Gastropod-borne trematode communities of man-made reservoirs in Zimbabwe, with a special focus on Fasciola and Schistosoma helminth parasites

Ruben Schols
Persbericht

De verborgen passagiers in het nijlpaard

Voor ik het goed en wel besefte zat ik met mijn medestudente Kudzai in een tot de nok gevulde versleten wagen samen met negen soldaten. Het was een vreemd beeld dat me altijd zal bijblijven: ik, als bioloog, met een dissectie setje op de schoot, naast een gewapende soldaat met een hand vol kogels. Hij vond de munitie bovendien uitermate geschikt als wattenstaafje en pulkte er regelmatig mee in zijn oor. Na een hobbelige rit over smalle zandweggetjes kwamen we aan op de locatie. Hier lag het dan, het dier waar ik al dagen op zat te wachten.

Hoe ben ik hier terecht gekomen?

Het verhaal begint eind 2017 toen onderzoekers van het Afrikamuseum op een ongewone zoetwaterslak stuitten tijdens een exploratie in het Karibameer in Zimbabwe. Deze slak is afkomstig uit Noord Amerika, en bleek een onbekende leverbot parasiet met zich mee te dragen. De naam verraadt het al, de leverbot leeft in de lever van vele dieren, gaande van mensen en koeien tot giraffen en nijlpaarden. De onderzoekers vonden dat een uitzonderlijk hoog aantal van deze zoetwaterslakken besmet waren met deze worm, wat betekent dat de infectiedruk zeer hoog ligt. Maar wie de uiteindelijke eindgastheer was, bleef een raadsel. Het doel van mijn thesis was dit mysterie op te lossen. We besloten ons te focussen op het nijlpaard om twee voorname redenen. Ten eerste zijn ze enorm talrijk in het Karibameer en ten tweede bestaat er een leverbot specifiek voor het nijlpaard waar bijna niets over geweten is.

Figure 1

De leverbot heeft een complexe levenscyclus. Via stoelgang van de gastheer komen eitjes in water terecht waar ze zoetwaterslakken infecteren. Binnen de slak ontwikkelen ze zich tot larven. Wanneer ze volwassen zijn, verlaten ze de slak en hechten ze zich geduldig vast aan waterplanten. Wanneer mensen of dieren deze besmette planten opeten, ontwikkelen de larven zich tot volwassen leverbotwormen in de lever van hun finale gastheer waar ze eitjes gaan leggen. Zo kan de cyclus weer opnieuw beginnen.

Bron: sciencejournalforkids.org/articles/why-do-invasive-species-like-artificial-lakes/

 

image 381Het Karibameer vormt deels de grens tussen Zambia en Zimbabwe en is op basis van volume het grootste kunstmatige meer ter wereld. Op locaties 3 en 16 verzamelden we slakken en hun parasieten.

Bron: sciencejournalforkids.org/articles/why-do-invasive-species-like-artificial-lakes/

 

Het verlossende telefoontje

Maandag kwamen Kudzai en ik aan in Kariba en zaterdag ochtend om 5 uur zouden we alweer moeten vertrekken naar Harare, de hoofdstad van Zimbabwe. De park wachters die het natuurreservaat van Kariba beschermen tegen stropers, krijgen elk jaar een quotum aan wilde dieren om te schieten. Ze schieten de dieren om de populaties in evenwicht te houden maar ook als een vorm van verloning. Ze zouden ons contacteren wanneer ze een nijlpaard gingen doden. We moesten daarom zorgen dat we de komende dagen steeds bereikbaar waren. De spanning was daardoor te snijden en veel slaap zat er voor ons niet in. De dagen vlogen voorbij en tegen donderdag had ik voldoende slakken verzameld. Jammer genoeg was er nog geen nieuws van de wachters. Vol spanning plakte ik vrijdag, als het ware, aan mijn gsm. Tegen de avond was er nog steeds geen nieuws en de moed zakte me in de schoenen. Na het avondeten kwam dan toch het verlossende telefoontje. Een kwartier later zat ik in die versleten wagen naast de soldaat met zijn hand vol kogels op weg naar het nijlpaard.

De verborgen passagiers

De wachters verwerkten het nijlpaard in ijltempo en ondertussen onderzochten Kudzai en ik zoveel mogelijk organen op platwormen. Bij de eerste incisie in de lever vonden we ongelooflijk genoeg meteen twee leverbot wormen. Bovendien kregen we de kans om ook een deel van de maag te onderzoeken. Op de maagwand troffen we een duizendtal platwormen aan, behorende tot twee verschillende soorten.

 

image 382

De drie verschillende platwormen gevonden in het nijlpaard. Foto A is de gevonden leverbot. In ware grootte is deze parasiet meer dan 10 cm lang. Bovendien werden er nog twee andere soorten platwormen gevonden in de maag (B en C). Hiervan bleek C het talrijkste met bijna duizend individuen op een stukje maagwand ter grootte van een A4 papier.

 

Het detective werk

Eens terug in België, onderzochten we het DNA van deze wormen en vergeleken dit met parasitair-DNA gevonden in de vorige studie. Op deze manier konden we de levenscyclus reconstrueren - zoals echte detectives - en bleken de exotische slakken twee van de drie gevonden platwormsoorten (soorten A en B in de figuur) over te dragen op het nijlpaard. Bovendien was het inderdaad de verwachtte nijlpaard-specifieke leverbot waar weinig over geweten is. Daarom namen we foto’s van de volwassen wormen en gaan we het DNA online beschikbaar maken. Hierdoor kunnen toekomstige studies eenvoudiger DNA van deze soort uit stoelgang, slakken of volwassen platwormen identificeren.

figuur 4

Nijlpaarden voelen zich veilig in het water. Zolang we hun kortste weg naar het water niet blokkeren zijn we veilig, al moeten we dan nog steeds opletten voor de talrijke krokodillen die ons rauw lusten.

 

De gevolgen voor het nijlpaard

Voorlopig is er nog niet veel geweten over de schade die deze wormen aanrichten in het nijlpaard. Als we kijken naar de ernstige problemen die nauw verwante soorten veroorzaken in bijvoorbeeld koeien en mensen, voorspelt dit niet veel goeds. Zo veroorzaken leverbot infecties inwendige bloedingen en verlagen ze de vruchtbaarheid. In Zimbabwe staan nijlpaardpopulaties, net zoals in de meeste delen van Afrika, onder druk door illegale jacht en habitatverlies. Daarom staat de soort sinds 2006 op de rode lijst van de IUCN als ‘kwetsbaar’ geclassificeerd. Populaties die verzwakt zijn door ziektes zijn extra kwetsbaar voor andere bedreigingen. Daarom is er meer onderzoek nodig naar de verspreiding van deze parasiet. Mede dankzij onze resultaten kan dit nu gebeuren door DNA te isoleren uit slakken en stoelgang zonder een nijlpaard te moeten doden.

Heb je misschien de kriebels gekregen van al die wormen? Geen nood, want voor mensen in België is de kans op infectie tegenwoordig minimaal. Als je dan toch een tropische reis plant, kan het echter geen kwaad om je goed te informeren.

Bibliografie

Alicata, J. E., 1938. Observations on the life history of Fasciola gigantica, the common liver fluke of cattle in Hawaii, and the intermediate host, Fossaria ollula. Honolulu: University of Hawaii.
Anuracpreeda, P., Wanichanon, C. and Sobhon, P., 2008. Paramphistomum cervi: Antigenic profile of adults as recognized by infected cattle sera. Experimental Parasitology. 118, 203–207. doi: 10.1016/j.exppara.2007.08.005.
Appleton, C. C., 2003. Alien and invasive fresh water gastropoda in south africa. African Journal of Aquatic Science. 28, 69–81. doi: 10.2989/16085914.2003.9626602.
Appleton, C. C., Hofkin, B. V. and Baijnath, A., 2004. Macro-invertebrate predators of freshwater pulmonate snails in Africa, with particular reference to Appasus grassei (Heteroptera) and Procambarus clarkii (Decapoda). African Journal of Aquatic Science. 29, 185–193. doi: 10.2989/16085910409503809.
Appleton, C. C. and Miranda, N. A. F., 2015. Two Asian freshwater snails newly introduced into south Africa and an analysis of alien species reported to date. African Invertebrates. 56, 1–17. doi: 10.5733/afin.056.0102.
Armstrong, J. C., 1965. Mating Behavior and Development of Schistosomes in the Mouse. American Journal of Tropical Medicine and Hygiene. 51, 605–616. doi: 10.2307/3276242.
Bargues, M. D. et al., 2011. DNA sequence characterisation and phylogeography of Lymnaea cousini and related species, vectors of fasciolosis in northern Andean countries, with description of L. meridensis n. sp. (Gastropoda: Lymnaeidae). Parasites and Vectors. 4, 1–22. doi: 10.1186/1756-3305-4-132.
Barriel, V. and Tassy, P., 1998. Rooting with multiple outgroups: consensus versus parsimony. Cladistics. 14, 193–200. doi: 10.1006/clad.1998.0067.
Bennema, S. et al., 2009. The use of bulk-tank milk ELISAs to assess the spatial distribution of Fasciola hepatica, Ostertagia ostertagi and Dictyocaulus viviparus in dairy cattle in Flanders (Belgium). Veterinary Parasitology. 165, 51–57. doi: 10.1016/j.vetpar.2009.07.006.
Bickle, Q. D. et al., 1985. Resistance against Schistosoma mansoni induced by highly irradiated infections: studies on species specificity of immunization and attempts to transfer resistance. Parasitology. 90, 301–312. doi: 10.1017/S0031182000051003.
Blackie, W. K., 1932. A helminthological survey of Southern Rhodesia. London: No. 5 of the Memoir Series of the London School of Hygiene and Tropical Medicine.
De Bont, J. and Vercruysse, J., 1998. Schistosomiasis in cattle. Advances in Parasitology. 41, 285–364. doi: 10.1016/S0065-308X(08)60426-1.
Brant, S. V and Loker, E. S., 2009. Molecular systematics of the avian schistosome genus Trichobilharzia (Trematoda: Schistosomatidae) in North America. The Journal of parasitology. 95, 941–963. doi: 10.1645/GE-1870.1.
Brecko, J. et al., 2014. Focus stacking: comparing commercial top-end set-ups with a semi-automatic low budget approach. A possible solution for mass digitization of type specimens. ZooKeys. 464, 1–23. doi: 10.3897/zookeys.464.8615.
Carolus, H. et al., 2019. A cascade of biological invasions and parasite spillback in man-made Lake Kariba. Science of The Total Environment. 659, 1283–1292. doi: 10.1016/j.scitotenv.2018.12.307.
Cetron, M. S. et al., 1996. Schistosomiasis in Lake Malawi. The Lancet. 348, 1274–1278. doi: 10.1016/S0140-6736(96)01511-5.
Chandiwana, S. K., Taylor, P. and De. Clarke, V. V., 1988. Prevalence and intensity of schistosomiasis in two rural areas in Zimbabwe and their relationship to village location and snail infection rates. Annals of Tropical Medicine and Parasitology. 82, 163–173. doi: 10.1080/00034983.1988.11812224.
Chandiwana, S. K., Taylor, P. and Makura, O., 1987. Prevalence and distribution of Schistosoma mattheei in Zimbabwe. Annales van de Belgische vereniging voor tropische geneeskunde. 67, 167–172.
Christensen, N. O., Mutani, A. and Frandsen, F., 1983. A review of the biology and transmission ecology of African bovine species of the genus Schistosoma. Zeitschrift fur Parasitenkunde. 69, 551–570.
Christian Mage et al., 2002. Fasciola hepatica and Paramphistomum daubneyi: changes in prevalences of natural infections in cattle and in Lymnaea truncatula from central France over the past 12 years. Veterinary Research. 33, 439–447. doi: 10.1051/vetres:2002030.
Civitello, D. J. et al., 2015. Biodiversity inhibits parasites: broad evidence for the dilution effect. Proceedings of the National Academy of Sciences. 112, 8667–8671. doi: 10.1073/pnas.1506279112.
Clement, M. et al., 2002. TCS: estimating gene genealogies. Parallel and Distributed Processing Symposium, International Proceedings. 2, 184.
62
Correa, A. C. et al., 2011. Morphological and molecular characterization of Neotropic Lymnaeidae (Gastropoda: Lymnaeoidea), vectors of fasciolosis. Infection, Genetics and Evolution. 11, 1978–1988. doi: 10.1016/j.meegid.2011.09.003.
Cridland, C. C., 1967. Resistance of Bulinus (Physopsis) globosus, Bulinus (Ph.) africanus, Biomphalaria pfeifferi and Lymnaea natalensis to experimental desiccation. Bulletin of the World Health Organization. 36, 507–513.
Degeorges, A. and Reilly, B., 2007. Politicization of land reform in Zimbabwe: impacts on wildlife, food production and the economy. International Journal of Environmental Studies. 64, 571–586. doi: 10.1080/00207230701494589.
Detwiler, J. T., Bos, D. H. and Minchella, D. J., 2010. Revealing the secret lives of cryptic species: Examining the phylogenetic relationships of echinostome parasites in North America. Molecular phylogenetics and evolution. 55, 611–620. doi: 10.1016/j.ympev.2010.01.004.
Díaz, S., Settele, J. and Brondizio, E., 2019. Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the intergovernmental science-policy platform on biodiversity and ecosystem services. IPBES.
Dinnik, J. A. and Dinnik, N. N., 1961. On the morphology and life history of Fasciola nyanzae Leiper, 1910 from the hippopotamus. Journal of Helminthology. 53–62.
Doumenge, J., 1987. Atlas of the global distribution of schistosomiasis. WHO.
Ebbs, E. T., Loker, E. S. and Brant, S. V, 2018. Phylogeography and genetics of the globally invasive snail Physa acuta Draparnaud, 1805, and its potential to serve as an intermediate host to larval digenetic trematodes. BMC Evolutionary Biology. 18, 1–17. doi: 10.1186/s12862-018-1208-z.
Elton, C. S., 1958. The ecology of invasions by animals and plants. London.
Forsyth, D. M. and Macdonald, G., 1965. Urological complications of endemic schistosomiasis in school-children. Transactions of the Royal Society of Tropical Medicine and Hygiene. 59, 171–178.
Frandsen, F., 1980. A practical guide to the identification of African freshwater snails. (World Health Organization, Danish Bilharziasis Laboratory).
Frandsen, F. and Christensen, N. Ø., 1984. An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Tropica. 41, 181–202. doi: 10.5169/seals-313293.
Furstenburg, D., 2012. Focus on the hippopotamus (Hippopotamus amphibious).
Giannelli, A. et al., 2016. gastropod-borne helminths: a look at the snail-parasite interplay. Trends in Parasitology. 32, 255–264. doi: 10.1016/j.pt.2015.12.002.
Gibson, D., 1996. Guide to the parasites of fishes of Canada: Trematoda. Edited by L. Margolis and Z. Kabata. Canadian Special Publication of Fisheries and Aquatic Sciences.
Gibson, D., Jones, A. and Bray, R., 2002. Keys to the Trematoda. CAB International.
Gómez, A. and Nichols, E., 2013. Neglected wildlife: parasitic biodiversity as a conservation target. International Journal for Parasitology: Parasites and Wildlife. 2, 222–227. doi: 10.1016/j.ijppaw.2013.07.002.
Gower, C. M., Vince, L., Webster, J. P., 2017. Should we be treating animal schistosomiasis in Africa? The need for a one health economic evaluation of schistosomiasis control in people and their livestock. Transactions of the Royal Society of Tropical Medicine and Hygiene. 111, 244–247. doi: 10.1093/trstmh/trx047.
Grabner, D. S. et al., 2014. Invasion biology meets parasitology: A case study of parasite spill-back with Egyptian Fasciola gigantica in the invasive snail Pseudosuccinea columella. PLoS ONE. 9, 1–7. doi: 10.1371/journal.pone.0088537.
Halstead, N. T. et al., 2018. Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts. Nature Communications. 9, 1–10. doi: 10.1038/s41467-018-03189-w.
Hanelt, B. et al., 2009. Schistosoma kisumuensis n. sp. (Digenea: Schistosomatidae) from murid rodents in the Lake Victoria Basin, Kenya and its phylogenetic position within the S. haematobium species group. Parasitology. 136, 987–1001. doi: 10.1017/S003118200900643X.
Hanna, R. E. B. et al., 1988. Seasonal reproduction in Paramphistomum epiclitum and Gastrothylax crumenifer, rumen paramphistomes of the Indian water buffalo, and comparison with the biliary paramphistome Gigantocotyle explanatum. International Journal for Parasitology. 18, 513–521. doi: https://doi.org/10.1016/0020-7519(88)90016-1.
Havel, J. E., Lee, C. E. and Vander Zander, M. J., 2005. Do reservoirs facilitate invasions into landscapes? BioScience. 55, 518–525. doi: 10.1641/0006-3568(2005)055[0518:DRFIIL]2.0.CO;2.
63
Heard, M. J. et al., 2013. Increased threat of disease as species move towards extinction. Conservation Biology. 27, 1378–1388. doi: 10.1111/cobi.12143.Increased.
Hebert, P. et al., 2003. Biological identification through DNA barcodes. Proceedings of the Royal Society of London B. 270, 313–321.
Hoa Le, T. et al., 2008. Human fasciolosis and the presence of hybrid/introgressed forms of Fasciola hepatica and Fasciola gigantica in Vietnam. International Journal for Parasitology. 38, 725–730. doi: 10.1016/j.ijpara.2007.10.003.
Hopkins, R. D., 1992. Homing in on Helminths. The American Journal of Tropical Medicine and Hygiene. 46, 626–634.
ten Hove, R. J. et al., 2008. Multiplex real-time PCR for the detection and quantification of Schistosoma mansoni and S. haematobium infection in stool samples collected in northern Senegal. Transactions of the Royal Society of Tropical Medicine and Hygiene. 102, 179–185. doi: 10.1016/j.trstmh.2007.10.011.
Huyse, T. et al., 2009. bidirectional introgressive hybridization between a cattle and human schistosome species. PLoS PATHOGENS. 5: e1000571. doi: 10.1371/journal.ppat.1000571.
Huyse, T., den Broeck, F. Van, et al., 2013. Hybridisation between the two major African schistosome species of humans. International Journal for Parasitology. 43, 687–689. doi: 10.1016/j.ijpara.2013.04.001.
Huyse, T., Van den Broeck, F., et al., 2013. Regular treatments of praziquantel do not impact on the genetic make-up of Schistosoma mansoni in Northern Senegal. Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases. 18, 100–105. doi: 10.1016/j.meegid.2013.05.007.
Itagaki, T. et al., 2005. Genetic characterization of parthenogenic Fasciola sp. in Japan on the basis of the sequences of ribosomal and mitochondrial DNA. Parasitology. 131, 679–685. doi: 10.1017/S0031182005008292.
Itagaki, T. et al., 2009. Occurrence of spermic diploid and aspermic triploid forms of Fasciola in Vietnam and their molecular characterization based on nuclear and mitochondrial DNA. Parasitology international. 58, 81–85. doi: 10.1016/j.parint.2008.11.003.
Jackson, H. G., 1921. A revision of the genus Fasciola.
Khalifa, R. M. et al., 2016. Molecular and phylogenic characterization of Fasciola hepatica from Assiut, Egypt based on nuclear ribosomal DNA sequences. Journal of medical science and clinical research. 04, 9007–9009. doi: 10.18535/jmscr/v4i1.38.
King, C. H. and Dangerfield-Cha, M., 2008. The unacknowledged impact of chronic schistosomiasis. Chronic Illness. 4, 65–79. doi: 10.1177/1742395307084407.
King, K. C. et al., 2015. Hybridization in parasites: consequences for adaptive evolution, pathogenesis, and public health in a changing world. PLoS Pathogens. 11, 1–12. doi: 10.1371/journal.ppat.1005098.
King, K. C. and Lively, C. M., 2012. Does genetic diversity limit disease spread in natural host populations. Heredity. 109, 199–203. doi: 10.1038/hdy.2012.33.
Kuris, A. M. et al., 2008. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature. 454, 515–518. doi: 10.1038/nature06970.
Laidemitt, M. R. et al., 2016. Loads of trematodes: discovering hidden diversity of paramphistomoids in Kenyan ruminants. Parasitology. 144, 131–147. doi: 10.1017/S0031182016001827.
Leiper, R. T., 1910. The Entozoa of the hippopotamus. Proceedings of the Zoological Society of London. 233–251.
Lerer, L. B. and Scudder, T., 1999. Health impacts of large dams. Environmental Impact Assessment Review. 19, 113–123. doi: 10.1016/S0195-9255(98)00041-9.
Librado, P. and Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 25, 1451–1452. doi: 10.1093/bioinformatics/btp187.
Lounnas, M. et al., 2017. Self-fertilization, long-distance flash invasion and biogeography shape the population structure of Pseudosuccinea columella at the worldwide scale. Molecular Ecology. 26, 887–903. doi: 10.1111/mec.13984.
Lydeard, C. et al., 2004. The global decline of nonmarine mollusks. BioScience. 54, 321–330. doi: 10.1641/0006-3568(2004)054[0321:TGDONM]2.0.CO;2.
Mahmoud, A. A. F., 2001. Schistosomiasis. volume 3. Edited by G. Pasvol and S. Hoffman. Tropical Medicine Science and Practice.
Mandahl-Barth, G., 1962. Key to the identification of East and Central African freshwater snails of medical and veterinary importance. Bulletin of the world health organization. 27, 135–150.
Mas-coma, S., 2004. human fascoliasis: epidemiological patterns in human endemic areas of South America, Africa and Asia. The Southeast Asian journal of tropical medicine and public health. 35, 1–11.
64
Mas-Coma, S., Valero, M. A. and Bargues, M. D., 2009. Chapter 2 Fasciola, lymnaeids and human fasciolosis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology. 69, 41–146. doi: 10.1016/S0065-308X(09)69002-3.
McAllister, D. E. et al., 2001. Biodiversity Impacts of Large Dams.
de Meeûs, T., Prugnolle, F. and Agnew, P., 2007. Asexual reproduction: genetics and evolutionary aspects. Cellular and Molecular Life Sciences. 64, 1355–1372. doi: 10.1007/s00018-007-6515-2.
Mehmood, K. et al., 2017. A review on epidemiology, global prevalence and economical losses of fasciolosis in ruminants. Microbial Pathogenesis. 109, 253–262. doi: 10.1016/j.micpath.2017.06.006.
Michelson, E. H., 1989. Schistosomiasis in Zambia: an historical overview and review of the literature. African journal of medicine and medical sciences. 18, 269–281.
Mitchell, D. R. and Leung, T. L. F., 2016. Sharing the load: a survey of parasitism in the invasive freshwater pulmonate, Physa acuta (Hygrophila: Physidae) and sympatric native snail populations. Hydrobiologia. 766, 165–172. doi: 10.1007/s10750-015-2452-5.
Mitta, G. et al., 2011. Compatibility polymorphism in snail/schistosome interactions: from field to theory to molecular mechanisms. Developmental and comparative immunology. 37, 1–8. doi: 10.1016/j.dci.2011.09.002.
Morgan, J. A. T. et al., 2001. Schistosoma mansoni and Biomphalaria: past history and future trends. Parasitology. 123, S211-28. doi: 10.1017/S0031182001007703.
Morgan, J. A. T. et al., 2003. A newly-identified lineage of Schistosoma. International Journal for Parasitology. 33, 977–985. doi: 10.1016/S0020-7519(03)00132-2.
Morley, N. J., 2007. Anthropogenic effects of reservoir construction on the parasite fauna of aquatic wildlife. EcoHealth. 4, 374–383. doi: 10.1007/s10393-007-0130-4.
Mucheka, V. T. et al., 2015. DNA sequence analyses reveal co-occurrence of novel haplotypes of Fasciola gigantica with F. hepatica in South Africa and Zimbabwe. Veterinary Parasitology. 214, 144–151. doi: 10.1016/j.vetpar.2015.09.024.
Mukaratirwa, S. et al., 1998. Genetic and morphological variation of populations belonging to the Bulinus truncatus/tropicus complex (Gastropoda: Planorbidae) in South Western Zimbabwe. Journal of molluscan studies. 64, 435–446.
Mukaratirwa, S. et al., 2004. Susceptibility of 7 freshwater gastropod species in Zimbabwe to infection with Gastrodiscus aegyptiacus (Cobbold, 1876) Looss, 1896. Journal of the South African Veterinary Association. 75, 186–188.
Muller, M., 2019. Hydropower dams can help mitigate the global warming impact of wetlands. Nature. 566, 315–317.
Mutapi, F. et al., 2017. Human schistosomiasis in the post mass drug administration era. The Lancet Infectious Diseases. 17, e42–e48. doi: https://doi.org/10.1016/S1473-3099(16)30475-3.
Needham, A. J. E., 1977. Observations on the economics of treatment of Fasciola gigantica in cattle in Rhodesia. Rhodesia veterinary journal. 8, 14–20.
Nei, M. and Kumar, S., 2000. Molecular evolution and phylogenetics. Oxford university press.
Nelson, G. S., 1960. Schistosome infections as zoonoses in Africa. The Royal Society of Tropical Medicine and Hygiene. London. 54, 301–316.
Nguyen, T. B. N. et al., 2018. Distribution status of hybrid types in large liver flukes, Fasciola species (Digenea: Fasciolidae), from ruminants and humans in Vietnam. The Korean journal of parasitology. 56, 453–461. doi: 10.3347/kjp.2018.56.5.453.
Nolan, M. J. and Cribb, T. H., 2005. The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in parasitology. England. 60, 101–163. doi: 10.1016/S0065-308X(05)60002-4.
Pages, J.-R. and Théron, A., 1990. analysis and comparison of cercarial emergence rhythms of Schistosoma haematobium, S. intercalatum, S. bovis, and their hybrid progeny. International Journal for Parasitology. 20, 193–197.
Pfenninger, M., Cordellier, M. and Streit, B., 2006. Comparing the efficacy of morphologic and DNA-based taxonomy in the freshwater gastropod genus Radix (Basommatophora, Pulmonata). BMC Evolutionary Biology. 6, 1–14. doi: 10.1186/1471-2148-6-100.
Pfukenyi, D. M. et al., 2006. Epidemiological studies of Fasciola gigantica infections in cattle in the highveld and lowveld communal grazing areas of Zimbabwe. Onderstepoort Journal of Veterinary Research. 73, 37–51.
Pfukenyi, D. M. and Mukaratirwa, S., 2018. Amphistome infections in domestic and wild ruminants in East and Southern Africa: a review. Onderstepoort Journal of Veterinary Research. 85, 1–13.
65
Pitchford, R. J. et al., 1969. Cercarial shedding patterns of various schistosome species under outdoor conditions in the Transvaal. Annals of Tropical Medicine & Parasitology. 63, 359–371. doi: 10.1080/00034983.1969.11686637.
Pitchford, R. J., 1976. preliminary observations on the distribution, definitive hosts and possible relation with other schistosomes, of Schistosoma Margrebowiei, le Roux, 1933 and Schistosoma Leiperi, le Roux, 1955. Journal of Helminthology. 50, 111–123. doi: 10.1017/S0022149X00027590.
Rapsch, C. et al., 2006. Estimating the true prevalence of Fasciola hepatica in cattle slaughtered in Switzerland in the absence of an absolute diagnostic test. International Journal for Parasitology. 36, 1153–1158. doi: 10.1016/j.ijpara.2006.06.001.
Ricciardi, A., 2001. Facilitative interactions among aquatic invaders: is an ‘invasional meltdown’ occurring in the Great Lakes? Canadian Journal of Fisheries and Aquatic Sciences. 58, 2513–2525. doi: 10.1139/cjfas-58-12-2513.
Rohr, J. R. et al., 2008. Agrochemicals increase trematode infections in a declining amphibian species. Nature. 455, 1235–1239. doi: 10.1038/nature07281.
Rollinson, D. and Southgate, V. R., 1987. The genus Schistosoma: a taxonomic appraisal. in Rollinson, D. and Simpson, A. (eds) The biology of Schistosomes from Genes to Latrines. London: Academic Press. 1–49.
Le Roux, P. L., 1933. A preliminary note on Bilharzia margrebowiei, a new parasite of ruminants and possibly man in Northern Rhodesia. Journal of Helminthology. 11, 57–62.
Schols, R, et al., Under review. A Multiplex Rapid Diagnostic PCR (RD-PCR) approach for xenomonitoring of human and animal schistosomiases in a One Health context. Transactions of the Royal Society of Tropical Medicine & Hygiene.
Schweizer, G. et al., 2005. Estimating the financial losses due to bovine fasciolosis in Switzerland. Veterinary Record. 157, 188–193. doi: 10.1136/vr.157.7.188.
Schmitt, R. J. P. et al., 2019. Deploy diverse renewables to save tropical rivers. Nature. 569, 330–332.
Sey, O., 1984. Scanning electron microscopic examination of the tegumental surface of some amphistomes (Trematoda: Amphistomida). Parasitologia Hungarica. 17, 45–49.
Sey, O., 2017. CRC Handbook of the Zoology of Amphistomes. CRC Press. doi: 10.1201/9781315150871.
Simberloff, D. and Von Holle, B., 1999. Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions. 1, 21–32. doi: 10.1023/A:1010086329619.
Skerratt, L. et al., 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth. 4, 125–134. doi: 10.1007/s10393-007-0093-5.
Smith, K. F., Acevedo-Whitehouse, K. and Pedersen, A. B., 2009. The role of infectious diseases in biological conservation. Animal Conservation. 12, 1–12. doi: 10.1111/j.1469-1795.2008.00228.x.
Smith, N. F., 2001. Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts. Ecologia. 127, 115–122. doi: 10.1007/s004420000560.
Sokolow, S. H. et al., 2016. global assessment of schistosomiasis control over the past century shows targeting the snail intermediate host works best. PLoS Neglected Tropical Diseases. 10, 1–19. doi: 10.1371/journal.pntd.0004794.
Sokolow, S. H. et al., 2017. Nearly 400 million people are at higher risk of schistosomiasis because dams block the migration of snail-eating river prawns. Philosophical Transactions of the Royal Society B. 372, 20160127. doi: 10.1098/rstb.2016.0127.
Southgate, V. R., van Wijk, H. B. and Wright, C. A., 1976. Schistosomiasis at Loum, Cameroun; Schistosoma haematobium, S. intercalatum and their natural hybrid. Parasitenkunde. 49, 145–159.
Sow, S. et al., 2002. Water-related disease patterns before and after the construction of the Diama dam in northern Senegal. Annals of Tropical Medicine and Parasitology. 96, 575–586. doi: 10.1179/000349802125001636.
Standley, J. C., Dobson, P. A. and Stothard, J. R., 2012. out of animals and back again: schistosomiasis as a zoonosis in Africa. In Schistosomiasis. 209–230. doi: 10.5772/25567.
van Straaten, P., 2000. Mercury contamination associated with small-scale gold mining in Tanzania and Zimbabwe. The Science of the total environment. 259, 105–113.
Stringer, A. P. and Linklater, W., 2014. Everything in moderation: principles of parasite control for wildlife conservation. BioScience. 64, 932–937. doi: 10.1093/biosci/biu135.
Strong, E. E. et al., 2008. Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. Hydrobiologia. 595, 149–166. doi: 10.1007/s10750-007-9012-6.
Sugunan, V. V., 1997. Fisheries management of small water bodies in seven countries in Africa, Asia and Latin America. Rome. Available at: http://www.fao.org/docrep/w7560e/W7560E00.htm.
66
Tchuente, L. A. T. et al., 1994. interspecific stimulation of parthenogenesis in Schistosoma intercalatum and S. mansoni. Journal of Helminthology. 68, 167–173. doi: 10.1017/S0022149X00013717.
Théron, A., 1989. Hybrids between Schistosoma mansoni and S. rodhaini: characterization by cercarial emergence rhythms. Parasitology. 99, 225–228.
Toledo, R. and Fried, B., 2014. Digenetic Trematodes. Springer. doi: 10.1007/978-1-4939-0915-5.
Townsend, C. R., Begon, M. and Harper, J. L., 2008. Essentials of Ecology. Third edit. Oxford: Blackwell Publishing.
Utete, B. et al., 2017. Analysis of the abundance and spatial distribution of the common hippopotamus, (Hippopotamus amphibius) in the Manjirenji Dam, Zimbabwe, to inform conservation and detect human–wildlife conflict hot spots. African Journal of Ecology. 55, 754–759. doi: 10.1111/aje.12407.
Vanwyk, J. A., Rensburg, L. J. V. A. N. and Heitmann, L. P., 1997. Schistosoma mattheei infection in cattle: The course of the intestinal syndrome, and an estimate of the lethal dose of cercariae. Onderstepoort Journal of Veterinary Research. 64, 65–75.
Vareille-Morel, C. et al., 1993. Internal metacercarial cysts of Fasciola hepatica in the pulmonate snail Lymnaea truncatula. Parasitology Research. 79, 259–260.
Vilas, R., Criscione, C. D. and Blouin, M. S., 2005. A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology. 131, 839–846. doi: 10.1017/S0031182005008437.
Webster, B. L. and Southgate, V. R., 2003. Mating interactions of Schistosoma haematobium and S. intercalatum with their hybrid offspring. Parasitology. 123, 327–338. doi: 10.1017/S0031182002002883.
Webster, B. L., Southgate, V. R. and Littlewood, D. T. J., 2006. A revision of the interrelationships of Schistosoma including the recently described Schistosoma guineensis. International Journal for Parasitology. 36, 947–955. doi: 10.1016/j.ijpara.2006.03.005.
Wenseleers, T., 2016. Export: Streamlined Export of Graphs and Data Tables. Available at: https://github.com/tomwenseleers/export
Weyher, A. H. et al., 2010. Molecular Identification of Schistosoma mattheei from feces of kinda (Papio cynocephalus kindae) and grayfoot baboons (Papio ursinus griseipes) in Zambia. Journal of Parasitology. 96, 184–190. doi: 10.1645/GE-2186.1.
WHO, 1982. Manual on environmental management for mosquito control with special emphasis on malaria vectors. Switzerland.
Willmott, S., 1960. The morphology of Brumptia bicaudata (Poirier, 1908) Odhner, 1926 (Trematoda: Paramphistomoidea). Proceedings of the Zoological Society of London. 134, 623–634. doi: 10.1111/j.1469-7998.1960.tb05604.x.
Wright, W. H., 1972. A consideration of economic impact of schistosomiasis. Bulletin of the World Health Organization. 47, 559–565.
You, H. et al., 2018. schistosome vaccines for domestic animals. Tropical Medicine and Infectious Disease. 3, 68. doi: 10.3390/tropicalmed3020068.
Zisadza-Gandiwa, P. et al., 2011. Abundance, distribution and population trends of hippopotamus in Gonarezhou National Park, Zimbabwe. South African Journal of Wildlife Research. 40, 149–157. doi: 10.3957/056.040.0206.
WHO, (2018) Schistosomiasis (Fact sheets), World Health Organization.

Universiteit of Hogeschool
Master in de Biologie
Publicatiejaar
2019
Promotor(en)
Filip Volckaert en Tine Huyse
Kernwoorden
Share this on: