Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(1): 119-128, Jan./Feb. 1996 119 Thermal Effect on the Life-cycle Parameters of the Medically Important Freshwater () luteola (Lamarck) Md Abdul Aziz, SK Raut Ecology and Ethology Laboratory, Department of Zoology, University of Calcutta, 35 Ballygunge Circular Road, Calcutta 700 019, India The Lymnaea (Radix) luteola exhibited marked variations in growth, longevity, and attaining sexual maturity at different temperatures and diets. At 10°C, irrespective of foods, pH and salinity of water, the snails had minimum life span, maximum death rate and lowest growth rate. At 15°C, the growth rate was comparatively higher and the snails survived for a few more days. But at these tem- peratures they failed to attain sexual maturity. Snails exposed to pH 5 and 9 at 20°, 25°, 30°, 35°C and o room temperatures (19.6°-29.6°C); to 0.5, 1.5 and 2.5 NaCl ‰ at 20° and 35 C; to 2.5 NaCl ‰ at 25°C and room temperatures failed to attain sexual maturity. The snails exposed to pH 7 and different salinity grades at 20°, 25°, 30°, 35°C and room temperatures became sexually mature between 25-93 days depending upon the type of foods used in the culture.

Key words : Lymnaea (Radix) luteola - life-cycle parameters - temperature - food - pH - salinity - India

Lymnaeids are distributed worldwide (Godan available information is based on the results of 1983). They have drawn the attention of a large experimental studies considering only a single number of researchers because of their role as hosts factor (Vaughn 1953, Prinsloo & Van Eden 1969, for larval stages of the helminth parasites which 1973, Van der Borght & Van Puymbroeck 1971, cause disease in man and domestic (Liston Raut & Misra 1991,1993, Raut et al. 1992, Saha & Soparkar 1918, Rao 1933, Chatterjee 1952, & Raut 1992) it has not been possible to regulate Malek & Cheng 1974, Ghosh & Chauhan 1975, the density of these snails through the application Godan 1983, Burch 1985, Raut 1986). Consider- of these results. Accordingly, the present study was ing their involvement in regulating the life-cycle designed to collect detailed information on the life- of the worm parasites various aspects of the biol- cycle parameters viz., the growth rates, the age of ogy and ecology of these freshwater gastropod attainment to sexual maturity, the duration of re- snails were studied by Seshaiya (1927), Noland productive period, the rate of egg production, the and Carriker (1946), Kendall (1953), McCraw death rate and the life span of Lymnaea (Radix) (1970), Berrie (1965), Burla and Speich (1971). luteola (Lamarck), in order to consider the cu- Van der Steen et al.(1973), Hunter (1975) Raut et mulative effects of these different ecological pa- al. (1992), Raut and Misra (1993), and Misra and rameters. Since Lymnaea are adapted to a wide Raut (1993) with a view to developing methods range of temperatures (Walter 1968, Prinsloo & for control. Although additional information on Van Eeden 1969) the aim was to study the effect ecology of lymnaeids is available (Jong-Brink of temperature on the snails L. (R.) luteola under 1990, Moens 1991) an effective control device for varying ecological conditions such as food, water these snail intermediate hosts has not been found. pH and salinity (NaCl). The findings are presented Since the status of individuals of a species is largely herein. determined by the physical, chemical and biologi- MATERIALS AND METHODS cal parameters of the ecosystem to which they be- long it is most likely that a study on the cumula- Eighty-one healthy, sexually mature L. (R.) tive influence of these factors would provide us luteola were collected from the pond located in better information on the subject. As most of the the Ballygunge Science College campus, Calcutta University on 18 March 1991. They were released into an aquarium 30 x 20 x 25 cm, containing pond water, 20 cm in depth. A few examples of This work received financial support from the Muslim Chara, Vallisneria and Ipomoea were also released Association for the Advancement of Science (MAAS), into the water of the aquarium to provide resting India. Received 30 June 1994 and egg laying sites for the snails. The snails were Accepted 10 October 1995 regularly supplied with leaves, as food. The 120 Thermal Effect on the Snail Lymnaea luteola • A Aziz, SK Raut snails started egg-laying within a few days. The capsules was also counted and recorded. In all egg capsules were collected on a daily basis from cases the average was calculated for presentation the aquarium, and kept inside a glass jar (1000 ml of final data in respect to the life-cycle parameters capacity) containing pond water. In one glass jar considered for study. One-way ANOVA was ap- 7-10 egg capsules deposited within a 24 hr pe- plied for statistical interpretations of the data. riod, were kept together. The water in the glass Detailed comparisons of the data by way of jars was changed regularly with fresh pond water. ANOVA studies were made following Campbell Through regular observation newly hatched (1989). (zero-day-old) snails were taken daily from the jars. RESULTS The required number of individuals, when avail- L. (R.) luteola had different life spans (5.43 - able, were studied. These newly hatched snails 64.82 days) when cultured at different tempera- were placed in a plastic container (2 1 capacity) tures in respect to the type of food they consumed containing pond water. The containers were kept (Fig. 1) and the pH and salinity of the mainte- at 10°, 15°, 20°, 25°, 30°and 35°C (± 1°C) tem- nance water (Fig. 2). They exhibited marked varia- peratures (maintained in Biological Oxygen De- tion in the rates of growth, in shell length, shell mand Chamber), and at room temperature (19.6°- breadth and body weight when reared at different 29.6°C) in order to study the effect of these tem- temperatures (Fig. 3). In general, body weight in- peratures on the L. (R.) luteola. The experiments creased with the increase of temperature from 10° were conducted (i) using five different types of to 35°C, at intervals of 5°C. But the snails attained food viz. lettuce (Lactuca sativa), mustard (Bras- maximum body weight per day when maintained sica nigra), radish (Raphanus sativus), at room temperatures. Though a similar trend in (Spinacea oleracea) and aquatic weeds (Chara, the growth rates in shell length and shell width is Vallisneria), (ii) by maintaining three different lev- noted in snails maintained from 10° to 30°C, slight els of pH, viz. 5, 7 and 9 in the culture water and variations in the rate of increase were seen in in- (iii) by maintaining three different grades of sa- dividuals exposed to 35°C and room temperatures. linity viz 0.5, 1.5 and 2.5 NaCl ‰. The snails The snails cultured at 35°C with mustard leaves under experimental study with different pH and attained maximum shell size (16 mm in shell salinity grades were fed lettuce. The water in the length and 10 mm in shell width). In contrast to containers was changed regularly at an interval of this the lettuce fed individuals exposed to 30°C at 12 hr in order to maintain the pH and salinity at 0.5 NaCl ‰ attained maximum body weight (4.20 desired levels. The pH was maintained by adding mg) having 15 mm shell length and 9 mm shell HCl and NaOH, and the salinity was maintained width. by adding HCl to the freshly collected pond water Among the snails exposed to 10°C and 15°C, at an interval of 12 hr. A few examples of Ipomoea irrespctive of the type of food, pH and salinity of were kept in each container to provide resting and water, and those cultured at pH 5 and 9, irrespec- egg-laying sites for the snails. Dead snails’ faecal tive of temperatures, died prior to attaining sexual pellets and unconsumed food materials were re- maturity (Figs 1, 2). The snails in the remaining moved every 12 hr, at the time of removal of wa- cultures became sexually mature between 25 and ter in each container. 93 days after hatching and the percentages of such Data on the life-cycle parameters viz. the snails varied from 6.70 to 70.00 (Figs 1, 2). Indi- growth rates, the age of attainment of sexual ma- viduals maintained at 1.5 NaCl ‰ under room turity, the duration of reproductive period, the rate conditions with lettuce as food, reproduced on an of egg production, the death rate and the life span average, only for a period of 8 days, while those of the snails was collected regularly. In the course reared at 20°C with radish leaves as food repro- of data collection, attention was paid to record the duced for a period of 61.50 days (Figs 1, 2). The time taken by the eggs to hatch and the hatchabil- rate of egg production varied with the snails in ity percentage of the eggs, exposed to different tem- respect to the cultures maintained (Figs 1, 2). At peratures. Measurements of growth in shell length, room temperature, a lettuce fed snail on an aver- shell width and total body weight were taken ev- age deposited 0.27 eggs per day but the number ery two weeks, from ten individuals, selected at was as high as 18.35 in case of lettuce fed snails random, from the total population. But, when the cultured with 2.5 NaCl ‰ at 30°C. The eggs number was ten or less, all were considered for diposited by the snails of different culture stocks data collection. In the case of the study of egg- required, on an average, 7.0 to 10.50 days to hatch laying potential, the total number of egg capsules out (Figs 1, 2). The percentage of hatching was produced by the snails in the container were re- highest (96.20%) in eggs deposited by lettuce fed corded daily. The number of eggs present in these snails kept at room temperature and lowest Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(1), Jan./Feb. 1996 121

Fig. 1: influence of temperature on the life cycle parameters [a: longevity (in days), b: age of attainment of sexual maturity (in days), c: length of reproduction period (in days), d: snails attained sexual maturity (in per cent), e: rate of egg production (in number), f: developmental period of egg (indays), g: hatchability of egg (in per cent ) ] of Lymnaea (Radix) luteola maintained with five different types of food. 122 Thermal Effect on the Snail Lymnaea luteola • A Aziz, SK Raut

Fig. 2: influence of temperature on the life cycle parameters [a: longevity (in days), b: age of attainment of sexual maturity (in days ), c: length of reproduction period (in days), d: snails attained sexual maturity (in percent), e: rate of egg production (in number), f: developmental period of egg (in days), g: hatchability of egg (in per cent )] of Lymnaea (Radix) luteola maintained at different pH and salinity with the supply of lettuce food.

(43.70%) in eggs produced by weed fed snails ex- effect of all other higher temperatures in respect posed to 20°C (Figs 1, 2). Marked variations have to 10°C were made by applying ANOVA, to de- been noted in mortality rates of the snails exposed termine the optimum temperature for growth, re- to different temperatures. The average daily death production and development. From the F values rate ranged from 0.28% to 2.72% (Table I). The (Table II-IV) it is evident that temperature has sig- snails exhibited the lowest growth rate at 10°C. nificant effect on these events in L. (R.) luteola in An increasing rate of growth is evident with the respect to the type of foods used and the pH and rise of temperature. Detailed comparisons on the salinity grades maintained. Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(1), Jan./Feb. 1996 123

Fig. 3: influence of temperature on the daily rates of growth in shell length (mm), shell breadth (mm) and body weight (mg) of Lymnaea (Radix) luteola maintained with different foods (a: lettuce, b: mustard, c: radish, d: spinach, e :weed), pH (f : 5, g : 7, h: 9 ) and salinity (k: 0.5 NaCl ‰, m: 1.5 NaCl ‰, p: 2.5 NaCl ‰ ). 124 Thermal Effect on the Snail Lymnaea luteola • A Aziz, SK Raut

TABLE I Influence of temperature on the death rates (avarege % per day) of Lymnaea (Radix) luteola Temperature Food pH Salinity (NaCl‰) (°C) Lettuce Mustard Radish Spinch Weed 5 7 9 0.5 1.5 2.5 10 1.00 0.61 1.33 1.42 0.64 1.00 0.68 1.20 0.88 0.96 1.30 15 0.63 0.56 0.51 0.57 0.60 1.07 0.75 1.15 0.71 0.96 1.07 20 0.33 0.36 0.33 0.38 0.33 1.07 0.49 1.36 0.56 0.65 0.76 25 0.34 0.38 0.33 0.33 0.28 1.20 0.35 1.57 0.68 0.71 0.85 30 0.68 0.60 0.50 0.42 0.45 2.00 0.50 2.72 0.51 0.48 0.46 35 0.62 0.71 0.85 0.54 0.32 2.14 0.50 2.14 0.32 0.35 0.40 Room 0.60 0.55 0.75 0.45 0.39 2.14 0.52 2.50 0.76 0.83 1.16

DISCUSSION 30°, 35°C and room temperatures) irrespective of Temperature is considered as a critical envi- foods is significant at 0.1 % level. From the F ronmental factor in the ecology of most organisms values, it appears that the degree of interaction is (Precht et al. 1973, Magnuson et al. 1979, Vianey- almost at the same level as far as the results of Liaud 1982, Ahmed & Raut 1991, Raut et al. 35°C and room temperatures are concerned. 1992). It can act as both a trigger for the com- Though the effect of temperature on the age of mencement of a biological process and as a thresh- attainment of sexual maturity in snails is signifi- old essential for its continuation. The results of cant at 0.1% level throughout, the degree of inter- the present study are in agreement with the com- action is gradually higher with the rise of tem- ment of previous workers so far as the influence perature from 20° to 35°C and the impact of room of temperature on the biology of L.(R.) luteola is temperature lies in between 30° and 35°C. In con- concerned. It is evident that L. (R.) luteola is un- trast to this, the effect of 30°C is highly signifi- able to complete its life-cycle at 10° and 15°C cant as far as the duration of reproduction of a temperatures, irrespective of the foods it consumes, snail individual is concerned. However, room tem- and the pH and salinity grades maintained. Also, perature has its biggest effect on the rate of egg it fails to attain sexual maturity at 25°C, 30°C, production, the time required for the development 35°C and room temperatures when fed weed, at of embryo and the hatchability of eggs. It seems all the temperature gradients when maintained that even under all other similar factors, tempera- with lettuce at pH 5 and 9, and at 20° and 35°C ture plays a significant role to regulate the physi- in all the three salinity grades, and at 25°C and ology of the snails. As the physiological status of room temperatures when the snails were exposed an organism depends greatly on the available food, to 2.5 NaCl ‰ with the supply of lettuce food. In it is obvious that the life-cycle parameters of snails these experiments the snails exhibited marked would vary accordingly. This is dependent on the variations in the rates of growth in shell length, rate of feeding and conversion of carbohydrate, shell breadth and body weight. In all other ex- protein and fat from plant food sources, to snails’ periments the snails were able to complete their body, at various temperatures, as has been dis- life-cycle although significant variations in the cussed by Ahmed and Raut (1991). Since anoma- rates of growth, multiplication and survival have lies in longevity in snails cultured at different pH been noted in respect to the temperatures of the and salinity of water are well marked at identical waters of the containers concerned. Also, in most temperatures with identical food supply (lettuce) cases the effects of temperature on the life-cycle it is assumed that, at least pH and salinity (since parameters of L. (R.) luteola are influenced by the other factors have not been considered in the factors like quality of food, pH, and salinity of wa- present study) play important roles in the life pro- ter used in experiments. Detailed comparisons in cess. This is why the snails cultured at pH 5 and respect to 10°C revealed that the effect of 15° and 9 in all the temperatures and those cultured in 0.5, 20°C is significant while at 25°, 30°, 35°C and 1.5 and 2.5 NaCl ‰ at 20° and 35°C, in 2.5 NaCl room temperature the same is significant either at ‰ at 25°C and room temperature failed to attain 5% or 1% or 0.1% level when the snails were cul- sexual maturity. Since the percentage of sexually tured in waters having three different salinity mature snails varied with the thermal conditions grades but fed with lettuce. of the water used in cultures, it is apparent that The overall effect of temperatures (20°, 25°, adaptability in snails varied with the individuals. Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(1), Jan./Feb. 1996 125 a d d d d d d d d d c d d d d d d d d d d NS d d d d b d cultured with : not significant C v RT o 323.2248 170.19813 65.95603 178.94451 194.0626 63.8118 75.63445 50.73142 24.3467 163.70434 65.3266 32.9967 114.0885 79.3458 34.9871 75.8209 43.4538 54.2077 52.47208 39.4916 3.77305 38.8243 60.6506 10.29576 70.6467 97.9838 6.96791 NS C10 d d d d o d d d d d d d d d d d d d d d d d d d d d d d C v 35 o 448.8681 234.34443 27.27309 311.42371 385.6348 20.9362 126.6030 112.65847 13.30939 255.05248 117.4598 13.19195 88.8232 58.2948 21.0454 191.3543 142.165 12.5923 128.2756 1085474 40.55779 71.9048 90.2399 31.09833 128.9706 170.8553 55.82649 Lymnaea (Radix) luteola Lymnaea ht of C10 d d d d d d o d d d d d d c d d d NS d d d d d c c d NS b C v 30 o 519.40841 220.69628 14.83858 82.9343 109.3454 8.73583 26.61654 21.24049 3.58918 296.28782 117.4598 5.7244 11.51149 2.5301 10.1250 13.8420 13.3263 14.7600 131.00964 101.76491 59.01068 61.2116 100.2592 41.183069 54.5528 64.7401 12.00418 C10 d o d d c d d d d d c d d : significant at 5,1 and 0.1% levels, respectively b d NS d d d d d NS d NS NS NS b b b, c, d

C v 25 o 83.838 54.61535 6.76323 69.62724 84.9382 10.14991 19.12287 14.21884 1.25135 17.92859 1.2147 0.2517 98.5504 58.2948 29.2403 6.1193 4.7515 3.6585 77.52049 55.38133 12.02545 46.1463 58.0140 18.040039 36.04426 45.17622 2.23176 C ) o C10 o d NS NS NS C - 29.6 d d c NS c NS NS NS NS NS NS b b o d NS c NS c c c NS NS b TABLE II TABLE C v 20 o 14.008 12.56198 0.092188 7.29835 12.3147 0.08148 5.79649 4.99317 0.06106 7.37351 0.3036 0.03679 7.6427 6.4772 0.5217 9.1678 8.4981 9.5800 1.25166 0.092266 1.31833 0.068992 1.04765 1.6001 0.07325 NS C10 o NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS C v 15 : Room temperature (19.6 o a 0.54048 0.36395 0.0000017 0.63236 1.6284 0.0015 0.29211 0.17554 0.00057 2.37716 1.6534 0.0071 0.06316 0.0253 0.0095 1.1685 1.3529 0.0236 0.52054 0.000.001892 0.000.10986 0.000143 0.81813 1.19731 0.89605 0.00262 0.8889 d d d d d d d d d d d d d d d d d d d d d d d d d d d C )10 o ( Overall F - values temperature different food, pH and salinity. The snails considered for experiments with pH and salinity grades were fed lettuce food, pH and salinity. different SLSL 58.4309 64.6700 SBBWSBBW 106.061 23.87437 SBBW 115.5086 20.069 SBBW 70.5185 20.0286 SBBW 115.0946 19.6597 29.7185 13.0963 BW 17.1293 BWSLBW 30.3721 SL 34.1543 BW 24.68056 60.5464 26.7642 Lettuce SL 232.9599 Mustard SL 99.8607 Weeds SL7 43.6548 SB 41.2814 Radish SLSpinach SL 84.4485 196.288 0.51.5 SB2.5 SB 54.2044 SB 47.0703 79.3267 Calculated F-values in respect to the effect of temperature on the rates growth in shell length, breadth and body weig Calculated F-values in respect to the effect FOOD pH SALINITY body weight SL: shell length, SB: breadth, BW: 126 Thermal Effect on the Snail Lymnaea luteola • A Aziz, SK Raut

TABLE III Calculated F-values in respect to the effect of temperature on the longevity and mortality of Lymnaea (Radix) luteola maintained with different foods, pH and salinity Over all F - values temperature (oC ) 10oC v 15oC10oC v 20oC10oC v 25oC10oC v 30oC10oC v 35oC10oC v RTa Longevity Food 194.2927d 20.2881d 48.6286d 87.3681d 9.0907d 25.0906d 9.9420d pH 0.23739NS ------Salinity 4.05357c 0.12208NS 0.0931NS 11.2378d 6.0556c 3.9789b 4.88203c Mortality Food 7.48837d 14.6540d 34.5377d 36.0323d 8.1424d 12.4082d 6.4974d pH 0.7373NS ------Salinity 4.5821c 0.7771NS 6.6492c 3.9344b 13.8731d 20.8134d 0.7388NS a: room temperature ( 19.6oC - 29.6oC ) b, c, d: significant at 5, 1 and 0.1% levels, respectively NS: not significant - : did not compare due to overall insignificant effect

TABLE IV Calculated F-values in respect to the effect of temperature on the life cycle parameters of Lymnaea ( Radix ) luteola Overall F - values Life cycle parameters temperature (o C ) 20oC v 25oC20oC v 30oC20oC v 35oC20oC v RTa Age of attainment of sexual maturity 11.9278d 10.9894d 29.9788d 31.7239d 27.4537d Percentage of snails attained sexual maturity 21.40902d 34.7113d 58.4479d 54.4861d 46.3688d Length of reproduction period 5.81155c 3.2484b 8.4108d 3.0781b 0.1123NS Rate of egg production 5.11786c 4.6144c 0.0234NS 2.1071NS 5.2031c Developmental period of eggs 28.0615d 21.8266d 18.2256d 75.6797d 82.8493d Hatchability percentage of eggs 21.4329d 28.4455d 17.2704d 6.2343c 78.4124d a: room temperature (19.6oC - 29.6oC) b, c, d: significant at 5,1 and 0.1% levels, respectively NS: not significant

Such adaptability of the snails has been reflected of the incubation period of the eggs and the per- in the length of the reproduction period and the centage of hatching of eggs in respect to tempera- rates of egg production. This phenomenon is also ture have been noted in Lymnaea luteola, L. well evident from the facts of variations in the acuminata, I.exustus and Gyraulus convexius- length of the reproduction period and in the rates culus (Saha & Raut 1992). The present findings of egg production in snails exposed to 1.5 and 2.5 are in agreement with earlier observations al- NaCl ‰. Similar effects of temperature on the rate though variations in hatching percentages of the of growth, reproduction, and behaviour have been eggs produced by the snails, reared at the same noted in by Vaughn (1953), in temperature, but fed with different foods, are re- Australorbis glabratus by Michelson (1961), in corded for the first time. This may be explained (Physopsis) globosus by Shiff (1964), in by the relationship of stored nutrients in the eggs, by Sturrock (1966) and to the type of foods consumed by the mother snails Appleton (1977), in Biomphalaria glabrata by concerned. As hatching success of the eggs varied Chernin (1967), Sturrock and Sturrock (1972) and with the pH and salinity grades it is obvious that Vianey-Liaud (1982), in Biomphalaria pfeifferi by these factors have significant influence to alter the Shiff and Garnett (1967), in Bulinus truncatus and beneficial effects of temperature, to a certain ex- Biomphalaria alexandrina by El-Hassan (1974) tent. The present observations provide a sound and in exustus by Raut et al. (1992). basis for understanding the findings of The rate of population growth of a species is Chitramvong et al. (1981) on Bithynia siamensis very much governed by the length of the incuba- siamensis , and Indoplanorbis tion period and hatchability of its eggs (if the spe- exustus and of Raut and Misra (1991, 1993) on L. cies is oviparous) . Marked variations in the length (R.) luteola, I.exustus and Gyraulus convexius- Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(1), Jan./Feb. 1996 127 culus . Ghosh RK, Chauhan BS 1975. Fifty years of faunis- From the foregoing accounts it appears that tic survey in India. Rec zool Surv Ind 68: 367-381. the potential of an organism is very much depen- Godan D 1983. slugs and snails. Springer-Verlag, dent on its ability to adjust to the factors to which Berlin, Heidelberg, New York vi + 445 pp. it is exposed. Further, it may be stated that the Hunter RD 1975. Growth, fecundity and bioenerget- power of adjustment of an organism is determined ics in three population of Lymnaea palustris in upstate New York. Ecology 56: 50-63 by its ‘genome’ (Boughey 1973) or ‘dynamic’ Jong-Brink M De 1990. How trematode parasites in- (Misra & Raut 1993) factor. Depending upon these terfere with reproduction of their intermediate factors, the trend of population growth rate in a hosts freshwater snails. J Med Appl Malacol 2: species as well as the probability of variations in 101-133. ‘strain’ are determined. Such studies, from dif- Kendall SB 1953. The life history of Lymnaea ferent parts of the globe, although numerous (New- truncatula under laboratory conditions. Helminth ton 1955, Paraense 1955, Richards 1973, Scherrer 27: 17-28 . et al. 1976, Vianey-Liaud 1989, Misra & Raut Liston WG, Soparkar MB 1918. Bilharziasis among 1993), are lacking information on the cumulative animals in India. The life-cycle of Schistosomum effect of different ecological parameters in respect spindalis. Ind J Med Res 5: 567-569. to the strains of the snail species. Magnuson JJ, Crosder LB, Medvick PA 1979. Tem- perature as an ecological resource. Amer Zool 19: ACKNOWLEDGEMENTS 331-343 . To the Head, Department of Zoology, University of Malek EA, Cheng TC 1974. Medical and Economic Calcutta, for providing the necessary facilities. Malacology. Academic press, New York, London, 408 pp. REFERENCES McCraw BM 1970. Aspects of the growth of the snail Ahmed M, Raut Sk 1991. Influence of temperature on Lymnaea palustris ( Muller ). Malacologia 10: the growth of the pestiferous land snail Achatina 399-413 . fulica ( : Achatinidae). Walkerana 5: Michelson EH 1961. The effects of temperature on 33-62 . growth and reproduction of Australorbis glabratus Appleton C 1977. Review of literature on abiotic fac- in the laboratory. Am J Hyg 73: 66-74 . tors influencing the distribution and life cycles of Misra TK, Raut SK 1993. Dynamic of population- bilharziasis intermediate snails. Malacol Rev dynamics in a medically important snail species 11: 1- 125. Lymnaea (Radix) luteola (Lamarck). Mem Inst Berrie AD 1965. On the life cycle of Lymnaea stagnalis Oswaldo Cruz 88: 469-485 . (L.) in the west of Scotland. Malacol Soc London Moens R 1991. Factors affecting Lymnaea truncatula Proc 36: 283-295. populations and related control measures. J Med Boughey AS 1973. Ecology of population. 2nd ed. Appl Malacol 3: 73-84 . Macmillian Publishing Co. Inc., New York, x + 182 Noland LE, Carriker MR 1946. Observations on the pp. biology of the snail Lymnaea stagnalis appressa Burch JB 1985. Handbook on schistosomiasis and other during twenty generations in laboratory culture. snail-mediated diseases in Jordan. University of Amer Midland Naturalist 36: 467-493 . Michigan. Ann. Arbor, Michigan U.S.A. and Min- Newton WL 1955. The establishment of a strain of istry of Health, Amman Jordan, i-xv, 224 pp. Australorbis glabratus which combines albinism Burla H, Speich C 1971. Lymnaea auricularia and and high susceptibility to infection with Lymnaea ovata im Zürichsee. Rev Suisse Zool 78: mansoni. J Parasitol 41: 526-528 . 549-556. Paraense W 1955. Self and cross-fertilization in Campbell RC 1989. Statistics for biologists. 3rd ed. Australorbis glabratus. Mem Inst Oswaldo Cruz Cambridge University Press, Cambridge xvii+445 pp. 53: 285-291. Chatterjee KD 1952. Human parasites and diseases. Precht H, Christopherson J, Hensel, H, Larcher A The World Press Ltd. Calcutta vi + 776 pp. 1973. Temperature and life. Springer-Verlag, Ber- Chernin E 1967. Behaviour of Biomphalaria glabrata lin xi + 315 pp. and other snails in a thermal gradient. J Parasitol Prinsloo JF, Van Eeden JA 1969. Temperature and its 53: 1233-1240. bearing on the distribution and chemical conrol of Chitramvong YP, Upathan ES, Sukhapanth N 1981. freshwater snails. S Afr med J 43:1363-1365 . Effect of some physico-chemical factors on the Prinsloo JF, Van Eeden JA 1973. The influence of tem- survival of Bihynia siamensis siamensis, Radix perature on the growth rate of Bulinus (Bulinus) rubiginosa and Indoplanorbis exustus. Malacol tropicus (Krauss) and Lymnaea natalensis Rev 14: 43- 48 . (Krauss) (:Basommatophora). Malaco- El-Hassan A 1974. Laboratory studies on the direct logia 14: 81-88. effect of temperature on Bulinus truncatus and Rao MAN 1933. A preliminary report on the success- Biomphalaria alexandrina, the snail intermediate ful infection with nasal schistosomiasis in experi- hosts of schistosomes in Egypt. Folia Parasitol mental calves. Ind J Vet Sci Anim Husb 3: 160-162. Czechol 21: 181-187 . Raut Sk 1986. Snails and slugs in relation to human 128 Thermal Effect on the Snail Lymnaea luteola • A Aziz, SK Raut

diseases. Environment Ecology 4: 130-137. (Krauss) ( : ). Arch Hydrobiol Raut SK, Misra TK 1991. Effect of salinity on the 62 : 429-438. growth of three medically important snail species. Sturrock RF 1966. The influence of temperature on the Boll Malacologico ROC 16 : 67-74. biology of Biomphalaria pfeifferi (Krauss), an Raut SK, Misra TK 1993. Influence of salinity on the intermediate host of Schistosoma mansoni. Ann breeding of three medically important freshwater Trop Med & Parasitol 60: 100-105. snail species (Gastropoda : Basommatophora: Sturrock RF, Sturrock BA 1972. The influence of tem- et Planorbidae). Malakol Abh Mus perature on the biology of Biomphalaria glabrata Tierkd Dresden 16 : 173-176. (Say), intermediate host of Schistosoma mansoni Raut SK, Rahaman MS, Samanta SK 1992. Influence in St. Lucia, West Indies. Ann Trop Med Parasitol of temperature on survival, growth and fecundity 66: 385-390. of the Indoplanorbis exustus Van Der Borght SCK, Van Puymbroeck S 1971. Kinet- (Deshayes). Mem Inst Oswaldo Cruz 87: 15-19. ics of the direct uptake of Ca and Sr ions from Richards CS 1973. Pigmentation variations in water by freshwater Gastropods : Influence of Biomphalaria glabrata and other Planorbidae. temperature. Environ Physiol 1: 83-95. Malacol Rev 61: 49-51. Van Der Steen WJ, Jager JC, Timersma D 1973. The Saha TC, Raut SK 1992. Bioecology of the water-bug influence of food quality on feeding, reproduction Sphaerodema annulatum Fabricius. Arch Hydrobiol and growth in the pond snails Lymnaea stagnalis 124: 239-253. (L.) with some methodological comments. Proc K Scherrer JF, de Chquilof MAG, Freitas JR 1976. Med Akod Wet (Ser. C) 76: 47-60. Estudo comparativo da reprodução em quatro Vaughn ChM 1953. Effects of temperature on hatch- variedades genéticas de Biomphalaria glabrata ing and growth of Lymnaea stagnalis appressa Say. (Say, 1818). I-Fecundidade. Rev Inst Med Trop S Amer Midland Naturalist 49: 214-228. Paulo 18: 315-321. Vianey-Liaud M 1982. Effects des hautes temperatures Seshaiya RV 1927. On the breeding habits and fecun- sur la reproduction de Biomphalaria glabrata dity of the snail Lymnaea luteola Lamarck (Forma- (Mollusca: Basommatophora). (Proc 7th Intern typica). J Bombay nat Hist Soc 32: 154-158. Malacol Congr). Malacologia 22: 159-165. Shiff CJ 1964. Studies on Bulinus (Physopsis) globosus Vianey-Liaud M 1989. Growth and fecundity in a black- in Rhodesia. II. Factors influencing the relation- pigmented and an albinostrain of Biomphalaria ship between age and growth. Ann Trop Med glabrata (Gastropoda : Pulmonata). Malacol Rev Parasitol 58: 106-115. 22: 25-32. Shiff CJ, Garnett BG 1967. The influence of tempera- Walter HJ 1968. Evolution, revolution and ture on the intrinsic rate of natural increase of zoogeography of the Lymnaeidae. Amer Malacol the freshwater snail Biomphalaria pfeifferi Union Ann Rep 35: 18-20.