A REVIEW OF THE FOUR IMPORTANT ALIEN INVASIVE SPECIES

ON RICE AND MANGO IN THE PHILIPPINES

Josie Lynn A. Catindig and Kong Luen Heong

Entomology and Plant Pathology Division, International Rice Research Institute

DAPO Box 7777 Metro Manila, The Philippines ()

Summary

Four alien invasive pests of economic importance to the rice and mango are described. These are the golden apple snail (GAS), Pomacea canaliculata (Lamarck) (Mesogastropoda: Ampullariidae), the rice black bug (RBB), Scotinophara coarctata (Fabricius) (Hemiptera:Pentatomidae), the mango pulp weevil (MPW), Sternochetus frigidus (Fabricius) and the mango seed weevil (MSW), S. mangiferae (Fabricius) (Coleoptera:Curculionidae). Their ecology, distribution and management options are presented in this paper.

Introduction

According to the Convention on Biological Diversity (CBD), “Invasive alien species are species introduced deliberately or unintentionally outside their natural habitats where they have the ability to establish themselves, invade, outcompete natives and take over the new environments”. They are widespread in the world and are found in all categories of living organisms and all types of ecosystems. However, plants, mammals and insects comprise the most common types of invasive alien species in terrestrial environments (

In the Philippines, four of the most important alien invasive pests are the golden apple snail, locally known as golden kuhol (Pomacea canaliculata (Lamarck)), the rice black bug, locally known as “itim na atangya” (Scotinophara coarctata (Fabricius)), the mango pulp weevil (Sternochetus frigidus (Fabricius)) and the mango seed weevil (S. mangiferae (Fabricius)).

The golden apple snail and the rice black bug feed on rice. Rice, the food crop for more than half the world’s population is the staple food in the Philippines. Of the 4 million hectares of total rice area, the average rice yield in the Philippines as of 2000 was 3.1 metric tons (MT) per hectare (IRRI, 2002).

The mango pulp weevil, Sternochetus frigidus (Fabricius) and the mango seed weevil, S. mangiferae (Fabricius) attacked mango fruits of cultivated and wild species in some parts of Asia like the Philippines (Gabriel, 1977; De Jesus, et al., 2004).Mango is the national fruit in the Philippines and is the third most important fruit crop of the country based on export volume and value next to banana and pineapple. Mango export in the country reached to 35,771 MT in 2003 ($31.011 million) with country’s production of close to one million metric tons (

Golden Apple Snail, Pomacea canaliculata (Lamarck)

Lamarck first described the golden apple snail or GAS in 1822 from rivers at Guadeloupe in South America (De Souza Lopes, 1956). However, it was thought that the snail originated from the catchement area of the Paraguay and ParanáRivers and drain into the Atlantic in Argentina (Pain, 1960). Because of aquarium trade, it was introduced in Asia, specifically in Taiwan from Argentina in 1979 as human food to be cultured indoors (Mochida, 1991). From Taiwan, it spread to Japan in 1981 and to the Philippines in 1983 (Santos, 1987) to boost food production and increase the protein intake of average Filipino families. The Philippine government encouraged its production and sponsored a livelihood project in 1984-85 by distributing the snail to all main islands to be raised in soil pits as a backyard cottage industry and promoting it as a national livelihood program (Adalla & Morallo-Rejesus, 1989; Morallo-Rejesus et al., 1990). The urban enterpreneurs were among the first raisers who were interested in generating additional income.

The snail eventually escaped from backyards and by 1985, GAS was all over the Philippines and found its way to agroecosystem and started to alarm the rice farmers. Farmers consider the golden apple snail to be the most serious pest in the Philippines in 1986 (Morallo-Rejesus et al., 1990). Further, it is said that the population of the native apple snail, Pila luzonica, has declined drastically since the introduction of the golden apple snail.

Distribution. Aside from the Philippines, GAS is found in Argentina, Bolivia, Brazil, California, Cambodia, China, Dominican Republic, Florida, Guam, Hawaii, Indonesia, Japan, Korea, Laos, Malaysia, Papua New Guinea, Paraguay, Singapore, Suriname, Taiwan, Texas, Thailand, USA, and Vietnam (CABI, 2001; Rice IPM CD, 2001;

Biology and ecology. The golden apple snail is prevalent in wetland such as marshes, swamps, rivers and irrigation canals lined with vegetation or rice fields. It can survive harsh environmental conditions with pollutants in the water or low dissolved oxygen levels (CABI, 2001). It can bury itself in moist soil during the dry season. It aestivates for 6 months then became active again when the soil is flooded (PhilRice, 2001).

The golden apple snail shell is light brown with creamy white to golden pinkish or orange flesh (Fig. 1). It has both gills and a lung-breathing organ. It digs deep into the mud and surfaces again after renewed flooding. During drought, it closes its operculum. It prefers newly-transplanted rice seedlings up to 15 days after transplanting are vulnerable to golden apple snail damage and from 4 days to 30 days after sowing for direct-seeded rice (PhilRice, 2001). Young plants that are soft and succulent are susceptible because the snail feeds by scraping the plant surface with its rough tongue (Basilio & Litsinger, 1988). It also feeds on any decomposing organic matter. The golden apple snail has separate sexes, which can be morphologically distinguished by the curve of the operculum. The male has a convex operculum while the female has a concave operculum. The shell of the female adult snail curves inward while the male shell curves outward (Dela Cruz, et al., 2000) (Fig. 2).


Fig. 1. Golden apple snail adult and egg mass (PhilRice).

The average sexual maturity of the golden apple snail is attained in 60-90 d after hatching and may spawn at weekly intervals throughout the year (Saxena et al., 1987; Santos, 1987; Halwart,

1994). Mating occurs any time of the day in all seasons of the year in places where there is a continuous supply of water. It is prolific and reproduces ten times faster than the native species (Adalla & Morallo-Rejesus, 1989). A gravid female snail adult can lay as much as 25-1200 eggs or 25-320 bright pink eggs per week with 80% hatchability. Eggs are laid at night on any vegetation, levees, twigs, stakes, or stones above the water surface. Egg masses are bright pinkish-red (Fig. 1) and turn light pink when about to hatch. Egg incubation is from 7-15 d. After hatching, the soft-bodied juveniles drop into the water and cling onto nearby surface. Their shells harden in 2 days and the hatchlings crawl when they reach 2-5 mm in size (CABI, 2001). Hatchlings grow and mature fast. They are voracious feeders and grow quickly, maturing at about 2 months old. They have been called “eating machines” because they can eat 24 hours a day. The most destructive stage is when the length of the shell is from 10 mm or 1 cm (about the size of a corn seed) to about 40 mm or 4 cm (about the size of a pingpong ball) (Dela Cruz et al., 2000). It devours the base of young seedlings and can even consume the young plants in a rice field overnight. The feeding damage results to missing hills (Fig. 3) and floating cut leaves on the water surface (Saxena et al., 1987). At 30 days after transplanting, medium- sized snails (2-3 cm shell height) at a density of one and eight snails/m2 had reduced the number of tillers by 19% and 98%, respectively (Basilio, 1991). Furthermore, 0.5 snails/m2 cause 6.5% and 8.0 snails/m2 93% of missing rice hills. The golden apple snail can live from 2 to 6 years with high fertility.

Fig. 2 Ventral view of male and female adults of golden apple snail (PhilRice).

Fig. 3. Missing rice hills (JLA Catindig, IRRI).

The snail has become a major pest not only of rice but also of the aquatic nitrogen-fixing fern Azolla (Saxena et al., 1987; Mochida et al., 1991), taro, and lotus plants (Mochida, 1988) in the Philippines. It also feeds on maize, citrus, ramie (Adalla & Morallo-Rejesus, 1989), cassava, papaya, kangkong, sweet potato, algae, duckweed, water hyacinth, and other succulent leafy plants (PhilRice, 2001 & 2002).

Recent findings in the rice field in La Union, Philippines showed that the golden apple snail was found to be effective against weeds ( It is now consider by farmers an ally rather than an enemy because it can now manage weeds in lowland irrigated where transplanted rice is planted. The snail would benefit farmers provided that the field is leveled very well so that the depth of water as well as movement of the snail could be controlled. No water should be added to the field after transplanting for four to six days. Water should be released into the field once weeds have grown to one centimeter. By this time, the rice plants are already 25 to 28 days old and their stems are already hard. The snail would prefer the soft and succulent weeds.

Pomacea canaliculata is similar to other snails including P. doliodes and P. glauca, which are pests of rice in Suriname, and P. insularum in South America. It may also be confused with other snails of the genus Pomacea that are raised for food including P. gigas and P. cuprina which may have escaped into rice fields in Asia (CABI, 2001).

Damage and infestation. In the Philippines, the first report on actual damage of the golden apple snail was when it devastated Region 2 (Cagayan Valley) with an estimated damage of about 300 hectares of irrigated rice in 1986 (Adalla & Morallo-Rejesus, 1989). In 1988, the reported damage increased to an estimated 130,945.78 hectares to 426,000 hectares. It had reached more than 800,000 hectares by 1995 (Cagauan et al., 1998). Pesticide expenditure for 1988 was estimated to be US $ 2.4 million (Halwart, 1994). According to another estimate, yield loss of rice by GAS in 1990 was at 70,000 to 100,000 t valued at US $ 12.5-17.8 million (Naylor, 1996). The total cost due to the golden apple snail including yield loss, replanting cost and the cost of control such as molluscicides and handpicking was estimated at US $ 28-45 million. The cumulative costs after the snail invasion up to 1993 were estimated as between US $ 425-1,200 million (CABI, 2001). Since then, rice area infested with GAS has been increasing until it became a national menace (PhilRice, 2001). It was reported that of the 3 million hectares of rice fields in the Philippines, 1.2-1.6 hectares are infested by the golden apple snail (PhilRice, 2001).

Management. There are physical, mechanical, cultural, biological, and chemical control measures recommended against the golden apple snail (Anonymous, 1989; Morallo- Rejesus et al., 1990; Mochida, 1991).

The physical control practice of managing the snail is to install screens with 5-mm mesh at water inlets (Anonymous, 1989; Litsinger & Estaño, 1993). This can minimize the entry of snails into the rice fields and will also facilitate hand-collection.

Increase mortality by mechanical action prior to crop establishment is advisable. It includes handpicking and crushing, staking with bamboo or other wooden stakes before and after transplanting can be practiced to facilitate egg mass collection (Saxena et al., 1987). Likewise, the use of a hand-operated device to smash egg clusters between two snail egg clappers can also reduce the snail population (Awadhwal & Quick, 1991).

Among the recommended cultural control measures, crop establishment, planting methods, seedling rate, good leveling the field to remove snail refuges and facilitate drainage, planting at higher densities, burning straw, are the most used methods (FAO, 1989; Litsinger & Estaño, 1993; Halwart, 1994). Planting older seedlings, planting at higher densities, or planting on ridges above the water line are advised against the golden apple snail. The field can be leveled-off or hydrotiller or rototiller to prepare the land (Mochida, 1988). An off-season tillage to crush snails can also be employed. Snails can also be exposed to sun. Draining the field is also advised (Litsinger & Estaño, 1993). Crop rotation with a dryland crop and fallow periods is also recommended as control.

For easier drainage and collection of the golden apple snail, canalets can be constructed along bunds and inside paddies. Atractants like newspaper can be used (Joshi & de la Cruz, 2001).

Depressed strips can be constructed to retain a small amount of water drainage. This method also confines the snail to limited areas, hence handpicking can be facilitated. It can be done during the final harrowing period.

Good water management obtained by good levelling for the first two weeks is recommended.

Biological methods include herding ducks and raising fish such as carp and tilapia in the paddy is effective against the golden apple snail (Pantua et al., 1992; Litsinger & Estaño, 1993; Halwart, 1994). Birds prey on both eggs and neonates. Rats and snakes also feed on them. Red ants feed on eggs (

Molluscicides such as metaldehyde is recommended (Mochida et al., 1991). It is non-toxic to fish and other aquatic life.

Rice Black Bug, Scotinophara coarctata (Fabricius)

The rice black bug or RBB, Scotinophara coarctata (Fabricius) is a dreadful insect pest in the Philippines (Estoy et al., 1999). It was first reported as a rice pest in the Philippines on the island of Palawan in 1982 (Barrion et al., 1982). Before this year there was no record of occurrence of this pest in the Philippines (de Sagun et al., 1991). The first reported incidence of RBB in the Philippines was in the southern part of Palawan in September 1979 (Miyamoto et al., 1983). Its spread was later observed throughout the northern and the central parts of Palawan (Miyamoto, et al., 1983; Mochida et al., 1986; Villareal, personal communication). From Palawan, it moved to Mindanao in 1992 (PhilRice, 2000) and the Visayas region in 1998 and moved back again in Mindanao in 2000 and in the Visayas region in 2001.

Recently, the NationalCropProtectionCenter based at UP Los Baños has advised the DA Regional Office through the Regional Executive Director to be alert for possible entry of the rice black bug into the Bicol Region (

It was believed that the spread of RBB was due to frequent boat transportation between islands, the plain cultivation of wetland habitats and host plants and perhaps the lack of indigenous natural enemies.

Distribution. The rice black bug also occurs in Asian countries such as South China, Vietnam, Brunei, Indonesia, Malaysia, Cambodia, Sri Lanka, Thailand, Myanmar, India, Bangladesh, and Pakistan (Reissig et al., 1986; Subramanian et al., 1986; Singh & Singh, 1987; Ferrer & Shepard, 1987; Ito et al., 1993; CABI, 2001; Rice IPM CD, 2001). It has been a pest of rice in Malaysia for so many years (Corbett & Yusope, 1924; Grist & Lever, 1969; Van Vreden & Ahmadzabidi, 1986).

Biology and ecology. Unlike other pests, which damage the rice plants only at a certain stage, the rice black bug attacks rice at all stages of crop growth particularly from maximum tillering to ripening growth stage (Reissig et al., 1986; PhilRice, 2000). At vegetative stage, the damage is called deadhearts and whiteheads during the reproductive stage. RBB can cause plant stunting and bugburn where the leaves turn reddish brown, resulting to crop loss. The nymphs are the most destructive stage because it feeds at the base of the rice plant (Simbajon, 1992). It also prefers stem nodes because of the large sap reservoir (Reissig, et al., 1986).

The RBB is not common in upland rice ecosystem (Reissig et al., 1986). It inhabits both rainfed and irrigated wetland environments. It is attracted to high-intensity light and produces an offensive odor when disturbed (CABI, 2001; Rice IPM CD, 2001). The bug is a weak flier. Its adult flies to the rice crop to reproduce over several generations when weather conditions are favourable. It returns to its resting sites after crop harvests. It is capable of migrating long distances by ships and other means of transportation (CABI, 2001). Its flight activity is affected by the lunar cycle (PhilRice, 2000). The availability and quality of food also affects its flight activity. Its flight activity increases when there is no food. There is less migration and dispersal if rice plants are readily available as food in the field (PhilRice, 2000).

The adult of the rice black bug is oval-shaped and about 8-9 mm long (Fig. 4). It lives from 3 to 7 months.The female lays about 200 eggs during her lifetime and guards the egg until hatching (Reissig et al., 1986). It deposits its eggs on the lower part of the leaves or on the basal part of the rice plant near the water surface (PhilRice, 2000). The eggs are laid in masses of 40-60 individual eggs in several parallel rows (Fig. 4). During dry conditions, the female bug deposits its eggs on the leaves and stem. Eggs are also laid in cracks on the soil and on roots (Rice IPM CD, 2001). Freshly laid eggs are greenish and turn pink with age. Eggincubation of the rice black bug is 3 to 7 days. The nymphs are brown and yellow with black markings (Reissig et al., 1986). Six nymphal instars are completed in 29-35 days.

Like the adults, the nymphs have similar behavior of remaining in the base of the plant during the day and feeding at night (Fig. 4). The nymphs reached adulthood after 4 to 5 molts in 25-30 days.

Rice is the main host. It also feeds on a number of grasses and broadleaves (Mochida et al., 1982; IRRI Reporter, 1983; Miyamoto et al., 1983; PhilRice, 2000).

S. coarctata is similar to many other oval-shaped shield or stink bugs that occur in rice, but the non-pest species seldom occur in high numbers. S. coarctata is distinguishable from S. lurida by the position of spines on the pronotum (CABI, 2001).

Fig. 4. Black bug adult, egg mass (IRRI) and nymphs (PhilRice).

Damage and infestation. A number of infestations and outbreaks of the RBB have been recorded. For example, 1,246 hectares of rice fields in 4 municipalties in Palawan were damaged in 1982 (Perez, 1989). In this year, at the height of the RBB infestation, the Provincial Government formed the Task Force Black Bug and spent US $ 20,000 for chemicals against RBB (Barrion et al., 1982). A major outbreak in 1985 spread towards the central and northern Palawan covering 4,500 hectares of rice lands (Barrion et al., 1982). In Mindanao, it attacked 2,070 hectares of rice lands affecting 2,430 farmers who suffered a production loss estimated at 2.2 million in 1992 (Fernandez, 1993) and 10,000 hectares of ricelands in 1995 (Apao et al., 1998). In the Visayas, the RBB hit about 6,202 hectares of rice fields in Leyte provinces in 2000 (Tempo, 2004).