| Aquaculture and schistosomiasis |
E.S. Loker, B.V. Hofkin, G.M. Mkoji, J.H. Kihara, F.K. Mungai, B.N.Mungai, And D.K. Koech
The Louisiana red swamp crayfish, Procambarus clarkii, introduced into Lake Naivasha, Kenya, about 1970, has become well established and now supports a small but thriving aquaculture industry. This crayfish has since dispersed over a wide area in Kenya, giving rise to concerns about its ability to disrupt natural ecosystems both in Lake Naivasha and elsewhere. In addition, P. clarkii may adversely affect fin fisheries in Lake Naivasha, and has been implicated as a pest in rice cultivation schemes outside of Africa. In contrast, our investigations indicate that P. clarkii can effectively control or eliminate certain freshwater snail species, including those involved in the transmission of human schistosomiasis. As such, P. clarkii appears to offer hope as a biological control agent of snail-transmitted diseases in selected habitats in East Africa. In this paper, we present details regarding the currant distribution of P. clarkii in Kenya and discuss possible approaches to the use of crayfish in snail control operations. Furthermore, concerns regarding the impact of P. clarkii on non-target species and on Kenyan freshwater habitats are discussed, and areas in need of additional investigation are highlighted.
The Louisiana red swamp crayfish, Procambarus clarkii, is the most widely distributed of all crayfish species, having been introduced into 24 countries on five continents (Hobbs et al. 1989). In the United States, P. clarkii supports a thriving aquaculture industry. Elsewhere, this species is now harvested commercially in countries as diverse as Spain, Turkey, and Kenya (Hobbs et al. 1989).
Africa represents a unique situation regarding such introductions in that it lacks an indigenous crayfish fauna (Hobbs 1988). Procambarus clarkii is now present in the Sudan, Kenya, Uganda, Zambia, Zimbabwe, and South Africa (Hobbs et al. 1989). Details regarding the original introduction of P. clarkii into Kenya remain unclear, but the first individuals were probably imported from Uganda into small ponds in the Rift Valley in the mid-1960s (Oluoch 1990). In 1970, P.clarkii was introduced into Lake Naivasha, apparently in an attempt to develop a fishery for this species (Lowery and Mendes 1977a, Parker 1974, Oluoch 1990). Actually, there is an unconfirmed report that P. clarkii may have been introduced into the lake as early as 1952 for the purpose of leech control, but this claim needs verification. Since its original introduction, P. clarkii has become well established in Lake Naivasha and has supported a viable aquaculture industry. Crayfish are now considered to be one of four important commercial species harvested from the lake, with an annual average catch of approximately 60,000 kg (live wet weight) over the past 10 years. More than 80% of this catch is exported, primarily to western European countries (Kenya Fisheries Department, personal communication). The remainder is consumed locally, mostly in restaurants in Nairobi; crayfish have not been readily adopted by most Kenyans as a preferred food item. Other large freshwater habitats in Kenya, for example, the Masinga dam complex to the south and east of Mt. Kenya, may have potential for crayfish aquaculture. In Kenya, crayfish are not harvested commercially from the numerous small dams and ponds they occupy at present, and it seems unlikely that this will change in the future, owing to excessive transportation costs.
Current Distribution Of Procambarus Clarkil
In the estimated 20-30 years since its first introduction into Kenya, P. clarkii has expanded its range and its known distribution now includes a large portion of the country (Figure 1). Besides Lake Naivasha, its presence in the Rift Valley has been confirmed in freshwater habitats near Lake Nakuru (Lowery and Mendes 1977b) and from streams and ponds in the western highlands (near the towns of Eldoret and Kitale), which form part of the Lake Victoria drainage basin. Procambarus clarkii is especially abundant in the Athi River basin in and around Nairobi. It extends through the Muranga District in the central highlands and has been collected as far north as Nanyuki. Its presence has also been confirmed in the upper basin of Kenya's largest river, the Tana. We have also recovered P. clarkii in Machakos District, near the town of Tala. It has apparently not colonized habitats on the tropical coastal plain. The town of Matuu, approximately 300 km from the Indian Ocean, represents the easternmost site from which we have collected this species. Reports of its presence in Lake Victoria (Lowery and Mendes 1977b) have recently been discounted by local fisheries experts, and our own recent efforts to locate crayfish in Lake Victoria and in inflowing streams have not been successful. Of considerable interest are possible future extensions of its range in East Africa, either through natural or human-assisted dispersal.
Snail-Transmitted Parasites Of Medical And Veterinary Significance
Our interest in P. clarkii stems from our investigations into the biological control of schistosomes and other snail-transmitted parasites in Kenya. Schistosomiasis, a debilitating, chronic infection of the tropics and subtropics, is caused by blood flukes of the genus Schistosoma. It is estimated that between one and two million Kenyans are infected with either the intestinal or urinary forms of the disease, or both (Highton 1974, Diesfeld and Hecklau 1978, Iarotski and Davis 1981, Butterworth et al. 1984, Ouma et al. 1985, King et al. 1988). Pathology, especially in children, can be severe (Wilkins 1987). The life cycle of schistosomes is complex and involves humans (and potentially other mammals) and particular species of freshwater snails as hosts for adult and larval worms, respectively (see review by Rollinson and Simpson 1987). Humans are exposed to infection by entering bodies of water containing infected snails. Infective stages, termed cercariae, released from the snails penetrate human skin to initiate infection. Infected humans facilitate transmission by urinating or defecating in water, thereby ensuring passage of parasite eggs into the environment of the snail intermediate hosts.
Snails of the genus Biomphalaria serve as intermediate hosts for Schistosoma mansoni, the causative agent of intestinal schistosomiasis. Snails within the genus Bulinus fulfill this function for S. haematobium, the parasite responsible for urinary schistosomiasis. Other snail-transmitted trematode parasites commonly infect domestic ruminants in Kenya and include the blood flukes S. bovis and S. mattheei, the common liver fluke Fasciola gigantica, and paramphistome flukes (see Brown 1980 for a comprehensive review of freshwater snails and associated trematode parasites in Africa).
The distribution of human schistosomes in Kenya is widespread (Figure 2) and is dictated ultimately by the distributions of the associated snail species (Brown et al. 1981, Loker et al. unpublished data). It is noteworthy that the present geographic ranges of the relevant snails and of P. clarkii are broadly, but not completely, overlapping (Figures 1 and 2). Owing to a rapidly increasing human population, unabated pollution of freshwater habitats by human excrement, construction of dams and irrigation schemes that favor the growth of snail populations, and the lack of a comprehensive national control program, it is likely that the prevalence of human schistosomiasis will remain high, or even increase. Although effective chemotherapeutic agents are available and are capable of reducing morbidity and mortality resulting from infection, they are expensive, and unless repeatedly applied to infected individuals are unlikely to diminish transmission significantly. A schistosome vaccine is a laudable goal, but remains elusive (Skier et al. 1989). Snail control, in conjunction with other control measures, offers hope for interrupting the transmission cycle, but traditional methods for controlling snails have primarily relied on molluscicidal chemicals that are also expensive. Moreover, because of their lack of selectivity, molluscicides pose environmental concerns and can only be condoned for use in focal applications (Klumpp and Chu 1987). New approaches to the control of schistosomes are needed (Most 1987, Madsen 1990).
In the course of snail survey studies of Kenyan freshwater habitats, it was observed that schistosome-transmitting snail species rarely, if ever, were found in habitats containing P. clarkii. A more formal analysis of the extent to which crayfish and medically important gastropods occurred at the same time revealed a highly significant (p < 0.001) negative association between the presence of snails and P. clarkii (Hofkin et al. 1991). Of the 53 sites examined, snail-crayfish co-occurrence was recorded in only four; the snail species recovered from these four sites do not transmit human schistosomes. All 53 sites were within the known distribution of both medically important snails and crayfish and were considered, a priori, as suitable snail and crayfish habitats.
Subsequent experiments indicated that both juvenile and adult P. clarkii were able to significantly reduce Biomphalaria abundance in both laboratory aquaria and field enclosures in as few as five days (Hofkin et al., unpublished data). Crayfish consumed large numbers of snails even when alternative foods were available and frequently eradicated Biomphalaria populations within the five-day experimental period.
Furthermore, P. clarkii was able to significantly reduce the abundance of the aquatic plant, Nymphaea caerulea, in experimental aquaria and field enclosure cages (Hofkin et al., unpublished data). The presence of this common water lily has been positively correlated with the presence of both Biomphalaria and Bulinus snails (Woolhouse and Chandiwana 1989), which use them for food, oviposition sites, and refuge. By feeding on, and reducing the abundance of such plants, P. clarkii may also serve as a competitor of snails of medical and veterinary significance.
These research results have led us to believe that P. clarkii is effective in controlling and/or eliminating certain snails of relevance to human public health. As such, this crayfish may represent a viable option as a biological control agent of schistosomes and other snail-borne diseases. Some of the potential advantages offered by P. clarkii as a control agent are: 1) its impact on target species is likely to be long-lasting and, unlike chemically based methods of control, would not have to be repeatedly applied; 2) the expense involved in its use would be minimal, 3) it could simultaneously reduce transmission of all snail-transmitted parasites, including species relevant to both humans and domestic animals, and 4) because P. clarkii is able to withstand habitat drying, it could be used in both permanent and seasonal transmission sites. Enthusiasm for the use of P. clarkii in snail control operations must, however, be tempered by the realization that biological control, in and of itself, is probably only rarely sufficient for bringing about a complete cessation of transmission. Moreover, the use of P. clarkii in particular poses certain environmental risks (see below) that must be carefully considered before their widespread use as putative control agents can be advocated.
Perhaps the most immediate concern regarding the presence of P. clarkii in Kenya is its impact on fin fisheries in Lake Naivasha and, potentially, in other waterbodies with commercially viable fisheries. Because of its voracious feeding habits, P. clarkii is thought to pose a risk to nest-breeding, commercially important species such as Tilapia (Lowery and Mendes 1977a). For example, crayfish might interfere with the breeding of Tilapia zillii (itself an introduced species in Lake Naivasha) either by consuming its eggs or by disturbing its nest sites. Also, because of its omnivorous nature, P. clarkii can reduce the abundance of aquatic plants (Lowery and Mendes 1977a, Feminella and Resh 1989, Hofkin et al., unpublished) and therefore might restrict the available nursery areas for young fish. For example, crayfish are thought to be at least partially responsible for the dramatic decline of indigenous water plants in Lake Naivasha. Tilapia zillii catches have declined in the lake since the introduction of P. clarkii, to the point that fewer than 3,100 kg of this species have been harvested since 1980 (Kenya Fisheries Department, personal communication).
Crayfish might adversely affect commercial fisheries in Lake Naivasha in other ways. Fish taken in gill nets are often attacked and partially consumed by crayfish before the nets are recovered, resulting in a lower market price for the damaged catch. Crayfish also become entangled in the nets, necessitating both their removal and repair of the nets. It is interesting to note, however, that fishermen in Lake Naivasha are legally required to place their nets at least 100 m from the lakeshore. The vast majority of P. clarkii in the lake are found in shallow water near the shore, meaning that most net fishermen who suffer crayfish-related damage are actually fishing illegally (Kenya Fisheries Department, personal communications).
The exact role that crayfish may have played in the decline of lake fisheries is complex and unclear, owing in part to simultaneous man-made habitat modifications, natural climatic fluctuations, and introductions of several other exotic species. For example, a section of Lake Naivasha known as "Small Lake" was cut off from the main lake basin when a causeway was constructed in 1982. This now isolated part of the lake was regarded as a prime breeding area of T. zillii, so the decline in catches for this species may, in part, reflect this loss of breeding habitat. In addition, fish populations in the lake tend to fluctuate naturally as increasing or decreasing water levels either add to, or subtract from, the amount of suitable inshore breeding habitat. Lake Naivasha has experienced relatively dry conditions in recent years, which partially explains reduced T. zillii catches (Kenya Fisheries Department, personal communications).
The effect of P. clarkii on the other two important fisheries species in Lake Naivasha, largemouth bass (Micropterus salmoides) and a second tilapia species (Oreochromis leucostictus), seems more likely to be neutral or even beneficial. Oreochromis leucostictus is a mouth breeder and is therefore not subject to egg predation by crayfish. Largemouth bass nest along rocky shorelines where crayfish are uncommon. Additionally, P. clarkii comprise more than 70% of the largemouth bass diet, which, in turn, relieves predation pressure by bass on other potential prey, including Tilapia (Kenya Fisheries Department, personal communications).
A second concern regarding the further introduction of P. clarkii in Kenya involves its potential as a pest in rice cultivation schemes. Rice is grown in Kenya both for domestic consumption and for export. Procambarus clarkii is known to consume rice seedlings and to damage dikes as a consequence of its burrowing activities (Miltner and Avault 1980, Huner 1988). To date, P. clarkii has not been considered a problem for Kenyan rice farmers (Kenya National Irrigation Board, personal communication). In all major rice growing schemes in Kenya, seedlings are cultivated in nurseries for one month prior to transplantation into the paddies. At the time of transplantation, Furadan®, a carbamate insecticide and nematicide, is applied to the paddies at a concentration of 4 kg/acre. The effects of Furadan®, as used in Kenya, on crayfish are not known, but its use may explain the apparent absence of P. clarkii from rice schemes. For example, crayfish are absent from the Mwea scheme but are present in the Makuyu area, approximately 15 km away.
Thus, the potential impact of P. clarkii on rice cultivation remains unclear and deserves additional consideration. If crayfish are indeed excluded from rice fields through the routine use of Furadan®, it is encouraging that a widely used, commercially available pesticide may have value in preventing the spread of crayfish into habitats where their use in snail control might be contraindicated.
Another concern pertaining to P. clarkii that deserves consideration relates to its possible involvement in transmission of parasites of medical significance. Crayfish can serve as second intermediate hosts for lung flukes of the genus Paragonimus, including species known to infect humans (Sogandares-Bernal 1965). Paragonimus uterobilateralis and P. africanus are known from West Africa but have not been reported in Kenya or other parts of East Africa, presumably because the appropriate species of snail first intermediate host is absent (Brown 1980). In any case, it seems unlikely that lung fluke transmission in Africa would be substantially altered by the introduction of P. clarkii as several species of freshwater decapods are already present and are probably as likely as P. clarkii to serve as efficient second intermediate hosts. Because P. clarkii are sometimes frozen and usually cooked thoroughly before consumption, it is unlikely that they would serve as a significant source of parasitic infection for humans.
In addition to its possible impact on species of direct relevance to human commerce and health, the effect of P. clarkii on other non-target organisms and on natural ecosystems in general should be considered as well. Crayfish are voracious omnivores and are often able to significantly alter the structure of natural aquatic communities (Carpenter and Lodge 1986, Lodge and Lorman 1986). This might be achieved by direct depredation of indigenous aquatic invertebrates or vertebrates, or by vigorous consumption of macrophytes and detritus used by other organisms as food sources or as cover from predators. Its escape into large natural habitats such as Lake Victoria, or the other African great lakes, with their large numbers of endemic animal species, might have particularly drastic consequences.
Possible Sites Appropriate For Use Of P. Clarkii In Biological Control
Thousands of small man-made impoundments or rain-filled pools exist throughout rural Kenya and are heavily used as a source of water for domestic purposes and for watering livestock. These habitats are often heavily polluted by human or domestic animal wastes, and are frequently populated with disease-transmitting snails and/or mosquitoes (Ripert and Raccurt 1987, Jewsberry and Imbevore 1988). Insofar as such habitats are already extensively modified by intense usage, often in ways that promote disease transmission, they may be ideal candidates for receiving crayfish in schistosomiasis control operations. Another category of habitat that should be considered as possible introduction sites are polluted streams that are located within drainage basins in which crayfish are already abundant (for example, the upper basin of the Athi River).
Additional research addressing the points raised below should be undertaken before any introductions are contemplated, with both appropriate local and national authorities involved in the decision-making process. In general, experience should be gathered regarding the desirability of crayfish introductions in candidate habitats in regions within Kenya in which crayfish already are present. Particular attention should be given to the effects of crayfish activities such as burrowing on the structural integrity of dams and on the suitability of water for human consumption. Based on these experiences, decisions should then be made regarding possible introduction in suitable habitats within areas such as the coastal lowlands where crayfish are not known to be present. We presently do not advocate the introduction of crayfish for snail control into countries where they are not already found.
Conclusion And Priorities For Future Study
The potential environmental ramifications of further P. clarkii introductions that have been highlighted here underscore the need for additional study. Current concerns regarding the protection of natural ecosystems, the maintenance of biodiversity, and the protection of rare endemic species should give pause to anyone contemplating additional introductions of this exotic species into East Africa. These very real concerns must, however, be balanced by the realization that a species such as P. clarkii offers the potential of increased economic opportunity and improved public health. Furthermore, P. clarkii is, for better or worse, already firmly established in Kenya and may well increase its present range, irrespective of human activity. Bearing this in mind, further studies should focus on how to best manage this resource, and how to take maximum advantage of its positive attributes while keeping its environmental effects to a minimum.
Potential Avenues For Further Study
1. The ability of P. clarkii to reduce actual schistosome transmission. Although P. clarkii can control schistosome-transmitting snails in the laboratory and in field enclosures, this by no means ensures that it can actually reduce schistosomiasis transmission in complex natural foci of infection. That P. clarkii can actually reduce incidence and prevalence of both S. mansoni and S. haematobium in human populations in an endemic area should be clearly demonstrated before any decision to use P. clarkii in large-scale control programs. Such field trials might best be conducted in small man-made impoundments or quarry pits, for reasons specified above.
2. Effects of P. clarkii on the abundance and species composition of mosquito larvae. It is intriguing to consider what effect crayfish, used to control schistosomes, might have on the transmission of mosquito-borne diseases such as malaria, filariasis, and arboviral infections. Because it has the capacity to alter aquatic habitats by consuming macrophytes, P. clarkii has been suggested as a means of controlling mosquitoes in California marshes (Feminella and Resh 1986). In tropical Africa, the effect on mosquito breeding might be positive or negative, depending on the tendency of a particular mosquito species to breed in open or shaded water.
3. Are commercially available pesticides used in rice cultivation effective in controlling the spread of P. clarkii? Crayfish are absent from major Kenyan rice growing schemes, possibly due to the use of certain pesticides such as Furadan® to control insect pests. Even if P. clarkii should prove highly successful as a means of controlling schistosomes, its presence in rice fields would probably be counterproductive, owing to its ability to consume rice seedlings. Studies should be initiated to determine whether Furadan® or other pesticides that are routinely used for agricultural purposes can be used to eliminate crayfish from areas where they pose economic or environmental risks.
4. Assessment of the effects of P. clarkii on other components of the aquatic environment. Careful studies are required to ascertain how P. clarkii introductions might effect non-target species. With such information available, decisions about the use of crayfish for snail control can be better evaluated. Special care should be taken to elucidate how crayfish introductions might affect endangered aquatic species.
5. What factors control the present distribution of P. clarkii in Kenya? Is its distribution likely to expand? Procambarus clarkii is absent from large areas of Kenya, and it is unclear to what degree various biotic and abiotic factors interact to explain this distribution. A clearer understanding of these factors would ensure a greater likelihood of success in snail control operations and would make predictions about its capacity for environmental damage more valid.
The authors thank Dr. John H. Ouma, Director, Division of Vector Borne Diseases for his valuable comments. We also thank Mr. N. Odero, Director, Mr. R. Kundu, Mr. J.W. Kariuki, Mr. J. Arunga, Mr. B. Ogilo, and Mr. H. Murunga, all of the Kenya Fisheries Department, and Mr. A.A. Mohdhar, Kenya National Irrigation Board, for providing helpful insights. Dr. Rene Haller and Ms. Sabine Baer of Baobab Farms Ltd., in Bamburi, also provided helpful comments. This paper is published with the approval of the Director of the Kenya Medical Research Institute. The research was supported under Grant No. DPE-5542-G-SS-6018-00, Program in Science and Technology Cooperation, Office of Research, U.S. Agency for International Development. The authors also wish to thank the Office of Research, USAID, for funding the network meeting and the publication of this paper.
Brown, D.S. 1980. Freshwater Snails of Africa and Their Medical Importance. Taylor and Francis,
Brown, D.S., J.E. Jelnes, G.K. Kinoti, and J.H. Ouma. 1981. Distributions in Kenya of intermediate hosts for Schistosoma. Trop. Geogr. Med. 33:95-103.
Butterworth, A.E., P.R. Dalton, D.W. Dunne, M. Mugambi, J.H. Ouma, B.A. Richardson, T.K.
Siongok, and R.F. Sturrock. 1984. Immunity after treatment of human schistosomiasis mansoni. I. Study design, pretreatment observations and the results of treatment. Trans. R. Soc. Trop. Med. Hyg. 78:108-123. Carpenter, S.R. and D.E. Lodge. 1986. Effects of submersed macrophytes on ecosystem processes Aquat. Bot. 26:341-370.
Diesfeld, H.J. and H.K. Hecklau. 1978. Kenya - A Geomedical Monograph. Springer-Verlag, Heidelberg.
Feminella, J.W. and V.H. Resh. 1986. Effects of crayfish grazing on mosquito refuge at Coyote Hills Marsh. Proc. Calif. Mosquito Vector Control Assoc. 54: 101 - 104.
Feminella, J.W. and V.H. Resh. 1989. Submersed macrophytes and grazing crayfish: an experimental study of herbivory in a California freshwater marsh. Holarct. Ecol. 12:1-8.
Highton, R.B. 1974. Schistosomiasis. pp.347-355. in Vogel, L.C., A.S. Muller, R.S. Odingo, Z. Onyango, and A. De Gues (ed.). Health and Disease in Kenya. East African Literature Bureau, Nairobi.
Hobbs, H.H. 1988. Crayfish distribution, adaptive radiation, and evolution. pp.52-82. in Holdich, D.M. and R.S. Lowery (ed.). Freshwater Crayfish. Croom and Helm, London.
Hobbs, H.H., J.P. Jas, and J.V. Huner. 1989. A review of global crayfish introductions with particular emphasis on two North American species (Decapoda, Carnbaridae). Crustaceana 56:299-316.
Hofkin, B.V., G.M. Mkoji, D.K. Koech, and E.S. Loker. 1991. Control of schistosome-transmitting snails in Kenya by the North American crayfish Procambarus clarkii. Am. J. Trop. Med. Hyg. 45:339-344.
Huner, J.V. 1988. Procambarus in North America and elsewhere. pp.239-261. in Holdich, D.M and R.S. Lowery (ed.). Freshwater Crayfish. Croom and Helm, London.
Iarotski, L.S. and A. Davis. 1981. The schistosomiasis problem in the world: results of a WHO questionnaire survey. Bull. WHO 59:115-127.
Jewsberry, J.M. and A.M.A. Imbevore. 1988. Small dam health studies. Parasitol. Today 4:57-59.
King, C.H., G. Lombardi, C. Lombard, R. Greenblatt, H. Kinyanjui, J.H. Ouma, O. Omondi, P.J. Bryan, J. Muruka, P. Magak, D. Weinert, W. MacKay, D. Ransohoff, H. Houser, D. Koech, T.K. Singok, and A.A.F. Mahmoud. 1988. A chemotherapy based approach to control of infection and morbidity in Schistosoma haematoblum. Am. J. Trop. Med. Hyg. 39:295-305.
Klumpp, R.K and K.Y. Chu. 1987. Focal mollusciciding: an effective way to augment chemotherapy of schistosomiasis. Parasitol. Today 3:74-76.
Lodge, D.M. and J.G. Lorman. 1986. Reductions in submersed macrophyte biomass and species richness by the crayfish Orconectes rusticus. Can. J. Fish. Aquat. Sci. 44:591-597.
Lowery, R.S. and A.J. Mendes. 1977a. Procambarus clarhai in Lake Naivasha, Kenya and its effects on established and potential fisheries. Aquaculture 11:111-121.
Lowery, R.S. and A.J. Mendes. 1977b. The Louisiana red swamp crayfish in Kenya. East Afr. Nat. Hist. Soc. Bull. Jan.-Feb. :9-11.
Madsen, H. 1990. Biological methods for the control of freshwater snails. Parasitol. Today 6:237-241.
Miltner, M. and J.W. Avault. 1980. Rice and millet as forages for crawfish. Louisiana Agric. 24:8-10.
Mott, K.E. 1987. Schistosomiasis control. in Rollinson, D. and A.J.G. Simpson. (ed.). Ihe Biology of Schistosomes. Academic Press, London.
Olouch, A.O. 1990. Breeding biology of the Louisiana red swamp crayfish Procambarus clarkii Girard in Lake Naivasha, Kenya. Hydrobiologia 208:85-92.
Ouma, J.H., J.D.B. Wijers, and T.K. Siongok. 1985. The effect of repeated targeted mass treatment on the prevalence of Schistosoma mansoni and the intensity of infection in Machakos, Kenya. Ann. Trop. Med. Parasitol. 79:431-438.
Parker, I.S.C. 1974. The Status of the Louisiana Red Swamp Crayfish, Procambarus clarkii in Lake Naivasha. Wildlife Services, Nairobi.
Ripert, C.L and C.P. Raccurt. 1987. The impact of small dams on parasitic diseases in Cameroon. Parasitol. Today 3:287-289.
Rollinson, D. and A.J.G. Simpson (ed.). 1987. The Biology of Schistosomes. Academic Press, London.
Sher, A., S.L. James, R. Correa-Oliveira, S. Hieny, and E. Pierce. 1989. Schistosome vaccines: current progress and future prospects. Parasitology 98:61-67.
Sogandares-Bernal, F. 1965. Parasites from Louisiana crayf~shes. Tulane Stud. Zool. 12:79-85.
Wilkins, H.A. 1987. The epidemiology of schistosomiasis in man. pp. 379-397. in Rollinson, D. and A.J.G. Simpson (ed.). The Biology of Schistosomes. Academic Press, London.
Woolhouse, M.E.J. and S.K. Chandiwana. 1989. Spatial and temporal heterogeneity in the population dynamics of Bulinus globosus and Biomphalariapfeifferi and the epidemiology of their infection with schistosomes. Parasitology 98:21-34.