BIOLOGICAL CONIROL OF HUMAN SCHIS TOSOMIASIS USING SNAIL EATING FISH by Sosten Staphiel Chiotha Dissertation subimitted to the Faculty of Graduate School of The University of Maryland in partial fulfillment of the req _rents for the degree cf Doctor of Philosophy 1990 Advisory ccxmittee: Professor Kenneth MoKaye, Chaiman/Advisor Professor Sam Joseph Associate Professor J. Edward Gates Associate Professor Raymond Morgan Professor Jay Stauffer IIi ''APR 5 " C Copyright by Sosten Staphiel Chiotha 1990 ACKNOlqLEDGMEW~ I am grateful to the Goverrments of Malawi and United States of America for the sponsorship to study for a Ph.D at the University of Maryland, College Park. The fellowship was administered by the staff of The African American Institute and I comend them for the expertise in handling academic and welfare issues affecting students in the programme. I am grateful to Prof. K. R. McKaye for playing a major role as an advisor and for devoting considerable tire to the study. I am also grateful to the dissertatinn canittee nmbers, Prof. Sam Joseph, Ass. Prof. J. Edward Gates, Ass. Prof. R. Morgan II, and Prof. J. Stauffer for their assistance during planning and execution of research and during writing of the dissertation. In the University of Malawi, I wish to thank Dr. John Dubbey (Vice Chancellor), Dr. Z. D. Kadzamira (Principal Chancellor College), Prof. B. B. Chimphamba (Principal Bunda college), Dr. D. C. Munthali, Dr. E. B. Khonga, Dr. E. Y. Sambo, Dr. T. Makhambera, Dr. Phoya, Mr. J. Likongwe, and others for their assistance in working out the logistics of research in Malawi, Africa. I am particularly grateful to the Malawi Fisheries Department for kindly allowing the project to take place and the Malawi Bilharzia control Unit (Ministry of Health) for helping in many ways. I thank Dr. E. Van den berghe, Dr. S. Seagle, Dr. P. LaChance, Dr. R. Raesly, Dr. G. Nelson, John Ypande, and Dave Brinker for their valuable ccmments on various drafts of the dissertation. I am especially indebted to Prof. K. Fuller, A. Allen (Ms), P. Orndorff (Ms), Kirk, E. (Ms) ii and other staff at the Appalachian Environmental Lab. for a number of services that created ai excellent atmosphere for Graduate study. I am grateful to Dr. R. nzer, Dr. I. Strand, Mary-Ellen Atkinson (Ms) and J. Wildberger (Ms) for an excellent job in co-ordinating studies in the NEES program. I am also grateful to Joan McKearnan for assistance in using the ccmputer and Dr. Lester Chitsulo for assistance in literature search. I wish to pay special tribute to James J. Msosa (Late) who assisted me in transporting fish. I am particularly grateful to my wife Chiwa and daughter Mtisunge, 1y parents, brothers and sisters, in-laws, and W. W. Kanjo for their moral support. I wish to thank C. Jenya, S. Mponda, S. Bvalani, T. Lovullo, A. Matambo and others who assisted in both the field and laboratory work. I wish, also, to thank J. Balarin and Dr. B. Costa.-Pierce of ICLRARM (Malawi), D. Malikebu and the fish farmers in Zrba for assistance in several respects. The research was funded by grants fran Agency for International Development, The Rockefeller Foundation and the International Foundation for Science. At the recammendation of the Dissertation ccmiittee, information from a project Funded by the ICLARM-GTZ aquaculture project in Malawi has been incorporated in the dissertation. iii TABLE OF CONTENTS Section Page List of tables vi List of figures viii CHAPTER 1 NDLLUSCICIDES USED TO CONTROL SCHISIOSQIAS IS: REVIEW Introduction 1 Types of nolluscicides 2 Mode of action 5 Factors that influence toxicity 8 Toxicity to humans and other non-target organisms 11 Conclusion 13 CHAPTER 2 BIOLOGICAL CONTROL OF SCHISTOSCMIASIS USING SNAIL EATING FISH: REVIEW. Introduction 15 The parasites 17 Justification for control 21 Methods of control 24 Fish as biological control agents 25 Advantages of fish as biocontrol agents 27 Ecological constraints and caveats in the use of 32 fish CHAPTER 3 PREY HANDLING IN Cyrtocara placodon: A SNAIL EATING FISH FROM MALAWI. Introduction 39 Materials and methods 40 Results 42 Discussion 45 CHAPTER 4 FOCD SELECTION IN TW SNAIL EATING FISH (C.placodon and Astatotilapia calliptera) FROM MALAWI AND ITS RELEVANCE TO BIOLOGICAL COIROL OF SCHIS ESOMASIS Introduction 58 Materials and methods 60 Results 63 Discussion 70 CHAPTER 5 THE INFLUENCE OF WEEDS AND SNAIL LOCATION ON THE POTENTIAL OF SNAIL EATING FISH (C. placodon and A. calliptera) FOR BIOCONTROL OF SCHISTOSOMIASIS Introduction 83 Materials and methods 84 Results 86 Discussion 90 iv CHAPTER 6 SCHISTOSOME VECTOR SNAIL CONTROL IN FISH PONDS IN MALAWI USING FISH Introduction 96 Materials and methods 97 Results 102 Discussion 117 CHAPTER 7 SUMMARY AND CONCLUDING REMARKS Water resource projects and regional expansion of schistoscniasis 121 Schistosomiasis control in inpounded waters of Malawi 125 APPENDIX 1 SNAM COLLECTION AND TRANSPORTATION 127 APPENDIX 2 FISH COLLECTION AND TRANSPORTATION 131 APPENDIX 3 ESTIMATION OF CERCARIAL DENSITY 134 REFEREhNES 135 v LIST OF TABLES Table 1. Tim (minutes) taken for 10 molluscivores (C.placodon) to start feeding on snails. 55 Table 2. Average nurber of snails eaten by C. placodon, given a choice of two snail species. 66 Table 3. Average number of small and large snails eaten by two molluscivores, C. placodon and A. calliptera. 67 Table 4. Prey selection by A. calliptera and C. placodon based on presence and absence of snail shell for B. globosus. 68 Table 5. Average number of cercariae per liter in aquaria stocked with C. placodon and A. calliptera. 69 Table 6. Frequency of C. placodon and A. calliptera under two treatment levels of weed presence, snail presence and snail location. 88 Table 7. The effect of weeds in aquaria on the number of snailA consumed by C. placodon. 89 Table 8. Effect on snails of stocking experimental ponds with C. anaphyrmis (molluscivore). 106 Table 9. Survival of C. placodon and 0. shiranus (non-molluscivore) in experimental ponds. 107 Table 10. Survival of 0. shiranus in experimental ponds, with and without C. placodon. 108 vi Table 11. Initial and final weight of 0. shiranus in experimntal ponds . ill Table 12. Weight gain by C. placodon and 0. shiranus in experimental ponds. 114 Table 13. Initial and final snail population in rural fazners' ponds, with and without C. placodon. 115 Table 14. Pilot breeding trial of C. placodon in experimental ponds. 116 vii LIST OF FIGURES .5 Fig. 1. Life cycle of schistosciasis 37 Fig. 2. External morphology of three snail species: 1.) Bulinus tropicus, 2.) Bulinus globosus and 3.) Bicmphalaria pfeifferi Fig. 3. Point load crusher for estimating static crushing resistance of snails 51 Fig. 4. Handling time in two C. placodon for B. globosus snails of different sizes 53 Fig. 5. Static crushing resistance of B. globosus, B. pfeifferi and B. tropicus snails 56 Fig. 6. Final snail population in experimental ponds with and without C. placodon 104 Fig. 7. Initial and final ueight of C. placodon in experimental ponds 109 Fig. 8. Weight increase (%) of 0. shiranus in experinental ponds with and without C. placodon 112 129 Fig. 9. Map of Malawi viii ABSTRACT Title of Dissertation: BIOLOGICAL CONTROL OF }KRAN SCHISTOSOMIASIS USING SNAIL-EATING FISH Sosten Staphiel Chiotha, Doctor of Philosophy, 1990 Dissertation directed by: Kenneth R. McKaye, Professor, Marine Estuarine and Environmental Studies Schistosomiasis, a debilitating disease affecting millions of people in the tropics, is caused by flatworms (Schistosomna spp.). Transmission involves water contact in habitats infested by vector snails. Disease control by snail destruction with rolluscicides has been attempted with variable success. Because nolluscicides are costly and some are toxic to non-target organisms, particularly fish, alternative control techniques are needed. This study was conducted to test three cichlid fishes native to Malawi, Africa, for biological control of schistosomiasis. The cichlids, Cyrtocara placodon, Cytocara anaphyrmis and Astatotilapia calliptera, were chosen based on earlier reports of snail-eating habits. In laboratory experiments, Bulinus globosus, Biomphalaria pfeifferi and Bulinus tropicus snails were used as prey; the first two being vectors of humaj schistosciiasis. Choice experiments of providing molluscivores with two snail species suggested no prey species preference. Given single snail species of two size classes, the molluscivores preferred small to large snails. Presented with normal and crushed snails, the rolluscivores consumed more of the latter. When introduced in aquaria under two treatments of weeds/no weeds or snails/no snails, the molluscivores spent more time in sections with weeds and snails respectively. Fewr snails were consumed in aquaria with than without weeds. When snails were buried in sediment, the molluscivores did not detect the snails. Alternative foods such as corn-bran and ccmercial aquarium cichlid food, except cercariae, were consumed by the molluscivores. Prey handling time in the molluscivores and static crushing resistance of snail shells, increased with snail size. Field trials demonstrated dramatic snail reduction from e.,:perimental ponds and rural farmers' ponds stocked with C. placodon. C. placodon survived well in ponds, gained weight and appeared to co-exist with Tilapia rendalli, a tilapine aquaculture species. No snail reduction was observed with C. anaphyrmis in ponds and survival was poor. Implications of these results for biological control are discussed. C. placodon is a promising biocontrol agent. CHAPTER 1 ICIDES USED TO O1NTROL SCHIS'IOSO4IASIS INnwrr"icN Molluscicides are chemicals designed specifically to kill various types of molluscs (Cremlyn, 1978; Ritchie, 1973). Mollu:zcs affect man in several indirect ways. Some molluscs, namely snails and slugs, cause considerable crop damage by feeding on seedlings and mature plant leaves (Cremlyn, 1978). Such crops as autumn-sawn wheat (Hartley and West, 1969) and tobacco in Malawi (Meredith, 1983) suffer severe attack by snails and slugs.