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Dynamics of Populations of glabrata and B. straminea under Semi-Natural Conditions Dinâmica das Populações dos Caramujos Biomphalaria glabrata e B. straminea em Condições Semi-Naturais

1 1 Frederico S. Barbosa ; 2Odécio Sanches ; 2 Constança S. Barbosa & Francisco Arruda

BARBOSA, F. S.; SANCHES, O.; BARBOSA, C. S. & ARRUDA, F. Dynamics of Snail Populations of Biomphalaria glabrata and B. straminea under Semi-Natural Conditions. Cad. Saúde Públ., Rio de Janeiro, 8 (2): 157-167, abr/jun, 1992. Growth curves and mortality rates for populations of Biomphalaria glabrata and B. straminea bred under semi-natural conditions are reponed. Snail populations of the above were maintained for 220 weeks in indoor cement channels. Data were recorded at 20 week intervals. Crude densities are significantly different for each of the studied populations. B. glabrata showed the lower figure while B. straminea R3 strain showed the best performance. The latter is able to live in half the volume of water needed for B. glabrata when both are submitted to population pressure. Keywords: Snail Population Dynamics; Competitive Displacement; Biomphalaria; Brazil

INTRODUCTION MATERIALS AND METHODS

There is strong and diversified evidence For the present observations, showing that is an laboratory-reared strains of B. glabrata and B. efficient competitor against B. glabrata straminea were used. The former (PA strain) (Barbosa, 1973; Michelson & Dubois, 1979; originated from natural breeding places in the Guyard & Pointier, 1979; Barbosa et al., 1981, county of Paulista, about 40 Km from Recife, in 1984, 1985; Barbosa, 1987). Studies on the coastal forest region of the State of interactions between the two species demand a Pernambuco, Brazil. Two strains of B. knowledge of the factors that may influence the straminea were used: an albino black-eyed competitive process. Among these factors strain (PT) partially resistant to with growth and reproduction are the most relevant mansoni, originated from irrigation In the current paper the population dynamics of ditches in the county of Petrolândia, 420 Km B. straminea and B. glabrata living under west of the sea coast of the State of semi-natural conditions, as previously described Pernambuco. The second one is a pure albino (Barbosa et al., 1983), is presented. This study resistant strain, named R3. This strain is limited to the presentation and discussion of originated from Sete Lagoas, State of Minos data on population growth, size-group Gerais, Brazil, was sent to Dr. C. S. Richards distribution and mortality rates. (Biomedical Research Institute, Rockville, Md, USA) by Dr. W. L. Paraense (Fundação 1 Oswaldo Cruz, Rio de Janeiro, Brazil). The Escola Nacional de Saúde Pública. Rua Leopoldo albino R3 stock was obtained through exposure 2Bulhões, 1480, 21041-210, Rio de Janeiro, RJ, Brasil Centro de Pesquisas Aggeu Magalhães, Campus da to infection and selection of the original Sete Universidade Federal de Pernambuco. Engenho de Meio, Lagoas strain (Richards, in letter to senior 50670-420, Recife PE, Brasil author, 1982). The snail populations were observed for the thirty days. The water is kept at pH neutral period of 220 weeks in separate indoors point by using powder. Sand channels measuring 4.5 m long. Cement roof is screened and washed in the laboratory before covers of the trade mark Kalheta built by its use. The water temperature is kept at 22.4 C Brasilit, were fixed upside down on strong (SD - 1.77) by the use of air conditioning supports in such a way that the upper end of ordinary equipment which is only used in hot the channel was held at 95 cm over the floor. days during summer. was the everyday Both ends of the channels were closed with food for the . In addition, on alternate cement walls. At one end of each channel a tap weeks, the snails were offered cooked-leaves of was fixed at 16 cm over the water surface. At stinging-nettle (Fleurya aestuans), fresh wheat the opposite end, an outlet was placed to germ and fish-food power. Elodea sp. was the regulate the volume of the water inside the only species of aquatic plant introduced in the channel. (Figure 1). Each channel holds 140.6 channels. Each colony was started by seeding (SD = 1.9) average liters of water. with 250 mature snails. The snail population Both indoor aquaria and channels receive dynamics were studied by examination of a 20 natural day light through ordinary windows. per cent sample taken at intervals of 20 weeks. Artificial lights placed in the snail rooms to For each channel, three fixed collecting stations increase the amount of light was only used were established at regular intervals along the during cloudy dark days. Tap water was used in channels. Each station was made of a cross the channels during the experiments. The water segment of a channel of the same size, and before arriving to the channels is dechlorinated inserted as a lining sheet over the inner surface through consecutive passages in two tanks of the channels used in the experiments. The placed at the roof of the building. The water content of the three stations corresponds to 20 drops continuously over the surface of the water per cent of the whole volume of the channel and its input is regulated in such a way that the water. At the moment of the sampling whole content of the channel is replaced every colection, both open sides of the stations are tightly closed with wooden walls kept in place RESULTS by means of two clamps each. To avoid escaping of very young snail specimens the Descriptive results are shown in Tables 1 to wooden pieces are set in a frame of soft rubber. 3 and Figures 2 to 5. Data from statistical At that moment, the whole channel segment analysis are presented in the text and in Figures (collecting station) is gently pulled up while the 2 to 4. Tables 1 to 3 show the absolute water content leaks through screened holes numbers of snails per sample: mortality is placed at the lateral surfaces of the wooden shown in absolute numbers and percentages (in pieces. The whole content of the sample is then brackets). spread over a large shallow pan and the snails In Figures 2 to 4, data on the absolute growth are counted and measured. Plants and sand are rates of the snail populations are plotted. At the carefully examined under a low magnification bottom of these figures the percentage stereoscope. After this operation, snails are put distribution of specimens according to back in the channels. size-groups, are seen2 . In the experimental channels, it was observed The values of c in the proportions trend test that a variable number of snails gathered around (data from Tables 1 to 3) for the survival of the snail populations, indicate that the growth air bubbles formed on the surface of the water curves of the three studied populations follow resulting from the dropping of water from the similar patterns: feeding faucets. To avoid this inconvenience the faucets were closed 48h before the counting a) Biomphalaria glabrata population tends to time. A similar phenomenon occurred with 2 pieces of lettuce around which groups of snails become stable beginning the 60th week (c 7df used to gather. For this reason snails were not = 9.39; 0.20 < P < 0.30). Adjustment of the fed during 48h before sampling (Barbosa et al., straight line for the stability period is 1983). Snails were classified in four size (maximum represented by the equation y = 150.1 + 0.31x diameter) groups as follow: B. glabrata ³ 6.9, (observation corresponding to 100th week was 7.0—11.9, 12.0—16.9, and ³ 17.0 mm; B. considered atypical); straminea £ 3.9, 4.0—5.9, 6.0—7.9, and ³ 8.0 mm. The relationship between age and size is b) for B. straminea, PT strain, the period of very complex and variable. Although age stability was attained at the 120th observation 2 cannot be determined precisely it was decided week (c - 5.04; 0.20 < P < 0.30. The to divide snail populations in size-groups, for 4df theoretical reasons and according to our own stability straight line equation was estimated as experience. The results obtained in the current y = 224.5 - O.10x (mortality rate at 160th week studies seem to warrant this decision. point was considered atypical); The statistical analysis was carried out on the following points: (1) stability of the survival c) the stability period of B. straminea, R3 2 proportions in the snail populations through the strain, begins at 160th week ( c = 0.51; 0.70 proportions trend test (Armitage, 1974); (2) 2df estimation of the stability straight lines for the < P < 0.80) and the estimated stability line number of survivors; (3) hypothesis tests for the corresponds to the equation y = 309.3 + 0.145x. straight line b coefficients; (4) estimation of the common b coefficient to the stability The hypothesis test for the b coefficient of straight line; and (5) covariance analysis for the the three stability straight lines shows that the straight line interceptions. The statistical null hypothesis is not disproved in any of the analysis was carried out on the whole snail snail populations studied (t7df = 0.34; 0.70 < P population samples, independent of their < 0.80 for B. glabrata; t4df = 0.71; 0.50 < P < divisions into size-groups. 0.60 for B. straminea PT strain; and t2df =

1.56; 0.20 < P < 0.30 for B. straminea R3 105.1 + 0.0094x; and B. straminea, PT strain, strain). The common b coefficient for the y = 205.4 + 0.0094x ; and B. straminea, R3 three stability straight lines was estimated strain, y = 307.2 + 0.0094x (Figures 2 to as bc = 0.0094. So, the equations for the 4). Covariance analysis shows that the straight adjusted stability straight line with bc = 0.0094, were as follows: B. glabrata y = line intercepts differ significantly. Figure 5 shows the comparative percentage There is marked variation among the mortality rates for each of the Biomphalaria species/strains of Biomphalaria, as expected. strains studied, according to size-groups at the These variations are related to the number of end of 220th week observation period. snails as well as to the period in which they The data analysis shows that the saturation occur. (carrying capacity) level of the snail colonies is The values of y calculated through the attained at the last countings when growth stability straight lines represent the snail crude begins to oscillate between limits that could be density for each species/strain population of the considered as variations of the population size saturation period. Taking into account the whole at a constant volume of water. Saturation level volume of water per channel (x = 140.6, SD can be also ascertained by changes which = 1.9, liters) and the number of snails estimated occurred in the size-group distributions. As seen as the crude density, it was possible to estimate in the growth curves (Figures 2 to 4), the the number of snails per liter of water during size-group distributions tend to show a regular the saturation period: 5.5 for B. glabrata; 7.3 balance among the four groups of "age" in for B. straminea, PT strain; 10.9 for B. which were divided, towards the end of the straminea, R3 strain. experiment.

DISCUSSION population cycles were independent of the cyclic fluctuations due to external Results show that populations of environmental factors. Another factor to be Biomphalaria can be maintained satisfactorily mentioned is that the Biomphalaria snails bred under semi-natural conditions for at least 220 in in-door channels were not submited to the weeks, and probably for much longer periods. influence of the ordinary macro-fauna found in We still have in our laboratory channels natural fresh-water habitats. flourishing colonies of B. glabrata kept for six Most of the negative intraspecific effects on years. population growth reported in the literature This method opens perspectives for other were observed in snail kept in "closed" types of studies such as snail ecology, genetics laboratory systems. As the experimental snails and related subjects. are generally maintained in laboratory glass We did not find any reliable procedure to aquaria under variable conditions this makes calculate the biomass for eachy snail quantitative comparison difficult (Hairston et population. However, it was possible to al., 1960). Comparisons with the present system estimate the higher snail population levels are unfortunately not possible. (crude density) in the channels at the periods in Results obtained in the current paper clearly which the populations attained their greatest show that different behavioral patterns emerged densities (saturation). These figures are from the studied populations of Biomphalaria significantly different for each of the studied (Figures 2 to 4). This indicates that each populations. The lower figure for B. glabrata species/strain has developed inherent growth can be explained, in part, by the larger size patterns which favor B. straminea. This may attained by those individuals. B. straminea R3 have significance on the competitive strain population took 160 weeks. B. glabrata displacement of B. glabrata by B. straminea attained the same level at 60 weeks. studied by Barbosa (1973, 1987) and other On the other hand, it was shown that under Authors (Guyard & Pointier, 1979: Michelson population pressure, the R3 strain of B. & Dubois, 1979). straminea attains higher density in the same The presence of B. straminea in Hong Kong volume of water than the two other studied and its spreading to new regions of south China snail populations. As a result, this strain is able give a very good idea of the adaptative capacity to live in half the volume needed by B. of this species (Yipp, 1990). glabrata when both are submited to population The most promising method for the biological pressure. control of the snail vectors of is Mortality data presented in Tables 1 to 3 the introduction of competitor non-susceptible should be taken with caution. As snail snails (WHO, 1987). Madsen (1990), countings were made at 20 week intervals, it is complemented by Coimbra (1991) covered most understandable that some snail shells, specially of the recent literature dealing with snail the juvenile ones, may disintegrate during the biological control. 140 day period between each sampling. The experiment by Barbosa-Figueiredo It was not possible to complete data on snail (1989),... the largest controlled and long-term demography due to some technical difficulties. field experiment so far conducted on congeneric For instance, we did not find any reliable competition in Biomphalaria... (Coimbra, 1991) technique to estimate directly fertility by shows that ... biological control based on counting the number of snail eggs laid. competitive displacement between close species It is usually accepted that a stable population holds important potential in the control of is kept in equilibrium by the balance between schistosomiasis (Coimbra, 1991). the limits to population growth imposed by the environment and the potential inherent growth ACKNOWLEDGMENTS of the population. Particular situations were created in the so This work was supported by the called "semi-natural" conditions. In the "Financiadora de Projetos e Pesquisa", Finep, particular case of the current study, the snail the "Superintendência de Desenvolvimento do Nordeste", Sudene, the "Conselho Nacional de , 1987. Competitive displacement of Desenvolvimento Científico e Tecnológico", Biomphalaria glabrata by B. straminea. Memó- CNPq, and the Agency for International rias do Instituto Oswaldo Cruz, 82: 139-141. Development, USA. BARBOSA, F. S.; PEREIRA DA COSTA, D. P. & ARRUDA, F., 1981. New field observations on the competitive displacement between two species of planorbid snail inhabiting north RESUMO eastern Brazil. Memórias do Instituto Oswaldo Cruz, 78: 361-366. BARBOSA, F. S.; SANCHES, O.; , 1983. Competitive interactions between BARBOSA, C. S. & ARRUDA, F. Dinâmica species of freshwater snails. I. Laboratory, la. das Populações dos Caramujos General methodology. Memórias do Instituto Biomphalaria glabrata e B. straminea em Osvaldo Cruz, 78: 335-341. Condições Semi-Naturais. Cad. Saúde Públ., , 1984. Competitive interactions between Rio de Janeiro, 8 (2): 157-167, abr/jun, 1992. species of freshwater snails I. Laboratory studies, Curvas de crescimento e taxas de mortalidade Ib. Comparative studies of the dispersal and the para populações de Biomphalaria glabrata e vagility capabilities of Biomphalaria glabrata B. straminea, criadas em condições and B. straminea. Memorias do Instituto Oswal- do Cruz, 79: 163-167. semi-naturais, são descritas no presente , 1985. Competitive interactions bet ween trabalho. As populações dos caramujos foram species of freshwater snails. I Laboratory studies. observadas durante 220 semanas em canaletas Ic. Comparative survival of Biomphalaria de cimento montadas no laboratório. Dados glabrata and B. straminea kept out of water. foram coletados a cada intervalo de 20 Memorias do Instituto Oswaldo Cruz, 80: 155- semanas. As densidades brutas de crescimento 157. foram significantemente diferentes para cada COIMBRA Jr., C. E. A., 1991. Biological Control população estudada. B. glabrata mostrou for Fresh water snails. Letters to the Editor. crescimento inferior às duas cepas de B. Today, 7: 124. straminea. A cepa R3 desta última espécie GUYARD, A. & POINTIER, J. P., 1979. Faune mostrou o melhor desempenho, sendo capaz malacologique dulciaquicole et vecteurs de la de viver em metade do volume de água schistosomose intestinale en Martinique. Annales necessária a B. glabrata quando ambas estão de Parasitologie, 54: 193-205. submetidas a pressão populacional. HAIRSTON, N. G., SMITH, F. E., & SLOBODKIN, L. B., 1960. Community structure, population Palavras-Chave: Dinâmica de Populações de control and competition. The American Natural- Caramujos; Deslocamento Competitivo; ist, 94: 421-425. Biomphalaria; Brasil MADSEN, H., 1990. Biological Methods for the Control of Freshwater Snails. Parasitology Today, 6: 237-241. REFERENCES MICHELSON, E. H. & DUBOIS, L., 1979. Com- petitive interaction between two snail hosts of ARMITAGE, P., 1974. Statistical Methods in Medi- : laboratory studies of cardl Research. Blackwell Scientific Publications, Biomphalaria glabrata and B. straminea. Revista 3 edition. Oxford: Great Britain. do Instituto de Medicina Tropical de São Paulo, BARBOSA-FIGUEIREDO, C., 1989. Interações 21: 246-253. entre especies de Biomphalaria, moluscos trans- WORLD HEALTH ORGANIZATION, 1987. Report missores da esquistossomose no nordeste do on a informal consultation on the detection, Brasil. MSC Thesis, João Pessoa: Universidade isolation, identification and ecology of biological Federal da Paraíba. agents of disease vectors. TDR/BCV/IC-GE/87.3. BARBOSA, F. S., 1973. Possible competitive dis- YIPP, M. W., 1990. Distribution of the schistoso- placement and evidence of hybridization, be- mose vector snail Biomphalaria straminea (Pul- tween two Brazilian species of planorbid snails. monata, ) in Hong Kong. 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