Letters 4: 103–113.

Kathiresan, K., and N. Rajendran. 2005. “Coastal Mangrove Forests Mitigated Tsunami.” Estua-rine, Coastal and Shelf Science 65: 601–606.

Kungvankij, P., I. O. Potestas, B. P. Pudadera, and L. B. Tiro. 1986. “Induced Spawning and Lar-val Rearing of grouper (Epinephelus salmoides Maxwell). In The First Asian Fisheries Forum, 663–666.

Landau, M. 1992. Introduction to Aquaculture. New York: John Wiley & Sons.

Lezama-Cervantes, C., and J. Paniagua-Michel. 2010. “Effects of Constructed Microbial Mats on Water Quality and Performance of Litopenaeus vannamei Post-Larvae.” Aquaculture Engineering 42: 75–81.

Liao, I. C., J. V. Juario, S. Kumagai, H. Nakajima, M. Natividad, and P. Buri. 1979. “On the Induced Spawning and Larval Rearing of Milkfish, Cha-nos (Forskal).” Aquaculture 18: 75–93.

Licamele, J. D. 2009. “Biomass Production and Nutri-ent Dynamics in an Aquaponics System.” Ph.D. Dissertation, University of Arizona.

Linde-Arias, A. R., A. F. Inácio, C. de Alburquerque, M. M. Freire, and J. C. Moreira. 2008. “Bio-markers in an Invasive Fish Species, Oreochromis niloticus, to Assess the Effects of Pollution in a Highly Degraded Brazilian River.” Science of the Total Environment 399: 186–192.

Macaranas, J. M., L. Q. Agustin, M. C. A. Ablan, M. J. R. Pante, A. A. Eknath, and R. S. Pullin. 1995. “Genetic Improvement of Farmed Tilapias: Bio-chemical Characterization of Strain Differences in Nile Tilapia.” Aquaculture International 3: 43–54.

Magcale-Macandog, D. B., Jaderick P. Pabico, Felino P. Lansigan, Arnold R. Salvacion, Keshia N. Ting-son, Jennifer D. Edrial, and Marlon A. Reblora. 2013. “Development of a Predictive Model for the Occurrence of a Fish Kill in Volcanic Taal Lake.” FEWS 4 Project Terminal Report sub-mitted to the Philippine Council for Agricul-ture, Aquatic and Natural Resources Research and Development – Department of Science and Technology (PCAARRD-DOST).

Manning, T. S., and G. R. Gibson. 2004. “Prebiotics.” Best Practice & Research Clinical Gastroenterology 18: 287–298.

Marshall, N. 1994. “Mangrove Conservation in Rela-tion to Overall Environmental Consideration.” Hydrobiologia 285: 303–309.

Page 75: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

REFERENCES 63

Marshall, B. M., and S. B. Levy. 2011. “Food Animals and Antimicrobials: Impacts on Human Health.” Clinical Microbiology Reviews 24: 718–733.

Marte, C. L., and F. Lacanilao. 1986. “Spontaneous Maturation and Spawning of Milkfish in Float-ing Net Cages.” Aquaculture 53: 115–132.

Marte, C. L., N. M. Sherwood, L. W. Crim, and B. Harvey. 1987. “Induced Spawning of Maturing Milkfish (Chanos chanos Forsskal) with Gonado-tropin-Releasing Hormone (GnRH) Analogues Administered in Various Ways.” Aquaculture 60: 303–310.

Marti-Cardona, B., Steissberg, T. E., Schladow, S. G., & Hook, S. J. (2008). Relating fish kills to up-wellings and wind patterns in the Salton Sea.Hy-drobiologia, 604(1), 85-95.

McGlone, M. L., R. V. Azanza, C. L. Villanoy, and G. S. Jacinto. 2008. “Eutrophic Waters, Algal Bloom and Fish Kill in Fish Farming Areas in Bolinao, Pangasinan, Philippines.” Marine Pol-lution Bulletin 57: 295–301.

Mine, S., and R. Boopathy. 2011. “Effect of Organic Acids on Shrimp Pathogen, Vibrio harveyi.” Cur-rent Microbiology 63: 1–7.

Mooney, H. A., and E. E. Cleland. 2001. “The Evo-lutionary Impact of Invasive Species.” Proceed-ings of the National Academy of Sciences 98: 5446–5451.

NACA (Network of Aquculture Centres in Asia). 1989. “Integrated Fish Farming in China.” FAO NACA Technical Manual 7. A World Food Day Publication of the Network of Aquaculture Centres in Asia and the Pacific, Bangkok, Thailand.

NCSB (National Statistical Coordination Board). Ac-cessed November 10, 2015. http://nap.psa.gov.ph/secstat/d_popn.asp.

Ng, W. K., C. B. Koh, K. Sudesh, and A. Siti-Zah-rah. 2009. “Effects of Dietary Organic Acids on Growth, Nutrient Digestibility and Gut Microflora of Red Hybrid Tilapia, Oreochromis sp., and Subsequent Survival during a Challenge

Test with Streptococcus agalactiae.” Aquaculture Research 40: 1490–1500.

Ögretmen, F., and K. Gökçek. 2013. “Comparative Efficacy of Three Anesthetic Agents on Juvenile African Catfish, Clarias gariepinus (Burchell, 1822).” Turkish Journal of Fisheries and Aquatic Sciences 13: 51–56.

Ordoñez, J. F. F., Asis, A. M. J. M., Catacutan, B. J., dela Pena, J., & Santos, M. D. (2015). First re-port on the occurrence of invasive black-chin ti-lapia Sarotherodon melanotheron (Ruppell, 1852) in Manila Bay and of Mayan cichlid Cichlasoma urophthalmus (Gunther, 1892) in the Philip-pines. BioInvasions Records, 4(2), 115–124.

Pagulayan, R. C. 1997. “Update on Freshwater Mol-lusk Research in the Philippines.” In Aquatic Biology Research and Development in the Phil-ippines, edited by R. D. Guerrero III, A. Tisi-co-Calpe, and L. C. Darvin, 69–80. PCAMRD, Los Baños, Laguna.

Pandian, T. J., and S. G. Sheela. 1995. “Hormonal Induction of Sex Reversal in Fish.” Aquaculture 138: 1–22.

Papa, R. D. S., & Mamaril Sr, A. C. (2011). History of the biodiversity and limno-ecological studies on Lake Taal with notes on the current state of Philippine limnology. Philippine Science Let-ters, 4(1), 1–10.

Philippine Veterinary Drug Directory. 2006. 8th Edition.

PNS/BAFPS (Philippine National Standards/Bureau of Agriculture and Fisheries Product Standards) 84: 2010. “Aquaculture Feeds.” Philippine Nation-al Standards, Bureau of Agriculture and Fish-eries Product Standards and Bureau of Product Standards.

PNS/BAFS 136:2014. “Fresh and Frozen Cephalo-pods.” Philippine National Standards, Bureau of Agriculture and Fisheries Product Standards and Bureau of Product Standards.

PNS/BAFS 137:2014. “Fresh-Chilled and Fresh-Fro-zen Tuna for Sashimi.” Philippine National

Page 76: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector64

Standards, Bureau of Agriculture and Fisher-ies Product Standards and Bureau of Product Standards.

PNS/BAFPS 128:2013. “Dried Sea Cucumber.” Phil-ippine National Standards, Bureau of Agricul-ture and Fisheries Product Standards and Bureau of Product Standards.

PNS/BAFPS 135:2014. “Code of Good Aquaculture Practice.” Philippine National Standards, Bureau of Agriculture and Fisheries Product Standards and Bureau of Product Standards.

PNS/BAFPS 66:2008. “Frozen Milkfish.” Philippine National Standards, Bureau of Agriculture and Fisheries Product Standards and Bureau of Prod-uct Standards.

PNS/BAFPS 67:2008. “Frozen Tilapia.” Philippine National Standards, Bureau of Agriculture and Fisheries Product Standards and Bureau of Prod-uct Standards.

PNS/BAFPS 68:2008. “Dried Danggit.” Philippine National Standards, Bureau of Agriculture and Fisheries Product Standards and Bureau of Prod-uct Standards.

PNS/BAFPS 70:2008. “Quick Frozen Shrimps or Prawns.” Philippine National Standards, Bureau of Agriculture and Fisheries Product Standards and Bureau of Product Standards.

PNS/BAFPS 72:2009. “Live, Chilled/Frozen Abalone.” Philippine National Standards, Bureau of Agri-culture and Fisheries Product Standards and Bu-reau of Product Standards.

PNS/BAFPS 73:2009. “Live, Chilled/Frozen Grou-per.” Philippine National Standards, Bureau of Agriculture and Fisheries Product Standards and Bureau of Product Standards.

PNS/BAFPS 91:2011. “Quick Frozen Lobsters.” Phil-ippine National Standards, Bureau of Agricul-ture and Fisheries Product Standards and Bureau of Product Standards.

PSA (Philippine Statistics Authority). 2015. Selected Statistics in Agriculture. Republic of the Philip-pines: PSA.

Popma, T. J., and B. W. Green. 1990. Sex Reversal of Ti-lapia in Earthen Ponds. Aquaculture Production Manual. Research and Development Series No. 35. Alabama: Auburn University.

Primavera, J. H. 1991. “Intensive Prawn Farming in the Philippines: Ecological, Social, and Eco-nomic Implications.” AMBIO: A Journal of the Human Environment 20: 28–33.

_______. 1993. “A Critical Review of Shrimp Pond Culture in the Philippines.” Reviews in Fisheries Science 1: 151–201.

_______. 1994. “Shrimp Farming in the Asia-Pacif-ic: Environment and Trade Issues and Regional Cooperation.” Workshop on Trade and Environ-ment in Asia Pacific, East-West Center, Honolu-lu, USA, September 23–25.

_______. 1995. “Mangrove and Brackish Water Pond Culture in the Philippines.” Hydrobiologia 295: 303–309.

Primavera, J. H., and R. F. Agbayani. 1997. “Compar-ative Strategies in Community-Based Mangrove Rehabilitation Programs in the Philippines.” In Community Participation in Conservation, Sus-tainable Use and Rehabilitation of Mangroves in Southeast Asia, edited by N. H. Phan, N. Ish-waran, T. S. Hoang, H. T. Nguyen, and S. T. Mai, 229–243. Hanoi, Vietnam: United Nations Educational Scientific and Cultural Organisa-tion; Japanese Man and the Biosphere Nation-al Committee; Mangrove Ecosystem Research Centre. Proceedings of the ECOTONE V, 8–12 January 1996, Ho Chi Minh City, Vietnam.

Primavera, J. H., C. R. Lavilla-Pitogo, J. M. Ladja, and M. D. Pena. 1993. “A Survey of Chemical and Biological Products Used in Intensive Prawn Farms in the Philippines.” Marine Pollution Bul-letin 26: 35–40.

PSA (Philippine Statistics Authority). 2015. Database. http://countrystat.psa.gov.ph/.

Ren, J. S., J. Stenton-Dozey, D. R. Plew, J. Fang, and M. Gall. 2012. “An Ecosystem Model for Op-timising Production in Integrated Multitrophic

Page 77: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

REFERENCES 65

Aquaculture Systems.” Ecological Modelling 246: 34–46.

Reyes, O. S., E. G. T. de Jesus-Ayson, B. E. Eullaran, V. L. Corre Jr., and F. G. Ayson. 2015. Devel-opment and Management of Milkfish Mroodstock. Aquaculture Extension Manual No. 62. Tigbau-an, Iloilo, Philippines: SEAFDEC Aquaculture Department.

Rico, A., K. Satapornvanit, M. M. Haque, J. Min, P. T. Nguyen, T. C. Telfer, and P. J. van den Brink. 2012. “Use of Chemicals and Biological Prod-ucts in Asian Aquaculture and Their Potential Environmental Risks: A Critical Review.” Re-views in Aquaculture 4: 75–93.

Ringø, E., R. E. Olsen, T. Ø. Gifstad, R. A. Dalmo, H. Amlund, G. I. HEMRE, and A. M. Bakke. 2010. “Prebiotics in Aquaculture: A Review.” Aquaculture Nutrition 16 (2): 117–136.

Ringø, E., Zhou, Z., Olsen, R. E., & Song, S. K. (2012). Use of chitin and krill in aquaculture–the effect on gut microbiota and the immune system: a review.Aquaculture Nutrition, 18(2), 117-131.

Salayo, N. D., M. L. Perez, L. R. Garces, M. D. Pido. 2012. “Mariculture Development and Liveli-hood Diversification in the Philippines.” Marine Policy 36: 867–881.

Sapkota, A., A. R. Sapkota, M. Kucharski, J. Burke, S. McKenzie, P. Walker, and R. Lawrence. 2008. “Aquaculture Practices and Potential Human Health Risks: Current Knowledge and Fu-ture Priorities.” Environment International 34: 1215–1226.

Sasekumar, A., V. C. Chong, M.U. Leh, R. D’Cruz. 1992. “Mangroves as a Habitat for Fish Prawns.” Hydrobiologia 247: 195–207.

Schwab, K. J., F. H. Neill, M. K. Estes, T. G. Metcalf, and R. L. Atmar. 1998. “Distribution of Nor-walk Virus within Shellfish following Bioaccu-mulation and Subsequent Depuration by Detec-tion Using RT-PCR.” Journal of Food Protection 61: 1674–1680.

Siddall, S. E., J. A. Atchue III, and P. L. Murray Jr. 1985. “Mariculture Development in Mangroves: A Case Study of the Philippines, Panama and Ecuador.” In Coastal Resources Management: Development Case Studies, edited by J. R. Clark. Renewable Re-sources Information Series, Coastal Management Pub. No. 3. Columbia, SC: Research Planning Institute, Inc. Prepared for the National Park Ser-vice, U.S. Department of Interior, and the U.S. Agency for International Development.

Spoehr, A. 1984. “Change in Philippine Capture Fish-eries: An Historical Overview.” Quarterly of Cul-ture and Society 12: 25–56.

Strange, R. J., and C. B. Schreck. 1978. “Anesthetic and Handling Stress on Survival and Cortisol Concentration in Yearling Chinook Salmon (Oncorhynchus tshawytscha).” Journal of the Fish-eries Board of Canada 35: 345–349.

Sumagaysay-Chavoso, N. S. 2007. “Analysis of Feeds and Fertilizers for Sustainable Aquaculture De-velopment in the Philippines.” In Study and Analysis of Feeds and Fertilizers for Sustainable Aquaculture Development, edited by M. R. Hasan, T. Hecht, S. S. De Silva, and A. G. J. Tacon, 269–308. FAO Fisheries Technical Pa-per. No. 497. Rome: FAO.

Tam, N. F. Y., and Y. S. Wong. 1999. “Mangrove Soils in Removing Pollutants from Municipal Waste-water of Different Salinities.” Journal of Environ-mental Quality 28: 556–564.

Tan, R. L., Y. T. Garcia, and I. M. A. Tan. 2011. “Tech-nical Efficiency and Profitability of Tilapia and Milkfish Growout Cage Operations in Taal Lake, Philippines.” In Development, Natural Resources and the Environment, edited by G. P. Carnaje and L. S. Cabanilla, 130–154.

Tan-Fermin, J. D., & Emata, A. C. (1993). Induced spawning by LHRHa and pimozide in the Asian catfish Clarias macrocephalus (Gunther). Jour-nal of applied ichthyology, 9(2), 89-96.

Tan-Fermin, J. D., A. C. Fermin, R. F. Bombeo, M. A. D. Evangelista, M. R. Catacutan, and C. B.

Page 78: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector66

Santiago. 2008. Breeding and Seed Production of the Asian Catfish Clarias microcephalus (Gun-ther). Aquaculture Extension Manual No. 40. Tigbauan, Iloilo, Philippines: SEAFDEC Aqua-culture Department.

Tendencia, E. A., and L. D. de la Peña. 2001. “Antibi-otic Resistance of Bacteria from Shrimp Ponds.” Aquaculture 195: 193–204.

Trading Economics. 2015. Accessed November 15, 2015. http://www.tradingeconomics.com/ philippines/population.

Trushenski, J. T., C. S. Kasper, and C. C. Kohler. 2006. “Challenges and Opportunities in Finfish Nu-trition.” North American Journal of Aquaculture 68: 122–140.

Valiela, I., J. L. Bowen, and J. K. York. 2001. “Man-grove Forests: One of the World’s Threatened Major Tropical Environments.” Bioscience 51: 807–815.

Venkat, H. K., N. P. Sahu, and K. K. Jain. 2004. “Effect of Feeding Lactobacillus-based Probiotics on the Gut Microflora, Growth and Survival of Post-larvae of Macrobrachium rosenbergii (de Man).” Aquaculture Research 35: 501–507.

Villaluz, D. K. 1966. “The Lake Lanao Fisheries and Their Conservation.” Manila, Philippines: Bu-reau of Printing.

Wang, X., D. Ryu, R. H. Houtkooper, and J. Auwerx. 2015. “Antibiotic Use and Abuse: A Threat to Mitochondria and Chloroplasts with Impact on

Research, Health, and Environment.” Bioessays 37: 1045–1053.

Wang, Y. B. 2007. “Effect of Probiotics on Growth Performance and Digestive Enzyme Activity of the Shrimp Penaeus vannamei.” Aquaculture 269: 259–264.

White, A., E. Deguit, W. Jatulan, and L. Eisma-Osorio. 2006. “Integrated Coastal Management in Phil-ippine Local Governance: Evolution and Bene-fits.” Coastal Management 34: 287–302.

White, P., R. Palerud, G. Christensen, T. Legović, and R. Regpala. 2008. “Recommendations for Prac-tical Measures to Mitigate the Impact of Aqua-culture on the Environment in Three Areas of the Philippines.” Science Diliman 20: 41–48.

Williams, J. E., J. E. Johnson, D. A. Hendrickson, S. Contreras-Balderas, J. D. Williams, M. Navar-ro-Mendoza, D. E. McAllister, and J. E. Deacon. 1989. “Fishes of North America Endangered, Threatened, or of Special Concern: 1989.” Fish-eries 14: 2–20.

Yambot, A. V. (2000). Problems and issues of Nile tila-pia cage farming in Taal Lake, Philippines. In 1. International Symposium on Cage Aquaculture in Asia, Tungkang, Pintung (Taiwan), 2–6 Nov 1999. AFS; WAS-SC.

Zimmermann, B., E. Bauer, and R. Mosenthin. 2001. “Pro- and Prebiotics in Pig Nutrition-Potential Modulators of Gut Health?” Journal of Animal and Feed Sciences 10: 47–56.

Page 79: An Overview of - World Bankdocuments.worldbank.org/curated/en/926231516770019437/...vi An Overview of Agricultural Pollution in the Philippines: The Fisheries Sector Table 6: Use and

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