J. Moll. Stud. (2002), 68, 194–196
© The Malacological Society of London 2002
RESEARCH NOTES Laboratory experiments on snail-size selection by a snail predator, Sargochromis codringtoni (Pisces: Cichlidae) Jakob Brodersen*, Moses J. Chimbari†‡ & Henry Madsen* *Danish Bilharziasis Laboratory, Jaegersborg Allé 1D, 2920 Charlottenlund, Denmark, and †Blair Research Laboratory, P.O. Box CY 573, Causeway, Harare, Zimbabwe ‡Present address: University of Zimbabwe, Lake Kariba Research Station, Kariba, Zimbabwe
The cichlid fish, Sargochromis codringtoni, is a known snail predator1–3 and has shown some promise in snail-control.4,5 However, some experiments showed that the fish failed to control the largest sizes of Bulinus globosus and preferred the smaller B. tropicus, which is not an intermediate host for S. haematobium.6 Obviously, this apparent preference for B. tropicus may not be entirely a question of snail size since, for example, palatability of the two species could be involved. However, from a snail control point of view, snail-size selection by a potential predator is important because within a snail population, larger specimens seem to be more important for transmission than smaller specimens, due to a higher rate of cercarial shedding7,8 and higher infection rates.9,10 Consumption of large specimens of snails might depend on the size/age of the predator. This, in turn, raises some practical considerations in terms of propagation of the predator. The diet of S. codringtoni in natural systems has been investigated on several occasions,2,11,12 but with different conclusions. It appears that diet is influenced by both habitat and fish size. For other molluscivores, varying degrees of preference for specific snail sizes have been demonstrated,13–15 but there is only limited knowledge about snail size selection of S. codringtoni. In this study, we investigated the preference of S. codringtoni for prey comprising B. globosus of different sizes in aquaria. A substratum of sand, to a depth of 3 cm was placed in seven large aquaria (L, 100 cm; W, 60 cm; H, 60 cm). Tap water (currently used routinely for snail culture in this laboratory) was added to 2/3 capacity (240 l) and was left to de-chlorinate over night. The following day, Bulinus globosus of six different size-classes (shell height, 4–5.9, 6–7.9, 8–9.9, 10–11.9, 12–13.9, and 14–16 mm) were introduced into the aquaria together with plants, which included 2 m of Lagarosiphon major strands and 40 g (wet-weight) of Najas pectinata. The number of snails introduced varied between size classes and slightly between repeat experiments due to variation in availability. For the classes 4–5.9 mm; 8–9.9 mm and 14–16 mm, 10 snails were introduced, while for the class 10–11.9 mm, 25 snails were used. For the classes 6–7.9 mm and 12–13.9 mm, 20 and 25 snails were introduced, respectively, in the first repeat. These numbers were, however, lowered to 15 and 20, respectively, in the second and third repeat. The largest snails (8–16 mm) were wild caught, while the smallest snails (4–7.9 mm) were laboratory-bred. The only source of light was the sunlight that entered through the windows in the laboratory (dark-period: 8 h 53 min). The fish used in the experiment were caught in Lake Kariba using hook and line, and driven to De Beers Research Laboratory in Chiredzi, Zimbabwe, where they were kept in earth ponds for 32 days prior to the initiation of the experiments. Between repeat experiments the fish were kept in one aquarium. The following day, one S. codringtoni was introduced into each of six aquaria, while the last aquarium was left without fish and served as a control. Before introduction, the fish were * Corresponding author: email
[email protected]
weighed and standard length (SL length from tip of snout to end of caudal peduncle) measured. The fish were divided into three size-classes: 40–60, 60–80, and 80–120 g, corresponding to SL of approximately 10.4–11.9, 11.9–13.0, and 13.0–14.5 cm, respectively. The fish were left in the aquaria over night and removed 18 h after their introduction. Physical conditions (temperature, pH, conductivity, and oxygen content) were measured using Digital-pH 90 (pH), YSI Model 55 Handheld Dissolved Oxygen System (Oxygen) and Digital Conductometer LF 92 (conductivity and temperature). The aquaria were then emptied and the number of snails remaining within each size-class counted. The experiment was repeated three times. The outcome (recaptured 0, not recaptured 1) for individual snails was analysed using logistic regression analysis16 using fish size (including the control), snail size (using the size class 14–16 mm as reference size class), and repeat experiment as factors. The proportion of snails removed is presented graphically together with exact 95% confidence intervals calculated as shown in Fleiss.17 For comparisons of physico-chemical parameters (temperature, conductivity, pH, and dissolved oxygen) across treatments (control and fish size), Kruskal–Wallis one-way analysis of variance18 was used. The physical conditions varied slightly (Table 1), but there were no significant differences for any of the recorded physical variables between the different treatments. The percentage of snails not recaptured after the experiment is shown in Figure 1. Dead snails with intact shells were assumed to represent snails that died from other causes than predation. Not all snails of the two smallest size classes were recaptured in the control aquaria, which is probably due to difficulties in locating the smallest snails on the rough sand substratum in the aquaria. Large proportions of the small snail size classes (4–9.9 mm) were removed by all sizes of fish. Small fish, however, appeared to eat fewer large snails than large fish. Only the largest sized fish removed a few of the largest snails (14–16 mm). Logistic regression analysis testing only for main effects showed that small fish consumed fewer snails (P 0.001) than the two largest size classes when adjusting for snail size (P 0.001) and repeat experiment (P 0.001). Differences between the two largest size classes of fish were not significant. All smaller size classes of snails were consumed to a greater extent (P 0.001 for all comparisons) than the reference size class (i.e. the largest group). Repeat experiments 1 and 2 did not differ, while more snails were consumed in experiment 2 than in 3 (P 0.01). The model showed that overall 83.5% of snails were correctly classified (80.9% of those not consumed and 86.3% of those consumed). The Hosmer and Lemeshow Test showed a reasonably good model fit (Chi-square 1.914, df 8, P 0.984). A significant statistical interaction was found between fish size and snail size (P 0.001) indicating that large fish consume more large snails than small fish.
RESEARCH NOTES 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
It is evident that all sizes of S. codringtoni included in this study prefer small snails. In a previous study, Chimbari et al.5 concluded that the fish did not show any preference for snails of any particular size. Chimbari et al. worked with both smaller sized snails and smaller fish (30–59 g) than used in the present study. Their largest size class of snails (9 mm) includes snails that in this experiment would be placed in our third smallest size class. As can be seen in Figure 1, the proportions of snails removed in the three smallest size-classes are quite similar, which may explain why Chimbari et al. did not find significant differences.5 The reason for this preference for small snails could be related to the fish’s ability to handle large snails. Thus Roberts & Kuris14 found that the freshwater prawn Macrobrachium rosenbergii does not show a preference for specific snail sizes as long as it is capable of handling them. At least the medium and the large size classes of fish (60–80 and 80–120 g) were able to prey on the largest size-class of snails, but still showed a preference for smaller snails. In a separate trial, where one S. codringtoni weighing 69 g was presented with 25 large Bulinus globosus (14–16 mm), 19 specimens were consumed over night. Although large fish consumed larger snails than small fish, it is not clear whether this reflects a difference in snail size preference or whether depletion of small snails in the aquaria made the larger fish consume larger snails. It may be of some importance that the smallest snails used in this experiment were laboratory bred, whereas the largest snails were wild caught. Osenberg & Mittelbach19 found that the crushing resistance of Physa acuta was much higher for wild caught specimens than for laboratory-bred specimens. Crushing resistance has often been shown to be important for size selection by molluscivores.20–24 The fish used in this experiment (up to 112 g) are not large compared to the size attained in nature, where the fish according to Skelton3 attains a total length 290 mm. This length corresponds to fish weighing about 500 g in Lake Kariba (personal observations). However, larger specimens are not uncommon. Of 28 net-caught S. codringtoni from Lake Kariba, 18 were above 500 g, with a maximum weight of 954 g. These large fish are difficult to catch with hook and line, which is why only relatively small specimens were used in this study. Netcaught S. codringtoni were not able to survive the transport to the laboratory. Previous studies have shown that hooking has minimal effect
on feeding, physical condition, and mortality.24–26 It seems unlikely that mouth damages caused by hooking should cause changes in the food preference of the fish. Hooks were usually placed in the mouth cavity and S. codringtoni uses the pharyngeal bone for crushing snails.3,11 Furthermore, hooks were gently removed and fish were kept for more than a month before experiments. Moyo27 investigated the relative abundance of different food types in stomachs from various sized S. codringtoni from Lake Kariba. The results indicated that fish between 12 and 17 cm consumed larger numbers of pulmonate snails than of prosobranch snails, whereas larger fish consumed more prosobranchs than pulmonates. Moyo & Fernando12 suggested that the large proportion of prosobranchs in the diet of large S. codringtoni in Lake Kariba was due to the dominance of prosobranchs at greater depths, where large fish were usually found. As one of the major target areas for schistosomiasis control are irrigation schemes, where water is usually shallow, it is unlikely that this dietary shift would happen. This is an area for further studies. An investigation of the preference for pulmonates compared to prosobranchs should also be made. Since it appears that large fish consume larger snails than small fish, we suggest that a relative high density of large fish (from about 100 g) should be preferred in snail control. The size of predators can affect gastropod communities. Thus, Brönmark & Weisner28 found that in Swedish lakes, where average sizes of molluscivores were large due to the influence of piscivores, the snail fauna was dominated by relatively small and hard-shelled species. Table 1. Average ( SD; n 3) values of various physical or chemical conditions in aquaria based on recordings at the end of the experiments. Temperature
Conductivity
Fish size
(°C)
(S)
Dissolved O2
Control
25·3 0·6
135 7·1
7·3 0·09
69·0 6·4
40–60 g
25·3 0·4
140 0·0
7·3 0·01
60·3 5·9
pH
(%)
60–80 g
25·1 0·5
133 5·2
7·3 0·05
63·4 5·6
80–120 g
25·2 0·5
135 5·8
7·2 0·05
61·4 4·1
P-value*
NS
NS
NS
NS
*Kruskal–Wallis one-way analysis of variance.
Figure 1. Percentage of Bulinus globosus snails of various size-classes, which were not recaptured from aquaria with Sargochromis codringtoni of various sizes.
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RESEARCH NOTES 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
13. STEIN, R.A., GOODMAN, C.G. & MARSCHALL, E.A. 1984. Ecology, 65: 702–715. 14. ROBERTS, J.K. & KURIS, A.M. 1990. Ann. Trop. Med. Parasitol., 84: 401–412. 15. WEINZETTL, M. & JURBERG, P. 1990. Mem. Inst. Oswaldo Cruz, 85: 35–38. 16. HOSMER, D.W. & LEMESHOW, S. 1989. Applied Logistic Regression. John Wiley & Sons, Harlow. 17. FLEISS, J.L. 1981. Statistical methods for rates and proportions. John Wiley & Sons. 18. SIEGEL, S. 1956. Nonparametric statistics for the behavioural sciences. McGraw-Hill Kogakusha Ltd., Tokyo. 19. OSENBERG, C.W. & MITTELBACH, G.G. 1989. Ecol. Monographs, 59: 405–432. 20 IRLEV, V.S. 1961. Experimental ecology of the feeding of fishes (translated from Russian). Yale University Press, New Haven. 21. STEIN, R.A., KITCHELL, J.F. & KNEZEVIC, B. 1975. J. Fish Biol., 7: 391–399. 22. TUCKER, A.D., YEOMANS, S.R. & GIBBONS, J.W. 1997. Am. Midl. Nat., 138: 224–229. 23. BROWN, K.M. 1998. Freshwater Biol., 40: 255–260. 24. MALCHOFF, M.H. & HEINS, S.W. 1997. N. Am. J. Fish. Manag., 17: 477–481. 25. THOMAS, M.V. & HAAS, R.C. 1999. N. Am. J. Fish. Manag., 19: 610–612. 26. BROADHURST, M.K. & BARKER, D.T. 2000. Arch. Fish. Mar. Res., 48: 1–10. 27. MOYO, N. 1995. The biology of Sargochromis codringtoni in Lake Kariba. PhD thesis, University of Zimbabwe. 28. BRÖNMARK, C. & WEISNER, S.E.B. 1996. Oecol., 108: 534–541.
ACKNOWLEDGEMENTS We would like to thank the staff at Lake Kariba Research Station for assistance on catching Sargochromis codringtoni and the staff at De Beers Research Laboratory in Chiredzi for help on performing the experiments. Furthermore, we would like to thank Rådet for Ulandsforskning, Denmark for financial support.
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