PREDATION ON EGGS OF THE APPLE SNAIL POMACEA CANALICULATA (GASTROPODA: AMPULLARIIDAE) BY THE FIRE ANT SOLENOPSIS GEMINATA

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1 PREDATION ON EGGS OF THE APPLE SNAIL POMACEA CANALICULATA (GASTROPODA: AMPULLARIIDAE) BY THE FIRE ANT SOLENOPSIS GEMINATA YOICHI YUSA Kyushu National Agricultural Experiment Station, Nishigoshi, Kumamoto , Japan (Received 29 February 2000; accepted 11 January 2001) ABSTRACT A field survey and two experimental manipulations were made to investigate the extent of predation on eggs of the apple snail Pomacea canaliculata (Lamarck) by the fire ant Solenopsis geminata (Fabricius) in the Philippines. First, when Pomacea egg masses found along levees of paddy fields were observed, more than half of them had some damage. More fire ants were observed near egg masses with higher degrees of damage. Secondly, when egg masses were experimentally placed on levees, on average 50% of the eggs were lost (removed or damaged) within two days in March and 38% were lost within three days in August. Thirdly, egg masses were placed in cups with or without water on levees; no eggs were lost when ants were successfully excluded by water. The proportion of lost eggs was highly variable among egg masses, but there was no difference between day and night. Possible use of this ant as a biocontrol agent for the apple snail is considered. INTRODUCTION The apple snail Pomacea canaliculata (Lamarck, 1819) is indigenous to South America. It was introduced as human food into Asia mainly in the 1980s, and became distributed in many countries in tropical, sub-tropical and temperate areas (Halwart, 1995), and its distribution is still expanding (Baker, 1998). P. canaliculata is a pest of rice in many Asian countries because it feeds voraciously on rice seedlings. Current methods to control P. canaliculata in paddy fields include draining or keeping water low while rice is young and susceptible to feeding, hand picking snails, and applying pesticides (Yusa & Wada, 1999). However, these methods are impossible or ineffective when fields are poorly-drained or flooded. Biological control may have potential not only in paddy fields (Halwart, 1995) but also in canals and ponds (Yusa & Wada, 1999). Ducks (Cagauan & Van Hove, 1998), carp or Nile tilapia (Halwart, 1995) have been released in paddy fields for snail control as well for as meat production. They are often effective in reducing snail density, but require a special care. Predators such as leeches (Ozawa, Makino & Isigami, 1989), firefly larvae (Kondo & Tanaka, 1989) or dragonfly larvae (Suzuki, Miyamoto, Matsumura, Arimura & Tubiano, 1999) can eat the snail in laboratory conditions, but few animals have been observed to consume the snail in the field (Yusa, Sugiura & Ichinose, 2000). The apple snail lays egg masses on stems of plants or walls above water, so the eggs face different predation pressures from young or adult snails. Irrespective of the conspicuous red color of the eggs, very few animals consume them, probably because they are unpalatable (Snyder & Snyder, 1971). Predation on the eggs of Pomacea canaliculata by the fire ant Solenopsis geminata (Fabricius) (Hymenoptera: Formicidae) has been observed in the Philippines (Way, Islam, Heong & Joshi, 1998) and Thailand (Chanyapate, 1997). The ant is indigenous to the southern part of North America and Central America. It was unintentionally introduced into many tropical and sub-tropical areas. In this study, the extent of predation on the snail eggs by the ant was quantified in the Philippines. MATERIALS AND METHODS Observations were made at the International Rice Research Institute (IRRI), Los Baños, Central Luzon in the Philippines (14 10 N, E). First, the first 50 egg masses of P. canaliculata found along the levees (bunds) of paddy fields were examined in the morning of 26 March The proportion of damaged eggs in each egg mass was estimated, and each mass was categorized into the following three types according to this proportion: 0%; 25%; or 25%. The number of S. geminata found within 20 cm of the plant with J. Moll. Stud. (2001), 67, The Malacological Society of London 2001

2 YOICHI YUSA an egg mass was estimated during a 20-second count. Fire ant behaviour was also observed. Secondly, intact egg masses of the snail were placed on levees for two or three days and the extent of egg loss during these periods was estimated. Twenty-five and 39 egg masses were used in March and August 1998, respectively. Stems of rice or weeds with undamaged egg masses were cut, and a tip of each stem was put into a hole of a rubber plug placed on the levees 2 m apart from each other along a transect. The lowest part of each egg mass was set 3 5 cm above the ground. They were observed once or twice a day (5:00 7:00 and/or 17:00 19:00). In each observation, the maximum length of each egg mass, and its maximum width (diameter) perpendicular to it, were measured with calipers. The proportion of removed eggs (i. e., eggs carried away) between two consecutive observations was estimated from the change in the length and width, since the total number of eggs in an egg mass can be estimated from its maximum length and width (Tanaka, Watanabe, Higuchi, Miyamoto, Yusa, Kiyonaga, Kiyota, Suzuki & Wada, 1999). The proportion of damaged eggs (i. e., eggs broken in situ) was estimated by sight. The proportion of lost eggs was defined as proportion of removed eggs added to that of damaged eggs. Thirdly, seven sites, 1 20 m apart, were randomly chosen along a transect on levees, to investigate the consequence of ant exclusion and the difference in ant predation rate between day and night. In each site one pair of plastic cups (ca. 7 cm diameter and 4 cm deep) with egg masses were placed 30 cm apart, for 4.5 days in March A rubber plug was placed at the center of each cup, and a plant stem with an intact egg mass of P. canaliculata was put in the hole of the rubber plug. Water (ca. 2 cm deep) was put in one cup of each pair to keep ants away from the eggs, and the other cup was kept without water. Egg masses were changed twice a day (5:00 7:00 and 17:00 19:00; thus egg masses were used for each water condition), and the proportion of eggs lost (either removed or damaged) during 12 hours was estimated. RESULTS Solenopsis geminata were observed consuming eggs of 18% (9 / 50) of Pomacea egg masses found along levees. Most were minor workers, but there also were major workers. The ants usually tried to remove individual eggs from the egg mass with their mandibles, and when successful, they carried the eggs away, presumably to their nests. Ants consumed eggs at any developmental stage, from newly-laid eggs (distinguishable by their milky pink color) to those ready to hatch (grayish color, which reflects the pigments of snails inside the eggs). Egg masses with damaged eggs were frequently found along the levees (Fig. 1), but ants appeared to damage eggs only when they failed to remove the eggs from the egg mass. Damaged eggs were found in 58% Figure 1. Egg mass of Pomacea canaliculata damaged by the fire ant Solenopsis geminata. (29 / 50) of egg masses. More fire ants were found near egg masses with higher proportions of damaged eggs (Table 1; H 19.4, P 0.001, Kruskal-Wallis test). Among egg masses experimentally placed on levees, both the number of masses with lost eggs (either removed or damaged) and the proportion of lost eggs per egg mass increased with time during the two- or three-day observation periods in March and August, respectively (Fig. 2). In March, at least some eggs in 92% (23 / 25) of egg masses were consumed in two days. In August, eggs in 59% (23 / 39) of egg masses were consumed in two days, and those in 67% (26 / 39) of egg masses in three days. Thus the number of egg masses with lost eggs were greater in March than in August within two days (P 0.01; Fisher s exact probability test). The average proportion of eggs lost per egg mass (including intact egg masses) was also greater in March than in August: 50 38% (mean SD, n 25) in March and 27 35% in August in two days (n 39; U 302, P 0.05; Mann-Whitney U-test), and 38 42% in three days in August. The sizes of egg masses (expressed as maximum length width in mm) were Table 1. Relationship between proportion of damaged eggs in egg masses of P. canaliculata deposited along levees and number of fire ants within 20 cm of the plant with each mass Proportion of No. of egg No. of ants damaged eggs (%) masses observed (mean SD)

3 PREDATION ON POMACEA EGGS BY ANTS Figure 2. Examples of change in the proportion of eggs of P. canaliculata lost over time in March (left) and in August (right). Each line indicates an egg mass. Thick line indicates the average. larger in March (mean SD ) than in August (248 56; U 295, P 0.01). In both months, the proportion of eggs lost in each egg mass varied greatly: some egg masses remained intact throughout the observation periods whereas others were completely lost (Fig. 2). Egg mass size had no significant correlation with the proportion of eggs lost at the end of the experiment both in March ( 0.13, P 0.3; Kendall s rank correlation test) and in August ( 0.12, P 0.2). When egg masses were placed in plastic cups without water, eggs in 34% (21 / 62) of egg masses were consumed within 12 hours (one egg mass was disturbed by accident and was excluded from the data). In contrast, only 2% (1 / 63) of egg masses were consumed when cups were filled with water. This was because the rice stem touched the edge of the cup and allowed ants to consume the eggs. Egg mass sizes were not significantly different between the two treatments (mean SD of the maximum length width in mm , n 62 for cups without water; , n 63 for cups with water; T s 835, P 0.3; Wilcoxon s signed-rank test for 62 pair observations). Egg loss percentages were highly variable among egg masses placed in cups without water (mean SD 7 15%). The percentages were not significantly different between observations at day and at night of the same date (n 1 n 2 7, T s 4.5, P 0.8 for 27 March; n 1 n 2 7, T s 0, P 0.1 for 28 March; n 1 n 2 7, T s 2, P 0.5 for March 29; data for 30 March were impossible to test statistically due to small data size with different ranks; Wilcoxon s signed-rank test). Egg mass sizes were not different between day- and nightobservations (n 1 n 2 7, T s 6 11, P 0.1 for each of the above date). DISCUSSION Direct observations indicated that S. geminata consumed eggs of P. canaliculata. There was no loss of eggs in egg masses when ants were successfully excluded. An unidentified species of small brown ant was sometimes observed on or inside damaged eggs of P. canaliculata, but it was not observed consuming intact eggs. Ants of the genus Pheidologeton also consume eggs of P. canaliculata (Way, pers. comm.). P. canaliculata egg masses were frequently observed both at day and at night before, during and after the experiments, but no other animals were observed consuming snail eggs. Therefore most of the damage observed in this study was attributed to fire ant predation. Snyder & Snyder (1971) reported that several animals, mainly fish and birds, eat eggs of the Florida apple snail P. paludosa Say in the laboratory. They also reported that a millipede and a frog infrequently ate eggs of P. paludosa in the field. In Brazil, Guimarães (1981) found that some aquatic birds consumed young and adult snails as well as egg masses of P. haustrum (Reeve), but the frequency of this predation was not recorded. Egg masses of P. canaliculata were examined by the present author in several places in southern Brazil and Argentina, but no predation was noticed. S. geminata is the only animal known to consume Pomacea eggs to any considerable extent in the field. In paddy fields without water, fire ants also attack young snails (Way et al., 1998; Yusa, pers. obs.). Recently, another fire ant, S. invicta Buren, was reported to attack adult apple snails, P. paludosa in a laboratory experiment (Stevens, Stevens, Darby & Percival, 1999). Half of the eggs of P. canaliculata placed on the levees were lost within two days in March, and about 277

4 YOICHI YUSA one-third were lost in three days in August. These figures were estimated using the changes in the maximum length and width of each egg mass between observations, but some eggs might have been lost without any change in the length and width of the egg mass. In such cases, the actual proportion of eggs lost should have been higher. As the embryonic period of the apple snail is 9 14 days under natural conditions in Central Luzon (Lacanilao, 1990), most of the eggs laid on levees would be eaten by fire ants before hatching. Solenopsis spp. are known as agricultural or human pests, but they are also beneficial predators of other pests (Pimentel, 1955; Risch, 1981; Risch and Carroll, 1982; Way et al., 1998). This study demonstrated that S. geminata is a predator of P. canaliculata eggs. The ants could consume eggs irrespective of developmental stages or egg mass size. Still, current predation pressure in the Philippines is not high enough to control snail populations. For a successful control, it is necessary to increase the number of active ants on levees, and to allow them to enter into paddy fields, where apple snails lay eggs on rice stems. Keeping suitable habitats for ants (dry, high levees with regular disturbance) and periodic draining of paddy fields would be effective for these purposes (Way et al., 1998). At the same time, care should be taken to control fire ant populations where they are already present, and to prevent expansion of their distribution, since they are also an exotic, potentially destructive pest. ACKNOWLEDGMENTS I wish to thank Ms. Liberty Almazan and Mr. Nanding Elec for help, Drs. Kong Luen Heong, Yoshito Suzuki for discussion, Mr. Alberto Barrion and Dr. Tomonari Watanabe for information on Solenopsis, Drs. Takashi Wada, Katsuya Ichinose, Michael Way for critical reading of the manuscript. I am deeply indebted to Dr. Michael Way for his kind suggestion, discussion, and encouragement during this study. This study was supported by Japan-IRRI shuttle project on the ecology of Pomacea canaliculata. REFERENCES BAKER, G.H The golden apple snail, Pomacea canaliculata (Lamarck) (Mollusca: Ampullariidae), a potential invader of fresh water habitats in Australia. In: Pest Management Future Challenges. Sixth Australian Applied Entomological Research Conference, 2: The University of Queensland, Brisbane, Australia. CAGAUAN, A.G. & VAN HOVE, C The effects of molluscicide, Nile tilapia (Oreochromis niloticus), the aquatic fern azolla (Azolla microphylla), and mallard ducks (Anas platyrynchos) on the abundance of golden apple snails (Pomacea canaliculata Lamarck) in integrated lowland irrigated ricefield. In: International Workshop on the Integrated Management of the Golden Apple Snail in Rice Production in Vietnam, 4 6 August 1998, Nghe An Province, Vietnam, 17 pp. Ministry of Agriculture and Rural Development of Vietnam and Food and Agriculture Organization of the United Nations. 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Behaviour, 40: STEVENS, A.J., STEVENS, N.M., DARBY, P.C. & PER- CIVAL, H.F Observations of fire ants (Solenopsis invicta Buren) attacking apple snails (Pomacea paludosa Say) exposed during dry down conditions. Journal of Molluscan Studies, 65: SUZUKI, Y., MIYAMOTO, K., MATSUMURA, M., ARIMURA, K. & TUBIANO, F Predacious natural enemies of the golden apple snail, Pomacea canaliculatajuveniles in paddy fields. Kyushu Agricultural Research, 61:

5 PREDATION ON POMACEA EGGS BY ANTS TANAKA, K., WATANABE, T., HIGUCHI, H., MIYA- MOTO, K., YUSA, Y., KIYONAGA, T., KIYOTA, H., SUZUKI, Y. & WADA, T Density dependent growth and reproduction of the apple snail, Pomacea canaliculata: a density manipulation experiment in a paddy field. Researches on Population Ecology, 41: WAY, M.J., ISLAM, Z., HEONG, K.L. & JOSHI, R.C Ants in tropical irrigated rice: distribution and abundance, especially of Solenopsis geminata (Hymenoptera: Formicidae). Bulletin of Entomological Research, 88: YUSA, Y., SUGIURA, N. & ICHINOSE, K Predation on the apple snail, Pomacea canaliculata (Ampullariidae), by the Norway rat, Rattus norvegicus, in the field. Veliger, 43: YUSA, Y. & WADA, T Impact of the introduction of apple snails and their control in Japan. Naga, The ICLARM Quarterly, 22:

Haruko YOSHIE and Yoichi YUSA*

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