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PREDATOR AVOIDANCE IN BULINUS GLOBOSUS (MORELET, 1866) AND B. TROPICUS (KRAUSS, 1848) (GASTROPODA: PLANORBIDAE) EXPOSED TO PREDATORY AND NON-PREDATORY FISH PAUL MAKONI 1 , MOSES J. CHIMBARI 2 , 4 AND HENRY MADSEN 3 1 De Beers Research Laboratory, Box 197, Chiredzi, Zimbabwe; 2Blair Research Laboratory, PO Box CY 573, Causeway, Harare, Zimbabwe; 3 Danish Bilharziasis Laboratory, Jaegersborg Allé 1d, DK2920 Charlottenlund, Denmark; 4 Present address: University of Zimbabwe Lake Kariba Research Station, PO Box 48, Kariba, Zimbabwe (Received 25 November 2002; accepted 1 March 2004) ABSTRACT The cichlid fish, Sargochromis codringtonii, has been suggested for biological control of freshwater snails, especially those serving as intermediate hosts for schistosomes. This study examined the behaviour of two aquatic snail species, Bulinus globosus and Bulinus tropicus, when exposed to water conditioned (defined as water inhabited by fish) by either Sargochromis codringtonii, a molluscivore, or Tilapia rendalli (Boulenger, 1896), a herbivore, and when exposed to predation risk in the presence of a refuge. Both snail species crawled above the waterline to a greater extent when exposed to water conditioned by S. codringtonii than when exposed to water conditioned by T. rendalli, or unconditioned water. Although the number of snails leaving the water tended to increase with the density of S. codringtonii, this was not statistically significant. While Bulinus globosus elicited a greater response to water conditioned by feeding fish than to that conditioned by non-feeding fish, B. tropicus did not respond differently to the two treatments. The introduction of S. codringtonii into tanks with a refuge caused snails to move actively into the covered areas. INTRODUCTION Snails may have morphological features or behavioural patterns that make it possible for them to coexist with their predators (Vermeij, 1974; Vermeij & Covich, 1978). The morphological features include thick protective shells and an operculum. These special morphological features may have evolved during the many years of coexistence of snails and their predators (Vermeij, 1974; Vermeij & Covich, 1978; Palmer, 1979). Snails can escape predation if they are too large for the predator to consume or if their shells are too thick to crush (Osenberg & Mittelbach, 1989). Most freshwater snails are generally less well adapted to avoid crushing from predators than most marine forms, with shells that are generally thinner than those of marine species. Instead, many thin-shelled pulmonates have behavioural adaptations that aid them in avoiding predators (Vermeij & Covich, 1978). The predator avoidance response of snails is a behavioural pattern that has been demonstrated in several studies (Covich, 1981; Alexander & Covich, 1991). Freshwater snails display several predator avoidance strategies that include burrowing into the sediment, crawling into vegetation or above the waterline, or vigorous movements of the shell upon contact (Alexander & Covich, 1991; Turner, 1996). Alexander & Covich (1991) observed a tendency by Physella virgata (Gould) and Planorbella trivolis (Say) to crawl above the waterline in response to the presence of the crayfish Procambarus simulans. Likewise, the presence of Procambarus clarkii caused Physa acuta Draparnaud to crawl above the waterline (Hofkin et al., 1991). The behavioural response of snails in the presence of predators may be due to the presence of the predator, disturbances due to attempted attacks by the predator, or fluids from crushed conspecific snails. Chimbari (1996) found an increased tendency for Bulinus globosus to leave water that had been conditioned by Sargochromis codringtonii. Correspondence: H. Madsen; e-mail: [email protected] J. Moll. Stud. (2004) 70: 353–358 The aim of the present study was to investigate the behaviour of Bulinus globosus and Bulinus tropicus in the presence of Sargochromis codringtonii (a molluscivore) and Tilapia rendalli (a herbivore), presence of different densities of Sargochromis codringtonii and whether feeding by fish influenced this behaviour. The study also investigated if snails would move into protected areas in the presence of a predator. MATERIAL AND METHODS Response of snails to water conditioned by fish The three experiments involved supplying water conditioned by fish, or unconditioned water, from large aquaria to snails in small test containers. Because the chemicals released by the conditioning fish could be volatile in water, the test containers received water continuously from the fish aquaria. Initially, tap water was put into an outdoor concrete pond and left to dechlorinate for 2 days. After dechlorination the water was pumped into five large aquaria (100 cm long and 60 cm wide and high). The aquaria were filled to 75% capacity. The water in the big tanks would either be conditioned by the addition of fish or left unconditioned. The water was conditioned by fish for two days prior to conducting the experiment. Each of the large aquaria continually supplied water to 10 500-ml plastic containers through siphoning tubes. A hole was punched into one side of the test containers to allow for a constant volume of water. At any given time each plastic containers held 370 ml of water. The rate of flow of the water was 0.13 cm3 per second per test container, which meant that water in test containers was replaced about 10 times during an 8-h period. Water was not added to the large aquaria during the experiments. The S. codringtonii fish used in the experiment had standard lengths (from snout tip to base of caudal peduncle) of 13–14 cm and total wet weights from 50 to 56 g. Tilapia rendalli, an herbivorous cichlid species, was used for comparison in experiment 1 and had standard lengths ranging from 13.0 to 14.5 cm and Journal of Molluscan Studies Vol. 70, No. 4 © The Malacological Society of London 2004, all rights reserved. P. MAKONI ET AL. wet weights from 63 to 71 g. Laboratory-bred Bulinus globosus and B. tropicus with shell heights ranging from 5.5 to 7.0 mm were used in the experiment. Five specimens of either B. globosus or B. tropicus were introduced into each test container. Each large tank supplied water to five containers with B. globosus and another five with B. tropicus. After 8 h the number of snails above the water line was counted. Water temperature, conductivity, dissolved oxygen and pH were measured in all the aquaria during counting of snails. Each experiment was repeated 10 times. Experiment 1: Water conditioned by Sargochromis codringtonii and Tilapia rendalli, effect over time. In each of two large aquaria a single S. codringtonii was introduced and one Tilapia rendalli was introduced in each of another two aquaria. The fifth aquarium without fish served as a control. After the first observation, which was done 8 h after the commencement of the experiment, the counting of snails above the waterline took place at hourly intervals for another 8 h. Experiment 2: Effect of different densities of S. codringtonii. Four aquaria were used and water was conditioned by one, three or five specimens of S. codringtonii, while in the last aquarium, water was left unconditioned. After 8 h the number of snails above the waterline was counted. Experiment 3: Effect of feeding by S. codringtonii. Three S. codringtonii were introduced into each of four aquaria, while the fifth one was a control without fish. In two of the tanks, the fish were fed with snails, whereas in the other two tanks the fish were not fed. The fish were fed at the beginning of the experiment with snails and then at 3-h intervals. Therefore, the fish were fed three times during the experiment. In order to avoid conditioning of water by live snails in the treatment, the fish were given snails at a rate that ensured that no snails escaped predation. Snails were added in approximately equal numbers of B. tropicus and B. globosus. A fish would be offered snails of the same size range as experimental snails until it stopped feeding. Each fish consumed 50–60 snails during the conditioning period. binary logistic regression (Hosmer & Lemeshow, 1989) where repeat experiment, time (experiment 1 only), conditioning factor and snail species were entered as categorical factors in mentioned order. Indicator coding was used with either the first or the last category as the indicator group. Interactions between snail species and the conditioning factor were made as the last step. Significance of a given factor was based on the change in the –2 log likelihood ratios. Model fit was assessed using the Hosmer-Lemeshow statistics (Hosmer & Lemeshow, 1989). The log of the regression coefficient is equivalent to the odds ratio, i.e. the likelihood of snails leaving water in a given group relative to that in the reference group, after adjusting for the other factors in the model. For the experiment with refuge, the three possible positions were analysed in a similar way using multinomial logistic regression. Comparisons of physical and chemical variables across treatments were done using either one-way or two-way (i.e. repeat experiment and treatment as factors) analysis of variance. The positions of snails were analysed using nominal logistic regression where repeat experiment, time, treatment (fish or no fish), snail species and the interaction between treatment and time were entered as factors. RESULTS Experiment 1: Water conditioned by Sargochromis codringtonii and Tilapia rendalli – effect over time Bulinus globosus and B. tropicus responded more to S. codringtoniiconditioned water compared with T. rendalli-conditioned water and unconditioned water (Fig. 1). The response varied significantly across repeat experiments (P 0.001), across conditioning factor (P 0.001), time (P 0.001) and between species (P 0.001). There was no significant interaction between conditioning factor and snail species. The number of snails out of water increased over time, and snails exposed to Presence of refuge Five large aquaria as described previously were filled to 75% capacity with water prepared as described. The refuge was built from two pieces of 7-mm-thick glass. A rectangular glass plate (40 45 cm) was supported by four 5-cm-tall ‘legs’ on one-half of a second rectangular glass (80 45 cm). The space between the top and bottom glass panes was intended to serve as a refuge to snails after the introduction of S. codringtonii. The fish used in the experiments ranged in standard length from 14.8 to 15.0 cm and had wet weights from 50 g to 56 g. The fish were too large to fit in the refuge space between the glass panes. The glass plates were placed in the five large tanks. The tanks were aerated using scorpion II filters during the experiment. Laboratory-bred specimens of Bulinus globosus and B. tropicus were used in the experiment. The snails had shell heights ranging from 5.5 to 7.0 mm. A total of 120 snails of each species were introduced into each tank and left for 24 h. Then a single S. codringtonii was introduced in each of three tanks whereas the other two served as controls. The number of snails within the refuge area, on open surfaces and out of the water was recorded just prior to the introduction of fish. After 8 h the number of snails occupying different positions was recorded and hourly thereafter for a total of 9 h. Water temperature, conductivity and pH were measured in all the aquaria. The experiment was repeated seven times. Statistical analysis Position of snails (1 out of water and 0 in water) in the three experiments with fish-conditioned water was analysed using Figure 1. Percentage of snails above the waterline in aquaria conditioned with Sargochromis codringtonii or Tilapia rendalli. 354 PREDATOR AVOIDANCE BEHAVIOUR IN BULINUS 1 2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 7 8 9 20 1 2 3 4 5 6 7 8 9 30 1 2 3 4 5 6 7 8 9 40 1 2 3 4 5 6 7 8 9 50 1 2 3 4 5 6 7 8 9 60 1 2 3 4 5 6 7 8 Table 1. Average (± standard deviation) values of physical and chemical variables measured in tanks containing Sargochromis codringtonii and Tilapia rendalli (n 10). P-values Variable Temperature (°C) Oxygen (%) Conductivity (S) Time Control S. codringtonii T. rendalli Repeat (h) (n 10) (n 20) (n 20) experiment Treatment ns 0 26.07 0.69 25.78 0.88 26.16 0.79 0.01 8 25.49 0.48 25.85 0.79 26.08 0.67 0.01 0.05 16 24.96 1.11 25.93 1.37 25.81 1.24 0.01 ns 0 61.73 4.88 61.27 5.07 63.55 6.36 <0.001 ns 8 61.00 4.95 58.20 4.81 60.02 6.52 0.001 ns 16 60.63 4.89 55.93 4.89 57.88 6.44 0.001 ns 0 118 8 125 9 122 11 ns ns 8 118 8 125 9 122 11 ns ns 16 pH 118 8 125 9 122 11 ns ns 0 7.69 0.26 7.67 0.22 7.79 0.19 0.001 0.05 8 7.71 0.30 7.66 0.26 7.76 0.22 0.001 ns 16 7.69 0.28 7.67 0.23 7.74 0.19 0.001 ns ns, not significant (P 0.05). fish were 5.548 times more likely to move out of the water than the control snails. Those exposed to water conditioned by three and five fish were 7.538 and 7.110 times, respectively, more likely to leave water than the control snails. Bulinus globosus was 1.334 times more likely to move out of water than B. tropicus. The Hosmer-Lemeshow goodness-of-fit test showed that the model fit was good (2 15.04, df 8, P 0.05). Overall, 66.3% of the snails were correctly classified by this model (72.0% of those in the water and 58.8% of those out of the water). The difference in response between the treatment with one fish and five fish was not significant and also the difference between densities of three and five fish was not significant. However, the response of snails exposed to water conditioned by one fish was significantly different from three and five fish pooled (P 0.05). The average values of physical and chemical parameters measured during the experiment are shown in Table 2. Oxygen was a slightly lower in aquaria with fish than in the control aquarium, and this difference was more pronounced at the end of the experiment. Tilapia-conditioned water were 2.296 times more likely to leave water than snails exposed to unconditioned water. Those exposed to water conditioned by S. codringtonii were 5.892 times more likely to leave water than those exposed to unconditioned water. Bulinus globosus was 1.274 times more likely to move out of water than B. tropicus. The Hosmer-Lemeshow goodness-of-fit test showed that the model of estimating whether snails were in or out of water was good (2 0.227, df 8, P 0.05). Overall, 70.6% of the snails were correctly classified by this model (87.0% of those in the water and 45.8% of those out of the water). A summary of the physical and chemical parameters measured during the experiment is shown in Table 1. Although these variables differed significantly between repeat experiments there was only a slight indication of variation across treatments. Experiment 2: Effect of different densities of Sargochromis codringtonii Bulinus globosus and B. tropicus did not respond differently to different densities of S. codringtonii (Fig. 2). Logistic regression analysis showed significant differences in response across repeat experiments (P 0.001), number of fish (P 0.001) and snail species (P 0.001). Snails exposed to water conditioned by one Experiment 3: Effect of feeding Sargochromis codringtonii The snails demonstrated a greater avoidance response to water conditioned by feeding fish than to water conditioned by nonfeeding S. codringtonii (Fig. 3). Logistic regression showed that there was a significant interaction between treatment and snail species (P 0.01) and the model reported on here includes this interaction. There was a significant difference in the response of snails across repeat experiments (P 0.001) and across treatments (i.e. unconditioned water, water conditioned by feeding and non-feeding fish (P 0.001)), whereas the main effect of snail species was not significant. The snails were 2.877 times more likely to move out of water when exposed to water conditioned by unfed fish than the control. Snails exposed to water conditioned by feeding fish were 3.899 times more likely to leave water than those exposed to unconditioned water. The significant interaction between treatment and snail species is because B. globosus elicited a greater response to water conditioned by feeding fish than to that conditioned by non-feeding fish, while B. tropicus did not respond differently to feeding and nonfeeding fish. The Hosmer-Lemeshow goodness-of-fit test indicated a good model (2 10.183, df 8, P 0.05). Overall, 65.0% of the snails were correctly classified by this model (78.5% of those in the water and 46.4% of those out of the Figure 2. Percentage of Bulinus globosus and Bulinus tropicus above the waterline in aquaria conditioned with different densities Sargochromis codringtonii. 355 P. MAKONI ET AL. Table 2. Mean ( standard deviation) values of physical and chemical variables measured in tanks containing different densities of Sargochromis codringtonii. Variable Time (h) Control One fish Three fish Five fish P-values Temperature 0 23.83 3.11 24.30 3.35 24.05 3.03 24.05 3.26 ns (°C) (n = 10) 8 23.28 2.74 23.98 3.15 23.59 2.80 23.82 3.12 ns Oxygen (%) 0 67.76 6.48 60.57 16.57 54.91 10.37 53.32 12.53 0.05 (n = 10) 8 63.72 7.27 47.82 14.31 49.07 11.00 49.06 14.81 0.05 Conductivity 0 120 10 118 12 118 4 125 12 ns (S) (n = 6) 8 120 10 118 12 118 4 125 12 ns pH (n = 10) 0 8.19 0.58 7.92 0.67 8.14 0.67 7.97 0.73 ns 8 6.58 0.75 6.41 0.67 6.59 0.96 6.43 0.90 ns ns, not significant (P 0.05). Table 3. Average (± standard deviation) values of physical and chemical variables measured in tanks containing fed and non-fed Sargochromis codringtonii. P-values Variable Temperature (°C) Conductivity (S) pH* Time No fish Fish fed Fish not fed Repeat (h) (n = 10) (n = 20) (n = 20) experiment Treatment 0 23.57 1.21 23.64 1.34 23.61 1.18 0.001 ns 8 23.68 1.09 23.66 1.20 23.73 1.11 0.001 ns 0 144 7 149 10 148 8 0.001 ns 8 145 5 150 8 149 6 0.05 ns 0 7.68 0.82 7.47 0.72 7.73 0.59 – ns 8 8.49 1.09 8.08 1.13 8.38 1.35 – ns *Done for three experiments only. ns, not significant (P 0.05). tribution of snails remained fairly constant throughout the study period. Multinomial logistic regression showed that there was a significant variation across repeat experiments (P 0.001), treatment (P 0.001), snail species (P 0.01) and further there was a significant interaction between conditioning factor and time (P 0.001). The model showed that snails were 3.758 times more likely to seek refuge in the presence of S. codringtonii than when no fish were present. Bulinus globosus had a slightly larger tendency to seek refuge than B. tropicus. Snails were 10.798 times more likely to leave water in the presence of S. codringtonii than when no fish were present. Bulinus globosus had a slightly lower tendency to leave water than B. tropicus. On average at the beginning of the experiments, about 22% of the snails were under the tray and 75% would be in the open surfaces, after 8 h, 64% of the surviving snails would be under the tray and 30% in the open surfaces. Averages of physical and chemical variables measured during the experiment are presented in Table 4. There was only little variation between repeat experiments while temperature was slightly higher in tanks with fish than in the controls. This temperature difference was evident during the last 3 h of the experiment (data not shown). Figure 3. Percentage of Bulinus globosus and Bulinus tropicus above the waterline in aquaria conditioned with feeding and non-feeding Sargochromis codringtonii. DISCUSSION water). Although the physical and chemical variables differed significantly between repeat experiments, there were no significant differences between treatments (Table 3). This study demonstrated the ability of Bulinus globosus and B. tropicus to respond behaviourally when exposed to water conditioned by S. codringtonii. Several studies have demonstrated that the presence of predators causes snails to respond. The addition of crayfish Procambarus simulans caused Physella virgata and Planorbella trivolvis to crawl out of water (Alexander & Covich, 1991). Hofkin et al. (1991) also reported a positive association between the crawling out of water behaviour of Physa acuta and the crayfish Procambarus clarkii. The crawling out of water behaviour of snails has been interpreted as a protective mechanism against predation. The snails reacted more to water Presence of refuge Sargochromis codringtonii was observed to start feeding on the snails once it was introduced into the tanks. Figure 4 show the percentage of snails occupying the three available positions over time in tanks with S. codringtonii and controls. The graphs show that more snails moved to the refuge after the introduction of S. codringtonii, whereas in the control aquaria, the relative dis356 PREDATOR AVOIDANCE BEHAVIOUR IN BULINUS 1 2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 7 8 9 20 1 2 3 4 5 6 7 8 9 30 1 2 3 4 5 6 7 8 9 40 1 2 3 4 5 6 7 8 9 50 1 2 3 4 5 6 7 8 9 60 1 2 3 4 5 6 7 8 conditioned by S. codringtonii than to water conditioned by Tilapia rendalli. Snails have been found to be able to distinguish between threatening and non-threatening species of predators (Kelly & Cory, 1987). Two freshwater snails Valvata piscinalis (Müller) and Bithynia tentaculata (L.) were able to distinguish between leeches, reacting only to the molluscivorous Glossiphonia complanata and not to the non-molluscivorous Erpobdella octulata (Kelly & Cory, 1987). The recognition of harmless species or organisms minimizes energy and time wasted due to unnecessary escape behaviour (Townsend & McCarthy, 1980). Chimbari (1996) investigated the behaviour of B. globosus and Melanoides tuberculata (Müller) in the presence of S. codringtonii. The results were inconclusive, but there was a greater tendency for B. globosus to crawl above the waterline than M. tuberculata in the presence of S. codringtonii. The density of fish did not cause significant differences in the response of snails. The observed results could also have been affected by the size of the tanks because the water in the tanks may have been ‘sufficiently’ conditioned by only one fish. Marine snails have been shown to be able to detect potential predators by distant chemoreception (Phillips, 1976; Schmitt, 1981; Watanabe, 1983). Few studies have demonstrated such predator defence mechanisms in freshwater snails. The Florida apple snail, Pomacea paludosa (Say) has been observed to respond to the ‘scent’ of a predatory turtle by moving down to the sediment and burying itself when a turtle comes into the vicinity (Snyder & Snyder, 1969). Results from these experiments indicate that snails did not only respond to the presence of S. codringtonii, but being exposed to water conditioned by feeding fish induced an enhanced response. The escape response of B. globosus to water conditioned by feeding fish supports observations made for Physella sp. (Turner, 1996), which increased refuge use when exposed to water conditioned by crushed conspecifics. Snails can reduce the costs of predator avoidance by avoiding false alarms and responding when predators pose a real threat (Phillips, 1978). Bulinus tropicus and B. globosus were able to move into covered areas where they were protected from predation by S. codringtonii. The high percentages (90%) of snails measured under the tray during the study may be due to an anti-predation response and an active refuge-seeking behaviour. However, this behaviour could also have been assisted by disturbances from the fish causing snails to detach and sink to the bottom, where the refuge was placed. Turner (1996) demonstrated that the behavioural responses of Physella decreased mortality due to predation. The snails were utilizing covered habitats more than crawling to the surface, Physella was observed to crawl out of water when the covered areas were absent. In the present study, few snails Figure 4. Percentage of snails occupying different positions in an aquarium in the presence of Sargochromis codringtonii and in control aquaria without fish. Time 0 is 24 h after snails were introduced and when fish were introduced. Table 4. Mean ( standard deviation) values of physical and chemical variables measured in tanks containing Sargochromis codringtonii (n 7). P-values Repeat Fish (n 21) Control (n 14) experiment Treatment 0 25.09 0.79 25.50 0.72 ns ns 8 25.39 0.81 25.30 0.59 ns ns 17 26.04 0.80 25.29 0.62 ns 0.05 0 125 8 129 10 ns ns 8 125 8 129 10 ns ns 17 125 8 129 10 ns ns Time (h) Temperature (°C) Conductivity (mS) pH 0 7.79 0.37 7.74 0.47 ns ns 8 7.67 0.35 7.60 0.37 ns ns 17 7.63 0.35 7.52 0.35 0.05 ns ns, not significant (P 0.05). 357 P. MAKONI ET AL. (about 9%) were observed to be moving out of the water in the presence of S. codringtonii, the majority of snails were crawling into the covered habitats. The anti-predator responses of snails affect growth rates of snails and delays reproduction (Yamanda, Navarrete & Needham, 1998; Crowl & Covich, 1990). During the experiments very few snails returned to the water once they had left. The presence of a predator will cause the snails to stay out of water, reducing their growth and reproduction. Staying out of water for relatively longer periods might decrease the encounter rates between miracidia and snails. However, since the snails actively sought refuge in the presence of S. codringtonii, the use of fish to control snails in areas with aquatic vegetation may be limited. Macrophytes provide some cover for snails against predators (Louda et al., 1984; Chimbari, Madsen & Ndamba, 1997), and the distribution of intermediate snails is associated with aquatic vegetation. For the molluscivorous fish to have an impact on snails in ponds with aquatic vegetation, herbivorous fish have to be introduced into the ponds (Bell-Cross & Minshull, 1988). In conclusion, the results suggest that Bulinus globosus and B. tropicus respond to water conditioned by S. codringtonii and have an enhanced escape response when exposed to water conditioned by feeding fish compared with non-feeding fish. The snails also actively sought refuge in the presence of S. codringtonii. 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