Laboratory observations on the biological control of Biomphalaria glabrata by a species of Pomacea (Ampullariidae)*

Bull. Org. mond. Sante 1972, 46, 243-247 Bull. Wld Hlth Org f Laboratory observations on the biological control of Biomphalaria glabrata by a species of Pomacea (Ampullariidae)* HELENE M. PAULINYI 1 & ERNEST PAULINI 2 Laboratory experiments have shown that medium-sized (30-S50 mm in shell height) Pomacea sp. snails consumed the egg masses ofBiomphalaria glabrata deposited either on glass or on the leaves of Salvinia, and that they also caused a high mortality rate among the newly hatched B. glabrata. When the two species of snail were kept in the same tank, the Pomacea sp. caused a reduction in the B. glabrata egg density in proportion to their relative numbers and the presence of Pomacea sp. prevented colonies of B. glabrata from becoming established. The identity of the Pomacea sp. has not yet been satisfactorily established. The control of Biomphalaria glabrata by predation of another snail (Marisa cornuarietis) has been reported from Puerto Rico (Oliver-Gonzalez & Ferguson, 1959; Ruiz-Tiben, Palmer & Ferguson, 1969), and was the object of laboratory studies by Chernin, Michelson & Augustine (1956). One of the present authors (E. P.) has noted that since 1955 B. glabrata has been absent from a natural lake (Lake Sete-Mares) in the Municipio Pedro Leopoldo, Minas Gerais, Brazil, about 40 km north of Belo Horizonte. Periodic collections from this lake have revealed the presence of a large population of snails belonging to a species of Pomacea, but B. glabrata has never been found in any collection in spite of the fact that most streams in that area harbour planorbid snails. Andrade (1959) referred to the presence of Pomacea haustrum (Reeves) in the lake of Pampulha (Belo Horizonte) and suggested that this ampullarid snail might have " competed " with B. glabrata for the habitat since the planorbid population was smaller than reported previously. The present authors have made periodic snail collections along the Pampulha lake shore during the last 3 years (1967-70) at 35 stations situated at 500-m intervals. * This study was supported by the World Health Organi- zation. I Biologist, Centro de Pesquisas Rene Rachou, Belo Horizonte, Brazil. 'Professor Titular, Escola de Engenharia da Universidade Federal de Minas Gerais, Belo Horizonte, Brazil. Table 1. Snail collections around Lake Pampulha, Belo Horizonte, Brazil No. of snails collected Date No.of dips B. Pomacea Physa Others glabrata sp. sp. 15 May 1967 350 29 55 5 2 12 Sept. 1967 370 3 127 - - 11 Feb. 1968 370 - 70 - 25 Sept. 1968 360 15 153 10 - 22 Dec. 1969 350 7 57 - 7 July 1970 350 13 29 _ _ The collections revealed many more Pomacea sp. than any other snail, including B. glabrata (Table 1). From these observations it became evident that an experimental laboratory programme to study the interaction between populations of Pomacea sp. and B. glabrata might be useful in explaining the absence of B. glabrata from habitats containing Pomacea sp., as observed in the field. MATERlALS AND METHODS The snails used in the experiments were taken from laboratory colonies. These colonies were started with specimens of B. glabrata and Pomacea 2797 - 243 - H. M. PAULINYI & E. PAULINI sp. collected in the Pampulha lake and maintained in 30-litre tanks. The water was continuously aerated and illuminated with fluorescent lamps. Salvinia sp. and several specimens of Lebistes reticulatis were also kept in each tank. Fresh lettuce in abundance was supplied daily as food for the snails. The water of the tanks was changed once a week. Maximum and minimum temperatures were recorded every day. RESULTS Experiment 1 The objective of the first experiment was to observe the fate of B. glabrata egg masses in the presence of large Pomacea sp. snails. Nine 200-ml beakers were stocked with 1-2 mature B. glabrata. After a few days, the snails and water were removed, and the number of egg masses deposited on the walls of each beaker was recorded. The beakers were then filled with chlorine-free tap water and 1 Pomacea (about 30 mm in shell height) was added to each of 7 beakers; 2 beakers served as controls. No food was supplied to the Pomacea sp. After 24 hours the number of egg masses in each beaker was again recorded. The results showed that in the absence of other food Pomacea sp. apparently consumed 25 (74%Y.) of the 34 egg masses present in the containers. This was the first direct evidence for the destructive effect of Pomacea sp. on B. glabrata egg masses. Experiment 2 The fate of B. glabrata egg masses when leaves of Salvinia were also present was then investigated. Since there was a possibility that Pomacea sp. might show a preference for the eggs of B. glabrata, Salvinia leaves with and without egg masses were offered to these snails. Three groups (A, B, C) of 4 beakers were prepared; each beaker contained 200 ml of water and 1 Pomacea sp. snail (about 40 mm in shell height). To each beaker of group A, 2 disks 1 cm in diameter cut out of Salvinia leaves without B. glabrata eggs were added. To each beaker of group B, a 1-cm disk of Salvinia leaf with a B. glabrata egg mass on it and another disk without eggs were added. To each beaker of group C, two 1-cm disks of Salvinia leaf, each bearing an egg mass, were added. After 24 hours, the number of leaf disks with and without eggs that had been eaten by the snails was recorded. Disks that had been eaten were replaced by new ones of the same kind, and another observa- tion was made after a further 72 hours. A second run was made with the same number of beakers and leaves, but with only one observation being made after 72 hours. There was no significant difference between the number of leaf disks with and without eggs that were eaten but there was some indication that Pomacea sp. snails may occasionally prefer eggs of B. glabrata in the presence of other food. Experiment 3 The fate of newly hatched B. glabrata in the pre- sence of Pomacea sp. snails was investigated in the following way. Six 500-ml beakers were prepared with clean tap water and about 100 newly hatched (1 day old) B. glabrata. One specimen of Pomacea sp. was added to each of three beakers, 2 Pomacea sp. snails were added to one beaker, and the other two beakers were left without any Pomacea sp. snails. No food was given to the snails. After 24 hours, the number of living B. glabrata was counted. The results showed that the mortality of B. glabrata was significantly higher in the presence of Pomacea sp. snails than in the control beakers, and that-when correction is made for the natural mortality of the B. glabrata by means of Abbott's formula-the Pomacea sp. snails caused a 60% reduction of the newly hatched snails under the experimental condi- tions. Experiment 4 The previous experiments showed that Pomacea sp. snails destroyed egg masses and newly hatched snails when they were confined together in a relatively small space. The next experiment was designed to observe the fate of B. glabrata egg masses when they were continuously produced by a fixed number of mature snails in breeding tanks in the presence of various numbers of Pomacea sp. snails. For this purpose 3 tanks (A, B, C) were prepared, each with 30 litres of water and 20 mature B. glabrata (shell height 14-30 mm). Salvinia was added to cover about a third of the water surface. Altogether, 10 specimens of Pomacea sp. (shell height 37-50 mm) were placed in tank A and 2 Pomacea sp. were placed in tank B. No ampullarid snails were added to tank C. Lettuce in excess was supplied daily to each tank. The number of snails and the number of egg masses of B. glabrata were counted and recorded weekly for 10 weeks. The results given in Table 2 show that there was a uniformly high egg density in tank C containing no Pomacea sp. snails. The egg density 244 BIOLOGICAL CONTROL OF BIOMPHALARIA GLABRATA BY A SPECIES OF POMACEA Table 2. Production of egg masses by B. glabrata in the presence of Pomacea sp. Tank A B. Egg mass glabrata a density b 20/0 20/19 20/64 19/53 19/70 19/74 16/40 11/40 0.95 3.20 2.80 3.70 3.90 2.50 3.63 Tank B Pomacea B. Egg mass sp. glabrata a density b 2 2 2 2 2 2 2 2 20/0 20/43 20/67 18/88 17/117 16/112 17/90 18/127 2.15 3.35 4.90 6.85 7.00 5.30 7.00 Tank C B. Egg mass glabrata a density b 20/0 20/13 20/143 20/160 20/150 20/151 23/161 c 55/158 C 7.55 7.15 8.00 7.50 7.55 7.00 2.87 a Number of snails/number of egg masses. b Average number of egg masses/snail. c Juvenile snails also included. was somewhat lower in tank B (2 Pomacea sp. snails) and about 50% lower in tank A in the presence of 10 Pomacea sp. Experiment 5 This experiment was designed to observe the formation of B. glabrata colonies in the presence of Pomacea sp. Three tanks (A, B, C) were prepared with 30 litres of water and Salvinia as in experiment 4. First, tanks B and C were each stocked with 10 mature B. glabrata (shell height 15-20 mm). After 10 days, 20 young Pomacea sp. snails (shell height 2-3 mm) were introduced into tanks A and B. Lettuce was supplied in excess to each tank. The temperature of the laboratory was maintained at 25° 3°C during the experiment, which lasted for 8 months. Observa- tions were made periodically on the number and size of snails and on the number of egg masses present. The population of Pomacea sp. in tank A decreased from 20 to 17 on account of accidental deaths, probably caused by repeated handling of the snails during the observation period. The surviving snails showed considerable growth and reached a maximum shell size of 47 mm in 248 days. No oviposition occurred during this period. The population of B. glabrata in tank C showed a slow increase at the beginning, then increased rapidly to over 20 times the original number. The number of egg masses also increased but much more slowly. Tank B with its mixed snail population showed the influence of the Pomacea sp. snails on the B. glabrata. There was only a slight increase in the planorbid population during the first month of observation; later, B. glabrata declined in number and finally disappeared from the tank. It was interesting that very few egg masses of B. glabrata were seen after the first day when Pomacea sp. snails were added to the tanks. These results indicate that, under the experimental conditions, mature B. glabrata failed to colonize a tank in which twice their number of Pomacea sp. snails were also present. The most important difference was seen in the number of egg masses, which became very scarce. Apparently no new gene- ration of planorbid snails could develop from the few eggs that might have escaped the destructive activity of the Pomacea sp. Experiment 6 This experiment was carried out to confirm the results obtained in experiment 5. The variation in number of B. glabrata in the two tanks during the experiment is shown in Fig. 1. There was a small decrease in the Pomacea sp. snail population in both tanks (A and B) and no eggs were laid by these snails during the observation period. The planorbid snails thrived very well in tank C, and their number increased 10-fold in 30 days and then remained stable. However, the B. glabrata population did not do Days 0 7 14 22 28 35 40 71 Pomacea sp. 10 10 10 10 10 10 10 10 l | 245 H. M. PAULINYI & E. PAULINI 1000 200 .0 E 100 50 20 10 5 2 Days 250 WHO 10932 Fig. 1. Variation of the B. glabrata population in the presence (tank B) and absence (tank C) of Pomacea sp. The initial population of tank B was 10 specimens of B. glabrata and 20 specimens of Pomacea sp. ( * = first experiment;A = second experiment). The initial population of tank C was 10 specimens of B. glabrata ( 0 = first experiment; 0 = second experiment). well in the presence of the Pomacea sp. Their number increased about 5-fold in the first month, but the population then started to decline in numbers and at the end of the fifth month of observation there were no B. glabrata in tank C. DISCUSSION The results obtained in the six experiments suggest that Pomacea sp. snails might reduce field popula- tions of B. glabrata under conditions that appear favourable for both species. Under laboratory con- ditions Pomacea sp. snails displayed some preference for B. glabrata egg masses as food but consumed the same proportion of Salvinia leaves with and without attached egg masses, and in the absence of other food they consumed the egg masses of B. glabrata depos- ited on glass. The Pomacea sp. snails caused very high mortality among the newly hatched B. glabrata snails and reduced the numbers of the latter 'by eating their egg masses, the reduction being proportional to the number of Pomacea sp. snails present. In two experiments of long duration, the presence of Pomacea sp. snails in the tanks prevented the estab- lishment of active B. glabrata colonies. These experiments suggest that Pomacea sp. might successfully compete with B. glabrata under field conditions that seem favourable for both species. The success of Pomacea sp. as an agent of biological control will depend on extensive preliminary field observations. Experiments should be carried out in the field in order to determine the environmental conditions most suitable for this type of control operation. If B. glabrata could be controlled in lakes, reser- voirs, and in standing water in general, by biological means, this would contribute considerably to the control of schistosomiasis, since great water masses are not at present treated with molluscicides on account of the high cost of such operations. When large field populations of this ampullarid snail are found in natural bodies of water, with or without small numbers of B. glabrata, it is highly probable that either a former B. glabrata colony has been 246 BIOLOGICAL CONTROL OF BIOMPHALARIA GLABRATA BY A SPECIES OF POMACEA 247 eliminated by the Pomacea sp. or that the formation of colonies is being prevented by the predatory activity of the Pomacea sp. There is apparently some doubt concerning the identification of the Pomacea sp. occurring in Lake Pampulha. Andrade (1959) referred to the Pomacea found in the lake as Pomnacea haustrum (Reeves) while Ferguson (1968) reported that he had received specimens of the same locality and called them Pomacea australis. Specimens sent to the British Museum (Natural History) were identified as Ampul- laria insularum (D'Orbigny). ACKNOWLEDGEMENTS The authors are grateful to Mr Ary Moreira de Miranda and Mr Wilson Silva for their assistance during this study. RtSUMJE OBSERVATIONS FAITES AU LABORATOIRE SUR L'EVICTION BIOLOGIQUE DE BIOMPHALARIA GLABRATA PAR UNE ESPLCE DE POMACEA (AMPULLARIIDAE) Dans certaines regions de l'Etat de Minas Gerais, au Bresil, la densite des populations de Biomphalaria gla- brata est particulierement faible lorsque ce mollusque coexiste avec une autre espece, Pomacea sp. Cette consta- tation a incite les auteurs a rechercher au laboratoire une eventuelle action predatrice de Pomacea. Une serie d'experiences ont montr6 que Pomacea se nourrit des amas d'aeufs de B. glabrata deposes sur les parois d'un recipient ou sur des feulles de vegetaux. Sa presence entraine une mortalite elevee chez B. glabrata recemment eclos. La densite des aeufs de B. glabrata decroit en proportion du nombre de Pomacea presents dans I'aquarium. Introduit dans la proportion de 2 contre 1 dans une population de B. glabrata, Pomacea empeche ce dernier de se d6velopper et l'elimine comple- tement apres 5 a 6 mois. Ces observations laissent supposer que dans des condi- tions de milieu favorables aux deux especes, Pomacea, par son action predatrice sur B. glabrata, d6truit ce der- nier ou tout au moins l'empeche de se multiplier. Le probleme de l'identification precise de Pomacea sp. n'est pas encore r6solu. REFERENCES Andrade, R. M. de (1959) Rev. bras. Malar., 11, 653-671 Chemin, E., Michelson, E. H. & Augustine, D. L. (1956) Amer. J. trop. Med. Hyg., 5, 297-307 Ferguson, F. F. (1968) Hyacinth Control J., 7, 7-11 Oliver-Gonzalez, J. & Ferguson, F. F. (1959) Amer. J. trop. Med. Hyg., 8, 56-59 Ruiz-Tiben, E., Palmer, J. R. & Ferguson, F. F. (1969) Bull. Wld Hlth Org., 41, 329-333