Golden Apple Snail Pomacea spp. in the Philippines1

A. G. Cagauana/ and R. C. Joshib/

a/ Freshwater Aquaculture Center, Central Luzon State University,
Science City of Muñoz, Nueva Ecija 3120, Philippines
E-mail: p-fishgn@mozcom.com

b/ Philippine Rice Research Institute, Maligaya,
Science City of Muñoz, Nueva Ecija 3119, Philippines
E-mail: joshiraviph@yahoo.com;joshiravi@hotmail.com

1 Presented at the 7th ICMAM Special Working Group on Golden Apple Snail, 22 October, 2002.

Introduction

The golden apple snail (GAS), Pomacea spp. is a freshwater gastropod native to South America. This snail had three routes of introduction into Philippines, namely: from Taiwan to Lemery, Batangas in 1982; from Florida, U.S.A. to Makati, Metro Manila in 1983; and from Argentina to Asturias, Cebu in 1984 (Mochida, 1987). Private entrepreneurs and government agencies introduced GAS (also referred to as Golden Kuhol) in the Philippines as a means of livelihood and to enrich the protein source in the human diet (Mochida, 1987; Madamba and Camaya, 1987; Rejesus et al. 1988). However, a few years after its introduction, GAS became an aquaculture species in confined environment. Eventually, GAS became feral when it escaped to creeks, rivers, streams, irrigation systems and rice fields. It is now considered a major pest in all rice ecosystems of the Philippines including UNESCO Ifugao Rice Terraces (Dancel and Joshi, 2000; Joshi et al, 2000; Joshi et al, 2001). Besides being a serious rice pest, GAS has been implicated in the drastic decline of edible native apple snail (NAS), Pila conica (Gray) [often erroneously quoted as Pila luzonica Reeve] in the Philippine rice fields and natural waterways (Acosta & Pullian, 1991; Halwart, 1994; Joshi, R. C. unpublished data & personal observations). GAS infestation poses several problems in rice farming systems. They damage young rice seedlings, causes poor crop stand, yield losses, additional expenses, and lethal effects of synthetic commercial molluscicides including the unaccounted environmental costs where bodies of water are the main recipients of the runoff of various formulations of nonspecific molluscicides (Dancel and Joshi, 2000). Filipino farmers became aware of GAS as pest of rice in 1986, when it was first reported damaging 300 ha of rice crops in Region 2 (Manila Bulletin, August 25, 1988). Six years after its introduction in the Philippines, GAS invaded about 3.6% of the total area planted to rice (Rejesus et al., 1988).

Reports on GAS were numerous from 1988 to 1990 and surprisingly declined after that year based from compilation of references found in Cariaso et al., (1993), Acosta and Pullin (1991) and Cagauan and Joshi (2001). The workshop on the “Management of Golden Snail in the Philippines” by the Rice IPM Network and supported by the Swiss Development Corporation was held at PhilRice, in 1991. This workshop report contains significant information such as GAS infestation levels in the different regions of the Philippines from 1987 to 1990, perceptions of rice farmers about GAS as a pest, and GAS management practices. Since then updated review on GAS in the Philippines does not exist. Our paper will attempt to review information from the past, more than a decade since the introduction of GAS in the Philippines, particularly new researches that evolved in the recent years, on level of infestation, food preferences, control methods and utilization of GAS.

How many Pomacea species are in the Philippines?

Records suggest that there are more than one species of Pomacea present in the Philippines (Table 1). GAS specimens from rice fields of Central Luzon State University (CLSU) sent to the Department of Malacology, Academy of Natural Sciences in Philadelphia, U. S. A. were identified as Pomacea insularis. Likewise, FAO and the Commonwealth Agricultural Bureau-International Institute of Biological Control (CAB-IIBC) identified the GAS as Pomacea insularis (Acosta and Pullin, 1991). Based on the morphological characteristics, GAS was identified as Pomacea canaliculata at the International Rice Research Institute (IRRI) (Saxena et al., 1987). According to Mochida (1987), P. canaliculata was introduced to Batangas from Taiwan in 1982. P. gigas from Florida were introduced to Makati Metro Manila in 1983. Another Pomacea species was directly introduced from Argentina to Cebu in 1984. Pila leopordivillensis, an African snail, was introduced from Taiwan. Pomacea cuprina is also found in the Philippines (Mochida, 1987). Most of the published reports refer GAS in the Philippines to as P. canaliculata.

Level of infestation

Most of the available information on the GAS infestation levels in the Philippines was until 1990. After six years of GAS introduction into the country, was its peak infestation. In 1988, surveillance efforts of different government agencies estimated its infestation in over 400,000 ha of rice farms (Rice IPM Network, PhilRice, 1991). After 1988, reports of area infested by GAS varied. In 1989 to 1990, PhilRice reported GAS infested rice farms per year were about 200,000 ha (Rice IPM Network, 1991). By 1999, it infested over 800,000 ha (Schnorbach, 1995). Estimated rice yield losses due to GAS infestation from 1985 to 1991 in the Philippines increased along with expanding infestation (Figure 1). In 1990, all thirteen regions of the Philippines reported GAS infestation (Rice IPM Network. 1991) and after that no additional new information on its infestation existed. The 1999 survey made by PhilRice indicated that about 35% of 71 provinces in various regions of the Philippines identified GAS as pest in rice farms (Provincial Rice Profiles, DA-PhilRice, 2000) but failed to provide data on GAS infested areas. Areas devoted to rice in the Philippines totals to 2,733,292 ha; 57% of which is irrigated, 37% rainfed and 6% upland (Figure 2).

There are claims that GAS infestation seemed to decrease because of control efforts involving the use of chemicals and other integrated management approaches. In addition, guidelines on the management of GAS and other rice pests are being taught to extension workers as well as farmers in relation to integrated pest management (IPM) program of the Department of Agriculture. There was an FAO-DA strategic extension campaign in 1990 for GAS in the Philippines (Adhikarya 1994; Escalada, 1991; Escalada and Heong, 1993). However, farmers still considered molluscicides like insecticides and herbicides---as one of the major agricultural inputs that they purchased (Tanzo et al 2000).

GAS infestation in the country brought about an increase in the use of molluscicides, thus, an increase in importation (Table 2). From 1984 to 1987, volume of molluscicides importation was less than 10 kg ha-1 and rose to 64 kg ha-1 in 1988 (FPA in Dancel and Joshi, 2000). In 1996, there was a remarkable increase of molluscicide importation to 130,000 kg ha-1 and almost doubled (241,683 kg ha-1 in 1997). Surprisingly, FPA record showed a remarkable decrease in 1998 to 67,340 kg ha-1, which is possibly attributed to the economic condition of the country during that year. The amount spent from 1980-1998 for molluscicides alone amounted to US$ 23 M. These statistics fails to partition how much molluscicide was used for the control of GAS, snails in brackishwater ponds, vector-snails against schistosomiasis and terrestrial snails.

Control Methods

Several control methods exists which are grouped as chemical, botanical, biological, cultural, mechanical, and manual. The PhilRice survey indicated that handpicking is widely practiced by farmers followed by chemicals and use of older seedlings (Rice IPM Network, 1991). Farmers observed that to control GAS, no single tactic was sufficient, but a combination of control methods was the best approach.

A.Agrochemicals

The quick knockdown effect of the pesticides on GAS that are directly hit makes this method popular among the farmers (Alba et al, 1993; Palis et al, 1993; DelaCruz et al, 2000; DelaCruz and Joshi, 2001). The efficacy of commercial molluscicides only lasted for 2-3 days against GAS, but unfortunately such compounds were more lethal to non-destructive native snail species, Vivipara costata (Quoy and Gaimard) (DelaCruz et al, 2000). The important side effect of increased pesticide usage is its negative impact on IPM strategy emphasizing use of cultural, biological, mechanical control measures and minimal use of pesticides. IPM is successfully being promoted in Asian rice production by the FAO Global IPM facility. Unfortunately farmers did not consider health or environmental effects in the choice of pesticides. Triphenyltin compounds (e.g. Brestan, Aquatin, Torque, Telustan) were the first group of pesticide used by farmers to kill GAS (Table 3). This practice stemmed from the use of the same compounds to kill the snail (Cerithide angulata) in milkfish ponds. Snail infestation greatly affects milkfish pond production because they compete with milkfish for algal food (Borlongan and Coloso, 1996). These compounds have been banned in September 1993 (FPA Board Resolution No. 1) (Lacierda et al., 2000) because of their adverse effects on human health (Adalla and Rejesus, 1989) and the environment (Acosta and Pullin, 1991). Endosulfan, an organochlorine, registered as insecticide and proven very effective to control GAS, is also banned by FPA. Table 3 shows other pesticides banned by the FPA.

Presently, there are four registered chemicals as molluscicide in the list of FPA, namely: niclosamide, metaldehyde, izazophos and copper hydrosulfate (Table 4). Farmers perceive that the most effective molluscicide available in the market today is niclosamide and metaldehyde. Niclosamide is effective against GAS but relatively non-toxic to humans (Amin, 1983). Niclosamide is also recommended by the Philippines’ Department of Health for schistosomiasis vector control (Palis et al., 1996). The effect of niclosamide on non-target organisms such as fish have been studied by Calumpang (1994) and Calumpang (et al., 1995) in relation to integrated rice-fish farming system. The researchers found that niclosamide at the rate of 0.250-0.0375 kg active ingredients (a.i.) ha-1 was toxic to carp causing 100% mortality at the time of application and 20-30% mortality in Nile tilapia. Residues of niclosamide in Nile tilapia (Oreochromis niloticus), ten pounder (Elops hawaiiensis) and goby (Amblygobius phalaena) were detected, but below the acceptable daily intake level of 3 mg kg-1 body weight. There were no residues found in milkfish (Chanos chanos) and tarpon (Megalops cyprinoides). Calumpang (1994) found that the niclosamide residue retention in fish depends on the method of processing. In cooked Nile tilapia, niclosamide residues amounted to 0.67 mg/kg and 0.60 mg/kg in the broth compared to 0.46 mg/kg in the uncooked fish. Washed fish had a remarkable decrease in niclosamide residues amounting to 0.46 mg/kg compared to 2.13 mg/kg in the unwashed fish. Recently, ovicidal properties of niclosamide to GAS eggs were discovered (Joshi et al 2002, in press).

Metaldehyde is relatively non-toxic to fish but effective against GAS and the brackishwater snail Cerithidea angulata. Borlongan and Coloso (1996) found that metaldehyde had no detrimental effect to milkfish. Metaldehyde is toxic on the GAS nervous system and possesses anaesthetic properties (Mills et al., 1989).
A number of alternative chemicals have been tested against GAS and most of them are insecticides and some are fungicides (Table 5). Farmers practice showed that whatever available insecticides they could have, they also tried against GAS. Cagauan et al. (1993) demonstrated that combination product (insecticides having two groups of a.i.) (e.g. monocrotophos+cypermethrin, chlorpyrifos+Cypermethrin, and chlorpyrifos+BPMC), were more toxic to GAS than those insecticides that had only one group of a.i. (e.g. BPMC, monocrotophos and cypermethrin except endosulfan) based on the 96-hr LC50 of formulated product (F.P.) (Table 6). Endosulfan was extremely toxic (<1 mg/l 96-hr LC50 of FP) similar to the metaldehyde molluscicide. Niclosamide was highly toxic to GAS, while the botanical tannin-glycoside-sterol was moderately toxic.

B. Botanicals

The only commercial botanical molluscicide registered for use against GAS by the FPA is tannin-glycoside-sterol-flavanoid (Protek?). Protek was developed from natural toxins with specific properties against Pomacea spp., low mammalian toxicity and high biodegradability because of low toxicity (Cyanamid Pro Green).

Table 7 lists 16 plants tested against GAS, of which some have been tested in different forms. Some of these plants were Azadirachta indica, Calotrophis gigantean, Citris mitis, Conyza balsamifera, Croton tiglium, Derris elliptica (philippinenses), Dioscorea hispida, Entada phaseoloides, Glericidia sepium, Jatropha curcas, Menispermum cocculus, Mikania cordata and Nicotiana tabacum. Botanical molluscicides are believed to be more environment-friendly compared to synthetic chemicals because they are easily biodegradable and leave no residues in the environment. Derris plant in the Philippines (Derris elliptica (philippinensis)) is a rich source of rotenone, which is effective against GAS but toxic to fishes. In the U.S., rotenone is one of two registered fish toxicant/piscicide under the Environmental Protection Agency (Federal Joint Subcommittee on Aqua. 1994). Derris plants in the Philippines have a potential botanical that can be explored as a source of rotenone for use against GAS.

C. Biological control

Biological predators of GAS are ducks, fish, birds, fire ants, spiders, rats, mites, snakes and other reptiles. Fire ant predation on GAS eggs was well quantified in field studies by Way et al (1998) and Yusa (2001). Recently Joshi et al (2001) reported long horned grasshopper as predator of golden apple snail eggmasses based on field and greenhouse evaluations. Predation by ducks and fishes are the most studied because they have economic values in the farming system aside and important roles in the environment. The use of ducks and fish as biological control agents against GAS should be viewed in the context of the total farming systems.

Ducks have been reported to control rice pests like weeds and insects (Furuno, 2000; Manda, 1992), GAS (Rosales and Sagun, 1997; Vega, 1991; Pantua et al., 1992; Cagauan et al., 2000) (Table 8). Ducks are effective biological control for GAS. Rosales and Sagun (1997) noted a decrease in the GAS abundance from 4.6 snails m-2 in the first year of cropping to 0.8-1.6 snails m-2 in the second year as a result of continuous duck herding in the rice fields after rice harvest. Using 900 ducks ha-1, Vega (1991) observed a 74-84% decrease of GAS in rice fields, hence, less rice missing hills. Pantua et al. (1992) observed also a significant GAS reduction consequently rice damage using 200 ducks ha-1.

In 1996, an FAO project at CLSU obtained a significant GAS density reduction from 8-17 snails m-2 before herding down to 1-2 snails m-2 after duck herding for a period of at least 30 days using 400 ducks ha-1 (Cagauan, 1999). Ducks were found to decrease the abundance of GAS with <4 cm shell height, the dominant size of GAS considered a threat to newly transplanted rice depending on its density. The duck herding employed before rice transplanting was a better control measure against GAS than the herding done for a period of 14-19 days at one month after rice transplanting. Duck control was more effective against the GAS than the chemical molluscicide. The molluscicide become ineffective either because of poor drainage in the plots or when GAS are still buried in the soil or GAS avoid exposure to molluscicide by simply crawling out of treated water on clay clumps or emergent vegetation (Van Dinther, 1973; DelaCruz and Joshi, 2001).

The adoption of ducks as biocontrol for GAS will depend on the availability of itinerant duck herders or on the farmers’ financial capability to own ducks (Cagauan, 1999). In the Philippines, it is common practice to herd ducks after rice harvest from one field to another depending on food availability but few farmers’ own ducks due to their high cost. Another reason for some farmers’ rejection of this practice is because it causes itchiness to farm workers.

Fish has been suggested as biological control for snails (Morallo-Rejesus et al., 1990; Rondon and Sumangil, 1991) but very little quantified research exists (Slootweg et al., 1993; Slootweg et al., 1994; Halwart, 1994; Nguyen Quang Dieu et al., 1998; Cagauan, 1999). Several laboratory and field researchers on the use of freshwater fishes with edible and economic value to control snail are found in Table 9. Very few researches exist on the assessment of fish on GAS in the Philippines such as in ricefields (Halwart, 1994; Cagauan, 1999) and in plots with rice in screenhouse (Cagauan and Joshi, 2002) and in Vietnam (Nguyen Quang Dieu et al., 1998). Some of the potential fish predators found in the Philippines are common carp Cyprinus carpio and red-bellied pacu Piaractus brachypomus. Commonly, carp is widely distributed in Asia and it is one of the recommended fish species for culture in integrated rice-fish culture. Red-bellied pacu is presently an aquarium fish species but it is a food fish in South America where it is indigenous. Cagauan and Joshi (2002) found both fishes (Table 10) to predate on GAS but it depends on their mouth size, as a function of body size, that is suitable to the size of GAS. However, large sized of pacu (42-49 g) and densities 2-3 fish m-2 caused damage (i.e. 2-3 hills plot-1) to 20-day old rice plants from transplanting. The damage caused by this fish mimics that of the damage caused by rats. Pacu with size: <10 g with densities 1-3 fish m-2 did not damage the rice plants. Asian catfish Clarias macrocephalus was not found to predate on GAS.

The effectivity of fish as biological control of GAS would depend on their feeding habit, size, density, culture system and duration of culture. A developed pharyngeal jaw apparatus have the capability to crush the shells of GAS. For short culture period such as in rice-fish culture with high yielding rice varieties, initial fish size and density are important in order to have an impact on GAS (Cagauan, 1999). Cagauan suggested that a polyculture system of fish species with different feeding habits may be better than the monoculture system in terms of GAS control because such system can put some pressures on the food availability of GAS. Vietnamese observed that there is a significant reduction of GAS in integrated rice-fish farms employed primarily with polyculture of common carp, black carp and catfish (FAO, 1998).

Caution must be taken on the use of fish, which are not native to one’s country in order to avoid threat to indigenous species. In the U.S., black carp, a molluscivorous fish, was introduced as a biological control for the parasite in trout. However, it was found later on that native populations of freshwater molluscs were diminishing due to the black carp. Presently, black carp is banned in the U.S.

D. Cultural and Manual

Some of the cultural methods employed by farmers are the use of metal screens, older seedlings, using higher seedling density per area, handpicking and intermittent draining of fields. Hand picking is the most widely practiced method followed by chemicals and the use of older seedlings (Rice IPM Network, 1991).

Providing alternative feeds for the GAS and at the same time to serve as attractant such as leaves of papaya, kangkong, sweet potato, cassava, taro and other succulent plants during the first five days after transplanting can reduce damage to rice seedlings by 75% (Guzman and Enriquez, 1991). However, this measure does not reduce the GAS population unless they are collected and destroyed. Joshi and DelaCruz (2001) identified newspaper as a new attractant for GAS management. It can be used in rice fields prior to crop establishment (direct seeding / transplanted) to attract GAS and thus facilitate easy and rapid GAS collection manually.

Plant preferences of GAS can be explored as an alternative feed or plant attractant to divert away the GAS from feeding the rice seedlings or these plants may be used to collect the snails to facilitate hand picking. Basilio and Litsinger (1988) found 9 plants that are preferred by GAS (Table 11). Azolla filiculoides was the most preferred by GAS compared with other species, possibly due to the adaptation of GAS to that particular azolla species before the test (Cagauan and Van Hove. 1995). DelaCruz et al (2002) found that GAS has preferences for different rice varieties. They found more damage in IR64 and PSBRc82 than other varieties like PSBRc40, PSBRc36, PSBRc38, and PSBRc68.

E. Integrated control

Farmers observed that to control the GAS, no single tactic is superior that a combination of control methods is the best approach. Overall, the existing control measures such as the use of chemicals, handpicking, ducks, draining and screens were considered by farmers as effective, although each control has some constraints (Rice IPM Network, 1991). Figure 3 shows an integrated management scheme for the GAS pooled from different farmers practices and strategies and expert advice and the management options to undertake a different stages of the rice crop.

Utilization of GAS

GAS can be used as human food and animal feed. As feed, it could possibly replace meat meal or fishmeal in animal diet. The nutrient composition of GAS in different forms: meal (cooked), meat (uncooked), meat meal and shell meal is shown in Table 12. The protein content of 62.5% is comparable to the CP value of Peruvian fish meal (61.2%) but a little bit lower than and the meat meal (66%) (Gerpacio and Castillo, 1979). GAS is also a good source of mineral as indicated by the contents of calcium (35%) and phosphorous (1.22%) and high source of energy (3,336 kcal kg-1). We have compiled results of feeding trials using GAS in its different forms (Table 13). Uncooked but fresh GAS meal in swine diets can be used up to 15% (Catalma et al., 1991) while up to 10% in the diet of native chicks (Catalma et al., 1991).

GAS in ricefields is good food for mallard ducks. Actually, it is a common practice by duck farmers to herd their flocks in the fields after rice harvest, in this way they can economize on feeds. Duck herding and with little feed supplementation during confinement can yield up to 60-70% egg production (Tacio, 1987). In integrated rice-fish-duck-azolla farming system, duck laying percentage was at an average of 60% (Cagauan, 2000). Ducks in the system were herded in the ricefield after rice harvest where they ate GAS, fallen rice grains, insects and azolla. During confinement just after the rice booting stage, ducks were fed with commercial duck layer pellet.

Feeding trials on Nile tilapia in aquaria showed that GAS meat meal at 75-100% of the diet mixed with rice bran is beneficial (Cagauan and Doria, 1989). In cage culture of Nile tilapia, fish grown in snail-meal based diet was superior to that obtained with fish fed with fishmeal based diet (Reazo, 1988). For freshwater prawn (Macrobrachium rosenbergii) larvae, 60% GAS meat meal in dried form mixed with rice bran, shrimp meal and fish meal gave good growth (Lansangan, et al., 2002).

As food for humans, GAS can be cooked with coconut milk, pickled as an appetizer, and made into “kropeck”. One of the major obstacles to their popularization is their short shelf life. PhilRice researchers in partnership with a rice farmer developed a new recipe chicharon (cracker) from GAS. This recipe is unique compared with other GAS recipes, in that it is devoid of water, has no offensive odor, with longer shelf life, and can be readily used as ingredient in other recipes (DelaCruz and Joshi, 2001). The Department of Agriculture-Cordillera Administrative Region (DA-CAR) is currently promoted this recipe in the FFS and farmers’ field days in the highlands of Cordilleras. In a related activity, a PCARRD study at CLSU showed that endosulfan (an organochlorine insecticide) could accumulate in the tissues of GAS and may get biomagnified when taken by humans (PCARRD Monitor, 2000). This insecticide has been banned for use in the rice fields of the Philippines for several years now.

Future Research Directions on GAS Research and Extension

Molecular mapping should be done to clarify the Pomacea species complex. This should be the first step before conducting detailed ecological and management studies on GAS.

The Department of Agriculture and related agencies should develop easily accessible information database and map out the distribution of Pomacea spp. complex, their infestation levels as well as other rice pests in the country at the regional, provincial and village levels.

Search for chemical rice seed coating should be explored to identify chemicals that will either inhibit/repel/or change the behavior of GAS in direct-seeded rice culture. The aim of this strategy is not to kill the GAS directly but to reduce GAS feeding to newly sprouted rice.

In case of hybrid rice planted as transplanted culture, GAS management should encourage GAS to feed on weeds rather than rice plants. This can be done by manipulation of certain cultural practices.

More basic research is needed in the following areas:
- Identify biopesticides (botanicals) that may have ovicidal action on GAS eggmasses.
- Basic population ecology of GAS and the NAS.
- Continue the search and evaluation of potential biocontrol agents against GAS.

Farmers and extension workers in the Philippines need to be exposed to new information sources on GAS management. This is of paramount importance as the proportion of wet-rice area infested with GAS is increasing (DA-FAO, 1989), and GAS continues to threaten the promotion of hybrid rice and direct-seeded rice cultures. Therefore there is a need to develop environment-friendly GAS management options for the above two rice cultures since all of the management strategies utilized in transplanted rice are not suitable for hybrid and direct-seeded rice systems.

References

• Acosta, B. O. and R. S. V. Pullin (eds.).1991. Environmental Impact of the Golden Snail (Pomacea sp.) on Rice Farming Systems in the Philippines: Summary Report of the Workshop held at the Freshwater Aquaculture Center, Central Luzon State University, Muñoz, Nueva Ecija, Philippines, 9-10 November 1989, ICLARM Conf. Proc. 28, Manila, Philippines. 34 pp.
• Adhikarya, R. 1994. Strategic extension campaign: A participatory-oriented method of agriculture extension. Rome: Food and Agriculture Organization of the United Nations.
• Agaceta, L. M., P. U. Dumag, J. A. Batolos, N. B. Ascandor and F. C. Bandiola. 1981. Study on the control of vectors of Fascioliasis; molluscicidal activity of some indigenous plants. Philipp. J. Anim. Indus. 36 (1-4):101-111.
• Agarrado, M. T. S. 2000. Beware of golden snails in rice fields. PCARRD Monitor 28(1):10.
• Alba, M. C. E. Vertosio, F. V. Palis and R. F. Macatula. 1993. The effect of botanical and chemical pesticides against golden apple snail (Pomacea sp.) in rice. 24. Pest. Mgt. Council of the Philippines, Cebu City, Philippines. 4-7 May 1993.
• Amin, A. 1983. Control of snail intermediate hosts of schistomiasis. p. 318 - 326. In: A. Youdeowei and M. W. Service (eds.). Pests and vector management in the tropics with particular reference to insects, ticks, mites and snails. Longman Group Ltd. 398 pp.
• Ancheta, D. A. 1990. Preliminary study on crushed fresh golden snail (Pomacea spp.) as feed supplement for laying hens. Undergraduate Thesis. Central Luzon State University, Philippines. (unpublished)
• Anonymous. 1998. Fishfarming in Vietnamese rice fields fights golden apple snail pest. Food and Agriculture Organization of the United Nations. Available: http://www.fao.org.news. 12 November 1998.
• Aquino. R. R. 1990. Golden snail, a major pest in the Philippines is potential feed for laying ducks. In: Proc. of the 5th Asian-Australasian Asso. of Animal Prodn. Soc. Meeting. Taipei, Taiwan.
• Banoc, L. M. and L. M. Noriel. 1991. Utilization of weed extracts for the control of golden snail (Pomacea canaliculata Lamarck). Philipp. J. Weed Sci. 18:90-99.
• Barcelo, P. M. and J. R. Barcelo. 1991. The potential of snail (Pila leopoldvillensis) meal as protein supplement in broiler diet. Tropicultura, 9:11-13.
• Berges, J. M. C. A. Baniqued and R. C. Perez. 1991. Extracted nami (Diocorea hispida Dennst) against golden kuhol (Pomacea canaliculata Lamarck). In-House Annual Review, Mla., Philippines. May 16-17, 1991. 19 p.
• Berjes, J. M., C. A. Baniqued and R. C. Perez. 1991. Extracted neem (Dioscorea hispida Dennst) against golden kuhol (Pomacea canaliculata Lam.). Paper presented at the In-House Annual Review, May 16-17, 1991, Bureau of Plant Industry, San Andres, Malate, Manila, Philippines. 19 pp. (unpublished)
• Borlongan, I. G. and R. M. Coloso. 1996. Use of metaldehyde as molluscicide in milkfish ponds. p. 205-212. In: I. Henderson (ed.). BCPC Sympo. Proc. No. 66: Slugs and Snail Pests in Agriculture. Proc. of a Sympo. held at the University of Kent, Canterbury, U.K., 24–26 September 1996. British Crop Protection Council. 450 pp.
• Cagauan, A. G. 1995. Studies on the aquatic gastropod (Pomacea canaliculata) and the aquatic fern azolla. Report of research experiment. Laboratory of Plant Biology, Catholic University of Louvain, Louvain-la-Neuve, Belgium. 42 pp. (with French abstract). (unpublished)
• Cagauan, A. G. and L. S. Doria. 1989. “Golden” snail Pomacea insularis (?) canaliculata (?) meal as feed for Nile tilapia Oreochromis niloticus fingerlings in aquaria. CLSU Scientific Journal. 9(3):24-29.
• Cagauan, A. G. 1999. Golden apple snail control. Chapter 5. p. 185-219. In: Production, economics and ecological effects of Nile tilapia (Oreochromis niloticus L.), a hybrid aquatic fern azolla (Azolla microphylla Kaulf. x A. filiculoides Lam.) and mallard duck (Anas platyrhynchos L.) in integrated lowland irrigated rice-based farming systems in the Philippines. Ph.D dissertation. Institut des Sciences Naturelles Appliquees, Université Catholique de Louvain. Louvain-la-Neuve, Belgium. 404 pp.
• Cagauan, A. G. and R. C. Joshi. 2002. Predatory effect of freshwater fishes on golden apple snail Pomacea canaliculata Lam. in screenhouse conditions. Intl. Rice Res. Notes. International Rice Research Institute, Los Baños, Laguna, Philippines. (in press)
• Cagauan, A. G. C. Van Hove and R. D. Branckaert. 2000. Integrating fish and azolla in rice-duck farming in Asia. Naga, The ICLARM Quarterly 23(1):4-10.
• Cagauan, A. G., C. Van Hove, E. Orden, N. Ramilo and R. D. Branckaert. 1996. Preliminary results of a case study on integrated rice-fish-azolla-ducks farming system in the Philippines. p. 35-61. In: H. Hayakawa, M. Sasaki and K. Kimura (editors). Integrated Systems of Animal Production in the Asian Region. Proc. of a Sympo. held in conjunction with the 8th AAAP Animal Science Congress, Chiba, Japan, 13-18 October 1996. Food and Agriculture Organization (FAO). 111 pp.
• Cagauan, A. G., E. C. Ferrer and W. Muangman. 1993. Acute toxicities of insecticides with single and two groups of active ingredients and molluscicides on golden snails (Pomacea sp.). p. 47-50. In: Final Report: Rice-Fish Ecology (July 1992-December 1993). Prepared by Arsenia G.
• Cagauan. Freshwater Aquaculture Center, Central Luzon State University, Nueva Ecija, Philippines. 50 pp.
• Cagauan, A. G. R. C. Joshi and M. S. dela Cruz. 2001. Bibliography on golden apple snail Pomacea spp. Crop Protection Division, Department of Agriculture, Philippine Rice Research Institute, Maligaya, Muñoz, Nueva Ecija, Philippines.
• Calumpang, S. M. F. 1994. Fate of niclosamide in various components of a fish and prawn pond ecosystem. Philippine Agriculturist. 77(3):393-401.
• Calumpang, S. M. F., M. J. B. Medina, A. W. Tejada and J. R. Medina. 1995. Environmental impact of two molluscicides: niclosamide and metaldehyde in a rice paddy ecosystem. Bulletin of Environmental Contamination and Toxicology. 55:494-501.
• Cariaso, M. R., A. V. De Lara, B. F. Cayabyab and M. D. Ebuenga (eds.). 1993. Abstract Bibliography on Apple Snail. National Crop Protection Center, College of Agriculture, University of the Philippines, Los Baños, Laguna, Philippines. 93 pp.
• Catalma, M. T., A. B. Serra, E. A. Orden, A. S. de Guia, E. A. Martin, M. S. Laureta, E. J. Rafael, R. A. Antalan and A. J. Barroga. 1991. Feeding value of golden snail (Pomacea sp.) meal for poultry and swine. In Proc. of the 28th Phil. So. Of Animal Sc. Annual Meeting, manila. p. 33-34.
• Catalma, M. T., D. T. Capili, R. A. Antalan, A. B. Serra, A. J. Barroga and E. Orden. 1991. Golden snail (Pomacea sp.) use in animal feeds. Int. Rice Res. Newsletter. 16(6):26-27.
• Cruz-Lacierda, E. R., L. D. dela Peña and S. C. Lumanlan-Mayo. 2000. Use of chemicals in aquaculture in Asia. P. 155-184. In: J. A. Arthur, C.R. Lavilla-Pitogo and R. P. Subasinghe (eds.). Proc. of the Meeting on the Use of Chemicals in Aquaculture in Asia, 20-22 May 1996, Tigbauan, Iloilo, Philippines. SEAFDEC. 235 pp.
• Dancel, K. T. and R. C. Joshi. 2000. “Golden” menace in Ifugao rice terraces. SEAFDEC Asian Aquaculture. 22(1):11-12, 31-33.
• Darby, P. C., P. L. Valentine-Darby, R. E. Bennetts, J. D. Croop, H. F. Percival and W. M. Kitchens. 1998. Ecological studies of apple snails. Florida Cooperative Fish and Wildlife Research Unit, University of Florida. Special Publication SJ98-SP6. Available:http://www.Flo.apple.snail. 12 November 1998.
• Datuin, J. M., J. T. Aquino and R. A. Tucay and R. C. Cayabyab. 1990. Utilization of golden kuhol on the egg production performance of mallard duck. Phil. J. Vet Anim. Sci. 17:65. (abstract)
• DelaCruz M. S., R. C. Joshi and E. C. Martin. 2000. Potential effects of commercial molluscicides used in controlling golden apple snails on the native snail, Vivipara costata (Quoy and Gaimard). Philippine Entomologist. 14(2):149-157.
• DelaCruz, M. S. and R. C. Joshi. 2001. Efficacy of commercial molluscicide formulations against golden apple snail Pomacea canaliculata (Lamarck). The Philippine Agricultural Scientist, 84 (1): 51-55.
• DelaCruz, M. S. and R. C. Joshi. 2001. New recipe: golden kuhol chicharon. SEAFDEC Asian Aquaculture, 22 (4): 12.
• DelaCruz, M. S., R. C. Joshi. and A. R. Martin. 2000. Basal application of fertilizer reduces golden apple snail population. International Rice Research Newsletter, 26 (1); 20-21.
• Department of Agriculture-Bureau of Agricultural Research (DA-BAR). 1996. New weapon against golden apple snail found. Farming Update. 8(2):3-4.
• Department of Agriculture-Philippine Rice Research Institute (DA-PhilRice). 2000. Provincial Rice Profiles. DA-PhilRice Socioeconomics Division. Philippines.
• Dupo, H. C., S. P. Ferido and H. Sambuichi. 1989. Control of snail damage on rice with demotrin (cartap hydrochloride). p. 16. In: Acosta, B. O. and R. S. V. Pullin (eds.).1991. Environmental Impact of the Golden Snail (Pomacea sp.) on Rice Farming Systems in the Philippines: Summary Report of the Workshop held at the Freshwater Aquaculture Center, Central Luzon State University, Muñoz, Nueva Ecija, Philippines, 9-10 November 1989, ICLARM Conf. Proc. 28, Manila, Philippines. 34 pp.
• Edar, E., R. Yabuki, K. Takayama, Y. Nakanishi, M. Manda, S. Watanabe, S, Matsumoto and A. Nakagama. 1996. Comparative studies on behavior, weeding and pest control of ducks (mallard, cherry valley and their crossbred) free-ranged in paddy fields. Japanese Poultry Science. Vol. 33. No. 4. 261-267.
• Escalada, M. M. 1991. Strategic extension Campaign on golden snail control. pp. 17-18. In: B. O. Acosta and R. S. V. Pullin (eds.) Environmental Impact of the golden apple snail (Pomacea sp.) on rice farming systems in the Philippines, ICLARM, Manila, Philippines.
• Escalada, M. M. and K. L. Heong. 1993. Communication and implementation of change in crop protection. pp.191-207. In: Chadwick, D. J. and J. Marsh (ed.) Crop Protection and Sustainable Agriculture. CIBA Foundation Symposium 177. Chichester: J. Wiley & Sons.
• Furuno, T. 1996. Significance and practice of integrated rice cultivation and duck farming - sustainable agriculture. Kyushu International Center, Japan International Cooperation Agency and Kitakyushu Forum on Asian Women. 12 pp.
• Gerpacio, A. L. and L. S. Castillo. 1979. Nutrient composition of some Philippine feedstuffs. University of the Philippines at Los Baños Tech. Bull. No. 21.
• Guzman, E. D. and F. B. Enriquez. 1991. Non-chemical strategies to reduce golden snail damage to rice. Paper presented at the Workshop on “Environmental Impact of the Golden Snail (Pomacea sp.) on Rice Farming Systems in the Philippines” held at the Freshwater Aquaculture Center, Central Luzon State University, Philippines on 9-10 November 1989 sponsored by the International Center for Living Aquatic Resources Management (ICLARM), Makati, Philippines. 15 pp.
• Halwart, M. 1994. Fish as biocontrol agents in rice. Tropical Agroecology 8. Margraf Verlag. Germany. 169 pp.
• Joshi, R. C. and M. S. DelaCruz. 2001. Newspaper: a new attractant for golden apple snail management. International Rice Research Newsletter, 26 (2): 49-50.
• Joshi, R. C., M. S. DelaCruz and A. V. Duca. 2001. Long-horned grasshopper: a predator of golden apple snail eggmasses in the Philippines. International Rice Research Newsletter, 26 (2): 83.
• Joshi, R. C., M. S. DelaCruz, A. R. Martin, J. C. Cabigat, R. F. Bahatan, A. D. Bahatan, J. Choy-awon, N. P. Chilagan, and A. B. Cayong. 2001. Current status of the golden apple snail, Pomacea canaliculata in the Ifugao rice terraces. Journal of Sustainable Agriculture, USA. 18 (2/3): 71-90.
• June, L., L. Ulep and M. M. Buenafe. 1991. Performance of broilers fed with snail (Pomacea canaliculata) meal as substitute to fish meal or meat and bone meal. Tropicultura. 9:58-60.
• Lansangan, V. A., A. G. Cagauan and M. Tayamen. 2002. Golden apple snail Pomacea canaliculata Lam. As feed for freshwater prawn Macrobrachium rosenbergii de Man. Poster paper 7th ICMAM, Los Baños, Laguna. Philippines.
• Lobo, P.P.G., M. A. Llgas and F. D. Laysa. 1992. Evaluation of starflower Calotropis gicantea) against golden aplle snail (Pomacea canaliculata) in lowland transplanted rice. Trans. Nat. Acad. Sci. Technol. 14:477-489.
• Madamba C. P. and E. Camaya. 1987. The golden apple snail: boon and bane? In. Proc. 18th Anniv. And Ann. Conv., Davao City, Philippines.
• Maini, P. M. and B. M. Rejesus. 1993. Antifeedant activity of the crude and formulated product of Azadirachta indica to golden snail (Pomacea spp.). 24 Pest Mgt. Council of the Philipp., Cebu Cit, Philipp. 4-7 May 1993.
• Maini, P. N. and B. Morallo-Rejesus. 1993. Molluscicidal activity of Derris elliptica (Fam. Leguminosae). Philippine Journal of Science. 122(1):61-69.
• Manda, M., H. Uchida, A. Nakagama, S. Matsumoto, K. Shimoshikiryo and S. Watanabe. 1993. Effects of aigamo ducks (crossbred of wild and domestic ducks) herding on weeding and pest control in the paddy fields. Japan Poultry Science. 30:365 - 370. (Japanese with English abstract)
• Mills, J. D., S. E. R. Bailey and C. R. McCrohan. 1989. Effects of molluscicides on feeding behavior and neuronal activity. BCPC Mono. 41. Slugs and Snails in World Agriculture. 77-83.
• Mochida, O. 1987. Pomacea snails in the Philippines. International Rice Research Newsletter. 12 (4):48-49.
• Nguyen Quang Dieu, Nguyen Due Hoi, Nguyen Puong Pung, Le Thi Hung and Do Thi Quyet.1998. Results of the use of fish on golden apple snail control in Nghe An, Can Tho and Quang Binh, Vietnam. Fish breeding, rearing and stocking programme. Paper presented at the International Workshop on the Integrated Management of the Golden Apple Snail in Rice Production in Vietnam, 4-6 August 1998, Nghe An Province, Vietnam sponsored by the Plant Protection Department (PPD), Ministry of Agriculture and Rural Development (MARD) in cooperation with the Food and Agriculture Organization of the United Nations. 15 pp. (unpublished)
• Noriel, L. M., J. Margraf and F. M. Y. Duatin and M. P. Guzman. 2000. Botanical control of golden kuhol (Pomacea canaliculata Lamarck) using asyang (Mikania cordata) (Bum. F.) B-L. Robinson). Annals of Tropical Research. 22(142):41-51.
• Pablico, P. P. and K. Moody. 1988. Effect of fentin acetate on wet-seeded rice, Pistia stratiotes and Azolla pinnata. 19. Pest Control Council of the Philippines. Cebu City, Philippines. 3-7 May 1988. 2 pp.
• Pantua, P. C., S. V. Mercado, F. O. Lanting, and E. B. Nuevo. 1992. Use of ducks to control golden apple snail Ampullarius (Pomacea) canaliculata in irrigated rice. International Rice Research Newsletter, 17, 27.
  PhilRice (2001). Management Options for the Golden Apple Snail. Rice Technology Bulletin No. 33, Philippine Rice Research Institute, Maligaya, Science City of Muñoz, Philippines: 12pp.
• Rejesus, B. M. and P. N. Maini. 1991. Sapogenic plant materials for golden apple snail (Pomacea spp.) control. PhilRice Terminal Report. Jan. 1990 – Dec. 1991). 47 pp.
• Rejesus, B. M., A. S. Sayaboc, and R. C. Joshi 1988. The distribution and control of the introduced golden snail (Pomacea spp.) in the Philippines. Proceedings of the Symposium on Introduction of Germplasm and Plant Quarantine Procedures, Kuala Lumpur (Malaysia), 14-15 December, 1988. pp. 213-223.
• Rice Integrated Pest Management (IPM) Network. 1991. Report of a Workshop on the Management of Golden Snail in the Philippines. Philippine Rice Research Institute (PhilRice), Nueva Ecija, . 74 pp.
• Rodriguez, C. D. and O. J. Lorenzana. 1989. Evaluation of molluscicides for the control of golden snail Pomacea canaliculata). Workshop on Rice Farming System in the Philippines, Muñoz, Nueva Ecija, Philippines, 9-10 November 1989. 11 p.
  Rondon, M. B. 1989. Field testing of copper sulfate against golden kuhol. A Report of research conducted by the National Integrated Pest Management Secretariat, Bureau of Plant Industry, Department of Agriculture, Philippines. 4 pp. (unpublished)
• Rondon, M. B., C. A. Baniqued and M. S. dela Cruz. 1992. Filed evaluation of alternative pesticides against golden snail Pomacea canaliculata Lamarck in lowland rice. In: Report of the Workshop on the Integ. Pest Mgt. Network Prog. Rep., Los Baños, Laguna. August 1991-August 1992. p. 73-82.
• Rosales, N. M. and C.M. Sagun. 1997. Rice-rice cropping pattern using a combination of inorganic fertilizer and Azolla+ducks. Paper presented at the in-house review of on-going projects sponsored by the Bureau of Agricultural Research, Quezon City, Philippines. 13 pp.
  Saxena, R. C., A. V. de Lara and H. D. Justo. 1987. Golden apple snail: a pest of rice. Int. Rice Res. Newsl. 12 (1):24-25.
• Schnorbach, H. –J. 1995. The golden apple snail (Pomacea canaliculata Lamarck), an increasingly important pest in rice, and methods of control with Bayluscid?. Pflanzenschutz-Nachrichten Bayer. 48(2):313-346.
• Serrano, R. C. 1988. Besting the golden apple snail. Philippine Council for Agriculture and Resource Research and Development Monitor. 16(5): 6, 11.
• Slootweg, R., E. A. Malek and F. S. McCullough. 1994. The biological control of snail intermediate hosts of schistosomiasis by fish. Review in Fish Biology and Fisheries. 4:67-90.
• Slootweg, R., P. A. Vroeg and S. J. Wierma. 1993. Effects of molluscivorous fish, water quality and pond management on the development of schistosomiasis vector snails in aquaculture ponds. Aquaculture and Fisheries Management. 24:123-128.
• Tacio, H. D. 1987. Raise snails for your ducks. Agribusiness Weekly, Philippines. 6-12 November. p. 16-17.
• Tanzo, I. R., R. C. Joshi and G. H. Baker. 2000. Farmers’ assessment of the golden apple snail Pomacea canaliculata (Lamarck) (Mollusca: Ampullariidae) management options promoted in the strategic extension campaign in the Philippines: lessons learnt and future implications. Poster presented at the Molluscs 2000 Conf., 4-8 December, Sydney, Australia. 49.
• Van Dinther, J. B. M. 1973. Molluscs in Agriculture and their Control. World Crops 11/12: 282-286.
• Vega, R. S. A. 1991. Agro-economic evaluation of non-chemical methods against golden snail (Pomacea canaliculata Lam.) in irrigated lowland rice. Univ. of the Philippines at Los Banos, Philippines. Master Thesis in Agronomy. 65 pp.
• Way, M. J., Z. Islam, K. L. Heong and R. C. Joshi. 1998. Ants in tropical irrigated rice: distribution and abundance especially of Solenopsis geminata (Hymenoptera: Formicidae). Bulletin of Entomological Research 88: 467-476.
• Yusa, Y. 2001. Predation of eggs of the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae) by the fire ant Solenopsis geminata. J. Moll. Stud. 67: 275-279.

http://www.applesnail.net