Philippine Journal of Science 143 (1): 49-59, June 2014 ISSN 0031 - 7683 Date Received: 06 January 2014

Impacts of Introduced Freshwater Fishes in the (1905-2013): A Review and Recommendations

Rafael D. Guerrero III

National Academy of Science and Technology, Philippines Philippine Heritage Center, DOST Compound, Metro Manila, Philippines

Based on existing records and observations, 62 freshwater fishes were introduced from 1905 to 2013 in the Philippines for aquaculture (45%), ornamental purpose (42%), recreational fishing (6%), and mosquito control (6%). An evaluation showed that 48 (77%) of the fishes are beneficial, 10 (16%) are invasive, and 4 (6%) are potentially invasive. In terms of of economic benefits, the gains derived from the introduction of beneficial fishes, particularly for culture and fisheries enhancement, are much more compared to the economic losses due to the negative impacts of invasive fishes. A review of the national policies and regulations on the introduction of imported live fishes showed that the required processes are adequate and in place. However, there are gaps that need to be urgently addressed to strengthen monitoring, surveillance and control to prevent the spread of the six invasive ornamental fishes now established in inland waters and to forestall the escapes of the potentially invasive fishes.

Key Words: Alien species, Aquaculture, Exotic species, Fisheries, Introductions, Invasive species

INTRODUCTION biological diversity.” With globalization, the transport of plants and Introduced aquatic species may have environmental, from one country to another through human intervention social and economic impacts. Species introductions can has been facilitated. The intentional or unintentional improve production and economic benefits from fisheries introduction of living organisms for economic and other and aquaculture. It has been estimated that 17% of the reasons can have beneficial or adverse impacts (Bruton & world’s finfish production is attributed to alien species. Merron 1985; De Silva 1989). Next to habitat destruction, Such species have “more positive socioeconomic benefits the introduction of “invasive species” is the second major reported than negative ecological impacts” (FAO 2014). cause of loss of biodiversity (IUCN 1999). Exotic fishes capable of breeding naturally in areas where Introduced aquatic animals such as fishes are defined they are introduced can become established with “open as those that have been transported into aquatic habitats or occupied niches” and replace local species due to outside their native range for the species (ICES 2003). their “numerical and/or fitness advantage” (Stachowicz Exotic or alien species are those that have been transferred & Tilman 2005). Invasive fishes can also cause genetic from one country to another or from one body of water to pollution with “uncontrolled hybridization, introgression another where they are non-native. Invasive alien species and genetic swamping” (Mooney & Cleland 2001). is defined by the Convention on Biological Diversity According to the Global Invasive Species Programme (2014) as “species whose introduction and/or spread (1999), “invasive alien species are a global threat whose outside their natural past or present distribution threaten impacts cost at least US$ 1.4 trillion annually and will have to be managed in perpetuity.” *Corresponding author: [email protected]

49 Philippine Journal of Science Guerrero III RD: Impacts of Introduced Freshwater Vol. 143 No. 1, June 2014 Fishes in the Philippines

In the Philippines, Juliano et al. (1989) reported the that 48 (77%) of the introduced fishes have been beneficial introduction of 34 freshwater fishes into the Philippines in terms of contributing to fish production in the country, from 1905 to 1988 for aquaculture, ornamental fish, for ornamental purpose, recreational fishing and biological biological control and sport fishing. The loss of 15 of the control of mosquitoes. Ten (16%) introduced fishes are 18 endemic cyprinids in Lake Lanao (Lanao del Sur) has considered invasive for causing ecological and/or economic been attributed to the accidental introduction of the white loss and four (6%) are regarded as potentially invasive goby, Glossogobius giuris (Juliano et al. 1989) and the species. eleotrid, Hypseleotris agilis, from Lake Mainit (Surigao) in Mindanao (Escudero 1993). According to FishBase Introduced Fishes for Culture (2013), of the 348 freshwater fishes in the Philippines, Of the 28 fishes introduced for aquaculture (food), 24 (86%) 195 are native (56%), 96 (28%) are endemic and 57 (16%) have been beneficial and only four (10%) have become are introduced. invasive. Seventeen fishes (61%) have become established Joshi (2006) noted that the impacts of invasive alien by successfully breeding in open waters (rivers and lakes) species (IAS) on native fishes in the Philippines are while three (11%) others have been artificially bred for “poorly understood because of lack of knowledge, lack culture. Eight (28%) introduced fishes have not become of expensive and comprehensive technical information, established because of their inability to in the wild. failure to realize the potential ecological damage to Among the introduced freshwater fishes that have made biodiversity and consequent economic losses and significant contributions to the fish production of the as possible hazards to human health, failure of country are the cultured tilapias, mainly the Nile tilapia implementation of laws on introduction of exotic species, (Oreochromis niloticus), carps, particularly the bighead and unwillingness to interfere in the commerce and trade carp (Aristichthys nobilis), and catfishes (Clarias of exotic species.” gariepinus and Pangasiodon hyopthalamus). In 2012, Information is limited on the impacts of fish introductions according to the fisheries statistics of the country (BAS in the Philippines. Based on information in FishBase, such 2013), the fishes contributed 290,513 mt to the total introductions had 62% unknown ecological impact and farmed fish production with a value of over PhP 20.16 54% unknown socio-economic impact (Casal & Bartley billion. From freshwater inland waters, the introduced 2000). There have been many unreported introductions fishes Nile tilapia (O. niloticus), carp (Cyprinus carpio), and data on documented reports need to be updated (Casal mudfish (Channa striata), Asiatic catish (Clarias 2005; FAO 2014). batrachus) and gourami (Trichopterus spp.) contributed 88,216 mt to the total inland fisheries production with a This study was conducted to review and assess the value of more than PhP 5.3 billion (BAS 2014). The Nile impacts of the introduced exotic freshwater fishes in tilapia stocked in lakes and reservoirs has also markedly the Philippines from 1905 to 2013 with the end in view enhanced fisheries in such water bodies with no evidence of recommending improvements in the processes and of adverse effect on the native fish fauna (Guerrero 1999). policies for the effective regulation and management of such introductions. The four fishes introduced for culture in the country that have become invasive are the Channa striata, In gathering data and information for the study, available Clarias batrachus, Monopterus albus and Oreochromis literature (published and unpublished) including data mossambicus. The mudfish (C. striata) is considered from FisBase and the FAO Database on Invasive Aquatic a pest for preying on the young of cultured fish such Species were reviewed, interviews with concerned as the Nile tilapia when it intrudes freshwater ponds persons of the Bureau of Fisheries and Aquatic Resources from the wild (Guerrero et al. 1990). The Asiatic catfish (BFAR) and other resource persons were conducted, and (C. batrachus) has been recorded to have ecologically site visits to fish markets and pet shops were displaced the native catfish (C. macrocephalus) in Laguna made. Information from national newspapers and publicly de Bay (Juliano et al. 1989) and other water bodies in televised programs were also sourced. Luzon where it has been introduced. The rice paddy eel (M. albus) has been reported to infest rice paddies in the Introduced Freshwater Fishes in the Philippines Cagayan Valley. Locally known as “kiwet,” it feeds on (1905-2013) and Their Impacts small fish, frogs and shrimp, and burrows into the bunds A total of 62 freshwater fishes was recorded/observed to of the paddies causing water loss (Lazaro 2013, Valencia be introduced in the Philippines for the period 1905-2013 2013). The Mozambique tilapia (O. mossambicus) (Table 1). Of these, 28 (45%) were for aquaculture, 26 has invaded brackishwater ponds for milkfish (Chanos (42%) for ornamental purpose, four (6%) for sport fishing, chanos) culture and competed for food and space (Juliano and four (6%) for mosquito control. An evaluation showed et al. 1989).

50 Philippine Journal of Science Guerrero III RD: Impacts of Introduced Freshwater Vol. 143 No. 1, June 2014 Fishes in the Philippines

Table 1. Status and impacts of introduced exotic freshwater fishes in the Philippines (1905-2013). Introduction Species Origin Year Status Impact Amatitlania nigrofasciatab ? ? O, En B (Convict )

b Anabas testudineus Malaysia ? C, En, W B (Climbing perch) Aplocheilus panchaxb ? ? O, En B (Killie) Arapaima gigasp South America ? O, En PI (Arapaima) Aristichthys nobilisab Taiwan 1968 C, Ei B (Bighead carp) Austrolebias nigripinnisb Argentina ? O, En B (Blackfin pearlfish) Barbonymus gonionotusab 1956 C, En, W B (Tawes) Bidyanus bidyanusb Australia 2005 C, N B (Silver perch) Carassius auratusb ? ? O, En B (Goldfish) Carassius carassiusab Japan 1964 C, EN, W B (Crucian carp) Catla catlaab India 1967 C, N B (Catla) Channa striatab Malaysia 1908 C, EN, W I (Mudfish) Channa micropeltespm ? O, EN, W I (Giant snakehead) chitalab Thailand ? O, EN, W Pi (Clown knifefish) Chitala ornatab Thailand ? O, EN I (Clown featherback) Cichla occularisp Central America ? O, EN PI (Peacock bass) Cirrhinus mrigalaab India 1967 C, N B (Mrigal carp) Clarias batrachusab Thailand 1972 C, EN, W I (Asiatic catfish) Clarias gariepinusab Taiwan 1985 C, Ei B (African catfish) Colossoma macropomumb ? O, EN B (Cachama) Ctenopharyngodon idellaab India 1967 C, N B (Grass carp) Cyprinus carpioab Hongkong 1915 C, EN, B (Common carp) Danio reriob ? ? O, EN B (Zebra danio) Fundulus heteroclitusab USA 1905 Bc, En, W B (Mosquito fish) Gambusia affinisab USA 1905 Bc, En, W B (Mosquito fish)

51 Philippine Journal of Science Guerrero III RD: Impacts of Introduced Freshwater Vol. 143 No. 1, June 2014 Fishes in the Philippines

Helostoma temminkiab Thailand 1950 O, En B (Kissing gourami) Hemichromis bimaculatusb ? ? O, En B (Jewel fish) Hyopthalmicthys molitrixab Taiwan 1968 C, N B (Silver carp) Ictalurus catusa USA 1935 C, N B (White catfish) Ictalurus punctatusab USA 1974 C, N B (Channel catfish) Labeo rohitaab India 1967 C, En, W B (Rohu) Lepomis cyanellusab USA 1950 R, N B (Green sunfish) Lepomis macrochirusab USA 1950 R, N B (Bluegill) Melanotaenia nigransd Australia ? O, En B (Rainbow fish) Micropterus salmoidesab USA 1915 R, N B (Largemouth bass) Micropterus salmoides floridanusa USA 1985 R, En, W B ( bass) Misgurnus anguillicaudatusab Japan 1937 C, En B (Dojo) Monopterus albusm Malaysia ? C, En, W I (Rice paddy eel) Oreochromis aureusab USA 1977 C, En B (Blue tilapia) Oreochromis hornorumc Singapore 1971 C, N B (Wami tilapia) Oreochromis mossambicusab Thailand 1950 C, En, W B (Mozambique tilapia) Oreochromis niloticusab Thailand 1972 C, En, W B (Nile tilapia) Oreochromis spirulusb Kuwait 2004 C, En B (Sabaki tilapia) Osphronemus goramyab Indonesia 1927 C, En, W B (Giant gouramy) Osteochilus hasseltia Indonesia 1957 O B (Hard-lipped barb) Osteoglossum bicirrhosind South America ? O B (Silver ) Pangasianodon hyopthalamusab Thailand 1978 C, Ei B (Pangasius) managuensisb Central America ? O, En, W I (Jaguar guapote) Piaractus brachypomusb South America ? O, En, W B (Pacu) Poecila latipinnaab Mexico 1914 Bc, En, W B (Sailfin molly) Poecila reticulataab USA 1905 Bc, En, W B (Guppy) Poecilia sphenopsb ? ? O, En B (Molly)

52 Philippine Journal of Science Guerrero III RD: Impacts of Introduced Freshwater Vol. 143 No. 1, June 2014 Fishes in the Philippines

Pterygoplichthys disjunctivusb South America ? O, En, W I (Vermiculated sailfin catfish) Pterygoplichthys pardalisb South America ? O, En, W I (Amazon sailfin catfish) Pygocentrus nattererijp South America ? O, En PI (Red-bellied-piranha) Sarotherodon melanotheronp ? ? O, En, W I (Black-chinned tilapia) Scleropages formosusb ? ? O, En B (Golden arowana) Syptomus tetrazonab ? ? O, En B (Sumatra barb) Tilapia zilliiab Israel 1977 C, En, W B (Red-bellied tilapia) Trichopterus leeriab Thailand 1938 C, En, W B (Pearl gouramy) Trichopterus pectoralisab Thailand 1938 C, En, W B (Snakeskin gouramy) Trichopterus trichopterusab Thailand 1938 C, En, W B aJuliano et al. (1989) C-Culture En-Natural breeding B-Benificial bFishbase (2013) O-Ornamental Ei-Induced breeding I-Invasive cRabanal (2000) Bc-Biological Control W-Found in wild Pi-Potentially invasive dFAO-DIAS (2014) R-Recreational N-Not existing ?-Unknown jJoshi (2006) mMedia pPersonal observation

Introduced Fishes for Ornamental Purpose The presence of the P. managuensis, a cichlid from Of the 26 fishes introduced for ornamental purpose, 16 Central America, in Lake Taal (Batangas) was first noted (62%) are considered beneficial or non-invasive while in 2003 (Agasen et al. 2006). There is no record of its six (23%) have become invasive upon “escaping” from introduction with the BFAR, the national agency tasked commercial and/or private keepers into open waters and with the regulation of imported fish introductions. The four (15%) others are regarded as potentially invasive piscivorous fish, locally known as “dugong” was found to fishes. have predated on and competed for the niche occupied by native fishes (Leiotherapon plumbeus and Glossogobius The six invasive fishes are the “janitor fish” giurus) in the lake (Rosana et al. 2006). It is not known (Pterydoplicthys disjunctivus and P. pardalis), the how the “jaguar guapote” got into the lake. “jaguar guapote” (Parachromis managuensis), the “clown featherback” (Chitala ornata), the “giant snakehead” The “clown featherback” (C. ornata), a native of Thailand, (Channa micropeltes), and the “black-chinned tilapia” is locally known as “arowana.” It was introduced in the (Sarotherodon melanotheron). country with permit from the BFAR. First observed in Laguna de Bay in 2011 (Palma pers. comm.), it is believed The P. dysjunctivus as a nuisance fish has caused economic to have escaped into the lake after a flooding event losses to fisherfolk in Laguna de Bay by reducing their caused by Typhoon Ondoy in 2009. An economic impact fish catch with gill nets and fish corrals (Chavez et al. assessment conducted by Palma (pers. comm.) showed 2006) and in Agusan Marsh (Hubilla et al. 2007). In that the species is “highly predaceous” on the cultured 2002, the LLDA (2005) reported that the invasive fish fishes (milkfish and Nile tilapia) and native fishes in the comprised 10-38% of the total fish corral catch in Siniloan, lake. In a fish catch survey, it comprised 40% of the total Laguna. The P. pardalis, on the other hand, is considered catch (3,15l kg/day) of the fisherfolk. Fortunately, the a pest with its burrowing habit in building nests which “clown knifefish” (C. chitala), a related species that is still have damaged the embankment of the Marikina River, being kept in aquaria by private and commercial keepers, a tributary of Laguna de Bay. The “janitor fish” was is not yet reported in our inland waters. introduced with authority from the Bureau of Fisheries and Aquatic Resources (BFAR) and is believed to have The “giant snakehead” (C. micropeltes), a native also of escaped into the lake from fishponds that were inundated Thailand, is locally known as “black mask.”It was reported in a lakeshore town. to be present in the Pantabangan Reservoir in Nueva Ecija

53 Philippine Journal of Science Guerrero III RD: Impacts of Introduced Freshwater Vol. 143 No. 1, June 2014 Fishes in the Philippines by a televised program, “Born To Be Wild.” It is said species. It feeds mainly on fish, aquatic insects, to be predaceous on the Nile tilapia and other fishes in invertebrates, mollusks and crustaceans, and grows the reservoir (Anon 2013). Although the live snakehead to a length of 33 centimeters and weight of 3.5 kilos. is on display in a commercial freshwater aquarium fish Among its negative impacts is its ability to cause human establishment in Pasig City, no official record of its injuries through bites or stings (Fuller et al. 1999). The introduction in the country is available. reputation of the piranha as a “man-eater” is said to be exaggerated and “it is unlikely to become widespread The “black-chinned tilapia”, Sarotherodon melanotheron, outside its natural habitat” (Vincentin et al. 2012; Bleher a native of Africa, was first observed by the author in pers. comm.). Supposedly prohibited in the Philippines, Laguna de Bay in 2008. It is caught by fisherfolk and live breeders of the “red-bellied piranha” were seen on sold in public wet markets as a food fish at a much lower display at the aquarium establishment in Pasig City. price than that for the Nile tilapia also fished in the lake. A salt-tolerant species, the S. melanotheron was reported The invasive nature of which is still to be a nuisance fish competing for the food and space confined in public and private aquaria in the country of cultured stocks in the brackishwater fishponds of can be similar to that of Chitala ornata (a major pest in Bulacan (Chavez 2013; Cervantes 2013). No record of Laguna de Bay) if it gets into open waters accidentally its introduction is available. or intentionally. The introduced fishes for ornamental purpose now Upon verification with the BFAR’s Regulation and confined in private and/or public aquaria that are Quarantine Division (RQD), the unit tasked with considered to be potentially invasive species because of approving exotic fish introductions in the country, their predaceous feeding habit, capability of spawning in it was confirmed (Ricablanca pers. comm.) that the tropical waters and known bio-invasive record in other introduction of the Arapaima gigas has been authorized. countries are the Arapaima gigas, Cichla occularis, No authorization, however, has been given for the Pygocentrus nattereri, and Chitala chitala. introduction of Cichla occularis, Monopterus albus, and The “arapaima”, a native of the Central Amazon in Pygocentrus nattereri. South America, has been exploited for human food and introduced in Peru and Bolivia in the 1980s. It is a Introduced Fishes for Recreational Fishing piscivorous fish that grows to a length of 4 m and weight Of the four fishes introduced for recreational or sport of 200 kg. Its introduction in Bolivia has led to the decline fishing, only the Micropterus salmoides floridanus, in the native fish populations (Miranda-Chumacero et recorded to have been introduced in 1985 in the country al. 2012). Live breeders of the species were seen in two is believed to have become established in Lake Caliraya commercial freshwater fish aquarium establishments in (Laguna) which is 700 m above sea level (Juliano et al. Paranaque City and Pasig City on display. Live juveniles 1989). Fishing tournaments have been held in the lake of the fish were also found at a fish pet shop in Cartimar, with “catch and release” of the fish for conservation. Pasay City being sold at PhP 5,500 each. There is no report on the invasiveness of the species. The “peacock bass”, Cichla occularis, a native of South America, is also a piscivore that has been introduced Introduced Fishes for Biological Control in the lakes of Panama and Brazil for sport fishing. In All of the four introduced fishes for biological control Panama, it “caused significant damage to the native of mosquitoes in open waters have become established fish assemblage by eliminating 7 out of 11 previously in the country. Some have been considered invasive in common fish species” (Pelicice & Agostinho 2008) while freshwater and brackishwater fishponds as nuisance fishes in Brazil, there was a “95% decline in the fish density but to a limited extent. The “mosquito fish”, Gambusia and 80% decline in richness in only two years from its affinis, locally known as “kataba” or “milyon” can eat as introduction”(Latini & Petrere 2004). Live breeders of many mosquito wrigglers as its weight in a day (Guerrero C. occularis were seen on display at the commercial 2013). The introduced fishes have also been used as establisment in Pasig City and live juveniles for sale in a aquarium pets and for feeding highly-prized aquarium fish pet shop in Cartimar, Pasay City. fishes like the piscivorous “arowana” (Scleropages spp.) The “red-bellied piranha”, Pygocentrus nattereri, a native of the Amazon River in South America, is a popular Policies on Fish Introductions aquarium fish worldwide that has been prohibited in The Philippines is a participating State in the United over 20 states in the US. It has been found in the rivers Nations Convention on Biological Diversity (CBD) of Colorado, Texas and Florida because of aquarium which adopted the “Guiding Principles for the Prevention, pet releases and is believed to prey on native freshwater Introduction and Mitigation of Impacts of Alien Species

54 Philippine Journal of Science Guerrero III RD: Impacts of Introduced Freshwater Vol. 143 No. 1, June 2014 Fishes in the Philippines that Threaten Ecosystems, Habitats and Species.” (environment, disease and effect on endemic species) and Article 8 of the CBD (1992) provides the framework for inspection of the importer’s facilities by the BFAR’s Fish national governments on developing their own policies Health Section. and strategies on invasive alien species to prevent entry, minimize spread and impact of these species once Risk analysis is defined as a “structured process for introduced. analyzing the potential for the occurrence of unwanted, adverse consequences associated with some action over In the Food and Agriculture Organization Code of Conduct a specified time period. For trade on live aquatic animals for Responsible Fisheries (FAO 1995) under the purview and their products, a formal risk analysis approach of “unintentional and intentional introductions, it is stated provides objective, repeatable and documented methods that States should consult with their neighboring States, for identifying, assessing and considering management as appropriate, before introducing non-native species options for the risks associated with the export-imort into transboundary aquatic ecosystems” (Article 9.2.3). process” (Arthur et al. 2004). “Efforts should be taken to minimize the harmful effects of introducing non-native species into waters, especially In FAO No. 221, an IRA Panel chaired by a Fish Health where there is a significant potential for the spread of such Officer with five permanent members appointed by the non-native species into waters under the jurisdiction of BFAR Director is tasked to categorize the importation the State” (Article 9.3.1). of live fish as to whether they are “low, medium, high risk or prohibited species.” Moreover, the FAO defines In Section 10 of the Philippine Fisheries Code of 1998 “low risk species such as aquarium fish that are perceived (R.A. 8550) on Introduction of Foreign Aquatic Species, to present no ecological, genetic and disease threats to it is stated that: “No foreign finfish, mollusk, crustacean native Philippine species and to aquaculture; medium risk or aquatic plants shall be introduced in Philippine waters species are species used in aquaculture or in aquarium without a sound ecological, biological and environmental or ornamental fish trade considered to pose potential justification based on scientific studies subject to the environmental impact; high risk species are exotic species bio-safety standard as provided for by existing laws; that may most likely pose adverse environmental impact; provided, however, that the Department (of Agriculture) and prohibited or banned species are exotic species with may approve the introduction of foreign aquatic species known adverse effect on local fauna, human health and for scientific/research purposes.” the environment.” For the importation of foreign or exotic fishes, the BFAR’s A check made with the BFAR RQD showed that there is no FRQD has a 5-step process (Figure 1) prior to the issuance permanent Import Risk Analysis Panel existing (Piscano of the Sanitary and Phytosanitary (SPS) Certificate that pers. comm.) as stipulated in FAO No. 221. Presently, the is in compliance with the General Agreement on Tariffs IRA for fish introductions is conducted by the BFAR Fish and Trade (GATT) of the World Trade Organization Health Section which is staffed by veterinarians who are (WTO) of which the Philippines is a member of. The said more qualified for Pathogen Risk Analysis. Furthermore, process provided for by Fisheries Administrative Order the BFAR has no dedicated quarantine facilities for high (FAO) No. 221 starts with a Letter of Request to Import risk species as required by FAO 221. addressed to the Director of the BFAR accompanied by an Application for a Permit to Import which is then forwarded While the BFAR RQD has a List of Live Aquarium to the FRQD. The next steps include the conduct of an Fishes Allowed for Importation with a total of 91 species, Import Risk Analysis (IRA) for evaluation of risk factors there are errors in the scientific names of the fishes

Receiving & Conduct Import If approved by For Signature and Release to Review Letter Risk IRA, Processing/ Approval Applicant The request to Import Analysis (IRA) Typing of Sanitary SPS Certificate to Evaluation of Rish and Phytosanitary Import Live Fish Factors Certificate (SPS) to (Section Chief and Director’s Office & Import Live Fishes Division Chief) Regulatory and (Environment, Quarantine Division Disease and Effect on Endemic Species) Regulatory and Regulatory and Inspection of Quarantine Divsion Quarantine Division Regulatory Importer’s Facilities) and Quarantine Fish Health Station Division

Figure 1. Import Procedure for Live Fish/Aquatic Animals (FAO No. 221)

55 Philippine Journal of Science Guerrero III RD: Impacts of Introduced Freshwater Vol. 143 No. 1, June 2014 Fishes in the Philippines

(e.g., Plecostomus sp. should be Pterygoplicthys sp. and causing ecological/economic losses in the country, it is Pangasius sutchi should be Pangasiodon hyopthalamus). concluded that the economic benefits derived from the The list of introduced fishes for ornamental purpose in beneficial introductions are far more than the economic this study does not tally with that of the RQD. Moreover, losses caused by invasive species. While it is more the RQD has no List of Prohibited Species prepared by difficult to assess ecological impacts, it can be said that the the IRA Panel as stipulated in FAO No. 221 (Section 7). introduction of most of the exotic fishes for aquaculture, particularly for those that have become established, have As earlier stated, two invasive fishes, the “jaguar guapote” enriched fish biodiversity in the freshwater ecosystems (P. managuensis) and “giant snakehead” (C. micropeltes) of the country rather than exterminating local fishes. that were most probably introduced for ornamental A case in point is that of the native catfish, Clarias purpose in the country are not in the List of Aquarium macrocephalus, which has been displaced by the Fishes Allowed for Importation of the BFAR and have introduced C. batrachus in Luzon. The former species is no records of importation with the RQD. Such fishes still found in many parts of the country especially in the therefore can be considered illegal introductions. The Visayas and Mindanao where the Asiatic catfish has not live specimens of the Araipama gigas, Cichla occularis been introduced. Moreover, the C. macrocephalus is not and Pygocentrus nattereri seen on display or for sale endemic in the country and is abundantly found in other in commercial aquarium fish shops that are potentially Southeast Asian countries. invasive are apparently not known to the RQD. In FAO No. 221 (Section 10) : “High risk and prohibited species which have already entered the country without valid import permit prior to promulgation of this order RECOMMENDATIONS FOR IMPROVING shall be monitored and evaluated by the IRA Panel and those that are found to be causing any adverse effect on REGULATIONS AND PROCESSES FOR the local fauna, human health and environment shall be IMPORTATION OF LIVE FISHES confiscated for destruction.” In view of this regulation, To forestall further economic and ecological losses due to the said introduced ornamental fishes and the “high risk” the introduction of exotic freshwater fishes that can incur Chitala chitala still confined in captivity should be closely damage to the ecology, economy and humans, especially monitored and controlled by the BFAR to prevent their when they escape into inland waters and become invasive, accidental or intentional escape into inland waters. there is urgent need to improve the regulations and processes applied for the importation of live fishes. The following recommendations are proposed: CONCLUSION AND A permanent Import Risk Analysis (IRA) Panel should RECOMMENDATIONS be organized by the BFAR in compliance with FAO 221 for competent and expert screening of live fish import An evaluation of the 62 introduced exotic freshwater applications. fishes in the country showed that 48 (77%) are beneficial or non-harmful, 10 (16%) are harmful or invasive, and four There should be dedicated quarantine facilities of the (6%) can be considered to be potentially invasive species. BFAR at the international ports of entry (i.e. international This analysis indicated that the majority of the introduced airports) to ensure the proper processing screening of fishes for aquaculture, ornamental purpose, recreational live fish importations (legal and illegal) as stipulated in fishing and mosquito control have been beneficial for FAO 221. the country. Of the 12 invasive and potentially invasive In addition to an updated and revised (corrected) “List of fishes, only three were introduced for aquaculture while Approved Aquarium Fishes For Importation,” the BFAR’s nine were introduced for ornamental purpose showing FRQD should have a “List of Prohibited Fishes” or “Black that introductions for ornamental purpose have been List” that should include “high risk” species already in more problematic than those for aquaculture. Of the 62 the country (e.g., Chitala chitala) and/or reported to be introduced fishes recorded in this study, 58 have been invasive in other countries. reported in the FishBase and FAO-DIAS while the other four have been reported by other sources and personal There should be strict and continuous monitoring and observations. surveillance of aquarium pet shops in the country by the BFAR to ensure that no illegally introduced freshwater Considering the benefits gained from the introduction fishes are being disseminated. In this respect, it is of exotic fishes in terms of fish production, ornamental recommended that commercial aquarium fish shops be purpose, recreational fishing and mosquito control registered with the BFAR through the Local Government compared to the negative impacts of the invasive fishes Units which provide them with business permits.

56 Philippine Journal of Science Guerrero III RD: Impacts of Introduced Freshwater Vol. 143 No. 1, June 2014 Fishes in the Philippines

Commercial aquarium fish establishments or private for larger ones. With the increasing exploitation of the aquarists illegally keeping “high risk” freshwater fishes species in the lake, its population can be regulated and should be dealt with according to the law or held responsible/ fisheries management should be put in place. Its accidental liable for possible deliberate or accidental “escapees.” A or intentional introduction in other lakes and reservoirs of Surety Bond for such purpose may be imposed. the country should, however, be checked by the BFAR. The capability of the BFAR’s FRQD should be To control the population of the “janitor fish” in Laguna strengthened in terms of manpower and facilities to carry de Bay, a “Bounty System” wherein fisherfolk are out its functions more effectively. paid for the fish they catch has been initiated by the government. Although the fish is edible, its use as food The BFAR in coordination with other stakeholders (i.e. fish from the lake is not recommended because of possible Local Government Units, Laguna Lake Development contamination with heavy metals and E. coli (Chavez et Authority and Fisheries and Aquatic Resources Management al. 2006). Various ways of utilizing the fish for fish meal, Councils, etc.) should conduct ecological impact studies fertilizer, fish leather and office/home décor have been and research on mitigation measures for the control and recommended (Hubilla et al. 2007). preventive spread of invasive fishes now causing problems in Laguna de Bay, Lake Taal and Agusan Marsh. To mitigate the “clown featherback” in Laguna de Bay, initiatives like the “Bounty System” for the “janitor fish” A massive Information, Education and Communication and utilizing the fish for the making of fish leather (Abello (IEC) campaign should be launched by the BFAR through 2013) and processed food products such as “fish cakes” the mass media to drum up the negative impacts of and “fish balls” have been made by the BFAR. The fish invasive fishes and stir up public awareness on the need caught in Laguna de Bay is safe for human consumption for responsible aquarium fish pet care and environmental according to Palma (pers. comm.). In Thailand, this author protection. was informed by a colleague from Kasetsart University that the C. chitala which is native to his country is valued as a food fish (Satapornvanit pers. comm.). The fish is also said to be a traditional delicacy in Indonesia where it is a RECOMMENDATIONS FOR THE high-valued species. Measures to contain the species in MITIGATION OF INVASIVE FISHES IN Laguna de Bay and prevent its introduction in other water THE PHILIPPINES bodies should be adopted by the BFAR. The presence of Channa striata and Clarias batrachus in The case of the “black-chinned tilapia “(S. melanotheron) open waters has enhanced our inland water fisheries. The is considered to be similar to the introduction of the mudfish is considered a high-value fish in Central Luzon Oreochromis mossambicus for culture in the 1950s. The for the making of fermented fish. With the preference latter fish was initially a “pest” in brackishwater ponds of consumers for the native catfish which has a better in the country until the 1970s when it became used for meat texture, the Asiatic catfish caught by fisherfolk is aquaculture as a food fish with improved management sold commercially in wet markets at a lower price. As (Guerrero 1981). Studies on the S. melanotheron, a predators in freshwater fishponds for the culture of the salt-tolerant species, should be done, particularly on its Nile tilapia, the C. striata and C. batrahus are eradicated population control, so it can be properly managed and not during pond preparation with the use of fish toxicants be invasive in brackishwater ponds used for aquaculture. (Guerrero et al. 1990). The rice paddy eel, Monopterus albus, earlier reported to be a “pest” in Northern Luzon is now a major export Channa micropeltes found in Pantabangan Reservoir in commodity and may no longer be considered invasive. Nueva Ecija is at present being exploited by local fish According to the BFAR, the export of the live species anglers for food and sport. With the establishment of as food fish to other Asian countries has earned PhP 517 the species, there is a possibility of its spread to the rice million from January to June in 2013 for the country paddies and fishponds in the lower areas supplied by the (Chavez 2013; Lazaro 2013). irrigation system. The fish should therefore be studied and monitored to limit its invasive extent. The “jaquar guapote” in Lake Taal is becoming a fish of value because of its acceptable quality as a food fish. In an ACKNOWLEDGEMENT economic impact study conducted by Rosana et al. (2006), The author gratefully acknowledges the funding support it was found that 75% of survey respondents said that it of the National Academy of Science and Technology was a “beneficial fish” in terms of their catch. The fish is (Philippines) for the conduct of the study. sold at prices of PhP 20-30 for small ones and PhP 70-80

57 Philippine Journal of Science Guerrero III RD: Impacts of Introduced Freshwater Vol. 143 No. 1, June 2014 Fishes in the Philippines

REFERENCES [CBD] Convention on Biological Diversity. 2014. Invasive alien species (http://www.cbd.int/invasive/ ABELLO MM. 2013. Exotic knifefish leather. Manila What are IAS. shtml) Bulletin (September 21, 2013) p. B-8. DE SILVA SS. 1989. Exotic aquatic organisms in Asia. AGASEN, EV, CLEMENTE JP, ROSANA MR, KAWIT Asian Fisheries Society, Special Publication 3, 154 p. NS. 2006. Biologicial investigation of jaguar guapote Parachromis managuensis (Gunther, 1867) in ESCUDERO PET. 1993. Lake Lanao fisheries: problems Taal Lake, Southern Luzon. Paper presented in the and recommendations. Paper presented at the National Conference-Workshop on Alien Invasive Species in the Symposium-Workshop on Lake Fisheries Management, Philippines and their Impact on Biodiversity. Marikina Los Banos, Laguna: Philippine Council for Aquatic and Hotel, Marikina City, Philippines. 23 p. Department of Marine Research and Development. 9p. Fisheries and Oceans, Government of Canada. 53 p. [FAO] FOOD AND AGRICULTURE ORGANIZATION. ANON. 2013. Environment invaders on GMA’s Born 1995. Code of Conduct for Responsible Fisheries. Impact. Philippine Star (March 17, 2013) p. D-3 Rome: Food and Agriculture Organization of the United Nations. 41 p. ARTHUR JR, BONDAD-REANTASO MG, BALDOCK FC, RODGERS CJ, EDGERTON BF. 2004. Manual on [FAO] FOOD AND AGRICULTURE ORGANIZATION. risk analysis for the safe movement of aquatic animals 2014 DATABASE ON INVASIVE ALIEN SPECIES (FWG/01/2002). APEC/DOF/NACA/FAO, 59 p. (http://ww.fao.org/topic/14786/en) [BAS] BUREAU OF AGRICULTURAL STATISTICS. FOOD AND AGRICULTURE ORGANIZATION. 2014. 2013. Fisheries statistics of the Philippines 2008-2010. Fisheries and Aquaculture Topics. Introduction of Quezon City: Department of Agriculture. 402 p. species. Topics Fact Sheets. In: FAO Fisheries and Aquaculture Department [online] [Cited 1 May 2014] BRUTON MN & MERRON SV. 1985. Alien and (http//www.fao.org/fishery/topic.13532/en) translocated aquatic animals in Southern Africa: a general introduction checklist and bibliography. South FISH BASE. 2013. (www.fishbase.org, accessed Nov. African National Scientific Program Report. 113:1-71. 19, 2013) CASAL CMV, BARTLEY D. 2000. The introductions FULLER P, NICO L, WILLIAMS J. 1999. Non- table, p. 106-112 In: Froese R, Pauly D. eds. Food and indigenous fishes introduced into inland waters of Agriculture Organization FishBase 2000: concepts, the United States. Special Publication 27, Bethesda, design and data sources. ICLARM, Los Banos, Laguna, Maryland, USA: AFS. p 613. Philippines. 344 p. GLOBAL INVASIVE SPECIES PROGRAMME. 1999. CASAL CMV. 2005. Documenting the presence and (UNEP/CBD/SBSTTA/5/5/22 October 1999) impact of introduced freshwater fishes for aquaculture GUERRERO RD III, GUERRERO LA, GARCIA LL. in the Philippines, p. 145-154 In: Cuvin-Aralar ML, 1990. Use of indigenous plants as sources of fish Punongbayan RS, Santos-Borja A, Castillo LV, toxicants for pond management in the Philippines. Manalili EV, Mendoza MM. eds. Proceedings of Philippine Technology Journal XV (2):15-17. the First National Congress on Philippines Lakes. Southeast Asian Regional Center for Graduate Study GUERRERO RD. 1999. Impacts of tilapia introductions and Research in Agriculture; 5 June 1992. Los Banos, on the endemic fishes in some Philippine lakes and Laguna, Philippines: Convention on Biologcal reservoirs, p. 151-158, In: Van Densen WLT, Morris Diversity. 1992. Convention on Biological Diversity. MJ. eds. Fish and Fisheries of Lakes and Reservoirs 29 p. in Southeast Asia and Africa, UK: Westbury Academic & Scientific Publishing. p 432. CERVANTES D. 2013. War declared vs “Gloria fish”. Philippine Star (September 17, 2013) p. 5. GUERRERO RD III. 1981. Introduction to fish culture in the Philippines. Manila, Philippines: Philippine CHAVEZ HM, CASAO EA, VILLANUEVA EP, Education Co., Inc. 70 p. PARAS MP, GUINTO MC, MOSQUEDA MB. 2006. Heavy metal and microbial analysis of janitor fish GUERRERO RD III. 2013. Fishes that help prevent (Pterygoplichthys spp.) in Laguna de Bay, Philippines. dengue. Agriculture Monthly 17(10):24-25. J Environ Sci Management 9(2):31-40. HUBILLA M, KIS F, PRIMAVERA J. 2007. Janitor CHAVEZ CA. 2013. “Arroyo” fish bane to Hagonoy fish, Pterygoplichthys disjunctivus, in Agusan Marsh: fisherfolk. Manila Bulletin (September 4, 2013) p. 2. a threat to freshwater biodiversity. J Environ Sci Management 10(1): 10-23.

58 Philippine Journal of Science Guerrero III RD: Impacts of Introduced Freshwater Vol. 143 No. 1, June 2014 Fishes in the Philippines

[ICES] INTERNATIONAL COUNCIL FOR THE managuensis in Taal Lake, Philippines. J Environ Sci EXPLORATION OF THE SEA. 2003. ICES Code of Management 9(2): 1-19. Practice on the Introductions and Transfers of Marine STACHOWICZ JJ, TILMAN D. 2005. Species invasions Organisms 2003. ICES, Copenhagen, Denmark. 28p. and the relationships between species diversity, [IUCN] International Union for the Conservation of community saturation, and ecosystem functioning. Nature. 1999. Red list of categroes and criteria version In: Species invasions: insights into ecology, evolution . The World Conservatin Union. Gland, Switzerland and biogeography (DF Sax JJ Stachowicz, Gaines SD). and Cambridge, UK. 242 p. Sunderland, Massachusetts: Sinauer Associates. 480 p. JOSHI RC. 2006. Invasive alien species (IAS): VALENCIA C. 2013. Pesky rice eel now an export concerns and status in the Philippines (www.agnet. commodity. Philippine Star (August 11, 2013) p. B-3. org/.../20110826121346/Paper-729213301.pdf) VINCENTIN W, DOS SANTOS COSTA FE, SUAREZ JULIANO RO, GUERRERO III R & RONQUILLO YR. 2012. Population ecology of red-bellied piranha, I. 1989. The introduction of exotic aquatic species Pygocentrus nattereri Kner, 1858 (Characidae: in the Philippines, p. 83-90. In: De Silva, S.S. (ed.) Serralminae) in the Negro River, Pantanal, Brazil. Exotic aquatic organisms in Asia. (19-21 June 1981) Environmental Biology of Fishes, 96(1): 57-66. Proceedings of the Workshop on Introduction of Exotic Aquatic Organisms in Asia. Asian Fish. Soc. Spec. Publ. 3, 154 p. [LLDA] Laguna Lake Development Authority. 2005. Laguna de Bay Environmental Monitor: A Report to the Stakeholders of the Laguna de Bay Region. LLDA, Pasig City, Philippines. 34 p. LANTINI AO, PETRERE M. 2004. Reduction of a native fish fauna by alien species: an example from Brazilian freshwater tropical lakes. Fisheries Management and Ecology 11(2):71-79. LAZARO FG. 2013. Farm pest now exported food. Manila Bulletin (August 31, 2013) p. 9 MIRANDA-CHUMACERO G, WALLACE R, CALDERON H, SILES TM, LARA K, CHUQUI D. 2012. Distribution of araipama (Arapaima gigas) (Pisces: Arapaimatidae) In Bolivia: Implications in the control and management of a non-native population. Bioinvasions Records 1(2): 129-138. MOONEY H, CLELAND E. 2001. The evolutionary impact of invasive species. Proc Nat Acad Sci 98(10): 5446-5451. PELICICE FM, AGOSTINHO AA. 2008. Fish fauna distribution after the introduction of a non-native predator (Cichla kelberi) in a Neotropical Reservoir. Biological Invasions 11(8): 1789-1801. RABANAL HR. 2000. Aquaculutre in the Philippines (1898-1998), p. 70-115, In: Guerrero III RD. ed. 100 Years of Philippine Fisheries and Marine Science, Los Banos, Laguna: Philippine Council for Aquatic and Marine Research and Development. 210 p. ROSANA, MR, AGASEN EV, VILLANUEVA LS, CLEMENTE JP, JR., KAWIT NJ, DELA VEGA JJ. 2006. Status and economic impact of Parachromis

59