Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-11T01:21:10.141Z Has data issue: false hasContentIssue false
  • English
  • Français

Rodents of Senegal and their role as intermediate hosts of Hydatigera spp. (Cestoda: Taeniidae)

Published online by Cambridge University Press:  28 August 2018

Stefano Catalano Open the ORCID record for Stefano Catalano [Opens in a new window] ,
Khalilou Bâ ,
Nicolas D. Diouf ,
Elsa Léger ,
Guilherme G. Verocai  and
Joanne P. Webster
Stefano Catalano*
Affiliation:
Centre for Emerging, Endemic and Exotic Diseases (CEEED), Department of Pathobiology and Population Sciences, The Royal Veterinary College, University of London, Hatfield AL9 7TA, UK
Khalilou Bâ
Affiliation:
Centre de Biologie et de Gestion des Populations (CBGP), Institut de Recherche pour le Développement (IRD), Campus ISRA-IRD Bel Air, Dakar BP1386, Senegal
Nicolas D. Diouf
Affiliation:
Unité de Formation et de Recherche (UFR) des Sciences Agronomiques, d'Aquaculture et de Technologies Alimentaires (S2ATA), Université Gaston Berger, Saint-Louis BP234, Senegal Institut Supérieur de Formation Agricole et Rurale (ISFAR), Université de Thiès, Bambey BP54, Senegal
Elsa Léger
Affiliation:
Centre for Emerging, Endemic and Exotic Diseases (CEEED), Department of Pathobiology and Population Sciences, The Royal Veterinary College, University of London, Hatfield AL9 7TA, UK
Guilherme G. Verocai
Affiliation:
Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA 30602, USA
Joanne P. Webster
Affiliation:
Centre for Emerging, Endemic and Exotic Diseases (CEEED), Department of Pathobiology and Population Sciences, The Royal Veterinary College, University of London, Hatfield AL9 7TA, UK
*
Author for correspondence: Stefano Catalano, E-mail: scatalano@rvc.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Hydatigera (Cestoda: Taeniidae) is a recently resurrected genus including species seldom investigated in sub-Saharan Africa. We surveyed wild small mammal populations in the areas of Richard Toll and Lake Guiers, Senegal, with the objective to evaluate their potential role as intermediate hosts of larval taeniid stages (i.e. metacestodes). Based on genetic sequences of a segment of the mitochondrial DNA gene cytochrome c oxidase subunit 1 (COI), we identified Hydatigera parva metacestodes in 19 out of 172 (11.0%) Hubert's multimammate mice (Mastomys huberti) and one out of six (16.7%) gerbils (Taterillus sp.) and Hydatigera taeniaeformis sensu stricto metacestodes in one out of 215 (0.5%) Nile rats (Arvicanthis niloticus). This study reports epidemiological and molecular information on H. parva and H. taeniaeformis in West African rodents, further supporting the phylogeographic hypothesis on the African origin of H. parva. Our findings may indicate significant trophic interactions contributing to the local transmission of Hydatigera spp. and other parasites with similar life-cycle mechanisms. We therefore propose that further field investigations of rodent population dynamics and rodent-borne infectious organisms are necessary to improve our understanding of host–parasite associations driving the transmission risks of rodent parasites in West Africa.

Keywords

Arvicanthis niloticusHydatigera parvaHydatigera taeniaeformisMastomys hubertiparasitesTaeniidaeTaterillusWest Africawildlife
Type
Research Article
Information
Parasitology , Volume 146 , Issue 3 , March 2019 , pp. 299 - 304
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alvarez, F, Iglesias, R, Bos, J, Tojo, J and Sanmartin, ML (1990) New findings on the helminth fauna of the common European genet (Genetta genetta L.): first record of Toxocara genettae Warren, 1972 (Ascarididae) in Europe. Annales de Parasitologie Humaine et Comparée 65, 244–248.Google Scholar
Baer, JG (1924) Contribution à la faune helminthologique Sud-Africaine. Annales de Parasitologie Humaine et Comparée 2, 239–247.Google Scholar
Baer, JG and Fain, A (1965) Cestodes. In de Witte Mission, G. F. (ed.), (1933–1935). Exploration du Parc National Albert. Brussels, Belgium: Institute des Parcs Nationaux du Congo Belge, pp. 3–8.Google Scholar
Bernard, J (1963) Cysticerques polycéphales chez le mulot. Archives de l'Institut Pasteur de Tunis 40, 269–277.Google Scholar
Bordes, F, Blasdell, K and Morand, S (2015) Transmission ecology of rodent-borne diseases: new frontiers. Integrative Zoology 10, 424–435.Google Scholar
Bowles, J, Blair, D and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.Google Scholar
Brouat, C and Duplantier, JM (2007) Host habitat patchiness and the distance decay of similarity among gastro-intestinal nematode communities in two species of Mastomys (southeastern Senegal). Oecologia 152, 715–720.Google Scholar
Brouat, C, Kane, M, Diouf, M, Bâ, K, Sall-Dramé, R and Duplantier, JM (2007) Host ecology and variation in helminth community structure in Mastomys rodents from Senegal. Parasitology 134, 437–450.Google Scholar
Burlet, P, Deplazes, P and Hegglin, D (2011) Age, season and spatio-temporal factors affecting the prevalence of Echinococcus multilocularis and Taenia taeniaeformis in Arvicola terrestris. Parasites & Vectors 4, 6.Google Scholar
Catalano, S, Sène, M, Diouf, ND, Fall, CB, Borlase, A, Léger, E, Bâ, K and Webster, JP (2018) Rodents as natural hosts of zoonotic Schistosoma species and hybrids: an epidemiological and evolutionary perspective from West Africa. The Journal of Infectious Diseases 218, 429–433.Google Scholar
Deter, J, Berthier, K, Chaval, Y, Cosson, JF, Morand, S and Charbonnel, N (2006) Influence of geographical scale on the detection of density dependence in the host-parasite system, Arvicola terrestris and Taenia taeniaeformis. Parasitology 132, 595–605.Google Scholar
Diagne, C, Ribas, A, Charbonnel, N, Dalecky, A, Tatard, C, Gauthier, P, Haukisalmi, V, Fossati-Gaschignard, O, Bâ, K, Kane, M, Niang, Y, Diallo, M, Sow, A, Piry, S, Sembène, M and Brouat, C (2016) Parasites and invasions: changes in gastrointestinal helminth assemblages in invasive and native rodents in Senegal. International Journal for Parasitology 46, 857–869.Google Scholar
Elowni, EE and Abu Samra, MT (1988) Observations on a polycephalic cestode larva from a Nile rat (Arvicanthis niloticus). Folia Parasitologica 35, 75–76.Google Scholar
Fagir, DM and El-Rayah, EA (2009) Parasites of the Nile rat in rural and urban regions of Sudan. Integrative Zoology 4, 179–187.Google Scholar
Fichet-Calvet, E, Giraudoux, P, Quéré, JP, Ashford, RW and Delattre, P (2003) Is the prevalence of Taenia taeniaeformis in Microtus arvalis dependent on population density? Journal of Parasitology 89, 1147–1152.Google Scholar
Galan, M, Pagès, M and Cosson, JF (2012) Next-generation sequencing for rodent barcoding: species identification from fresh, degraded and environmental samples. PLoS ONE 7, e48374.Google Scholar
Garba, M, Dalecky, A, Kadaoure, I, Kane, M, Hima, K, Veran, S, Gagare, S, Gauthier, P, Tatard, C, Rossi, JP and Dobigny, G (2014) Spatial segregation between invasive and native commensal rodents in an urban environment: a case study in Niamey, Niger. PLoS ONE 9, e110666.Google Scholar
Gaubert, P, Del Cerro, I, Centeno-Cuadros, A, Palomares, F, Fournier, P, Fonseca, C, Paillat, JP and Godoy, JA (2015) Tracing historical introductions in the Mediterranean Basin: the success story of the common genet (Genetta genetta) in Europe. Biological Invasions 17, 1897–1913.Google Scholar
George, T, Obiamiwe, BA and Anadu, PA (1990) Cestodes of small rodents of the rainforest zone of mid-western Nigeria. Helminthologia 27, 47–53.Google Scholar
Granjon, L and Duplantier, JM (2009) Les Rongeurs de l'Afrique Sahélo-Soudanienne, IRD Edn. Marseille, France: Publications Scientifiques du Muséum.Google Scholar
Han, BA, Schmidt, JP, Bowden, SE and Drake, JM (2015) Rodent reservoirs of future zoonotic diseases. Proceedings of the National Academy of Sciences 112, 7039–7044.Google Scholar
Han, BA, Kramer, AM and Drake, JM (2016) Global patterns of zoonotic disease in mammals. Trends in Parasitology 32, 565–577.Google Scholar
Herbreteau, V, Jittapalapong, S, Rerkamnuaychoke, W, Chaval, Y, Cosson, JF and Morand, S (2011) Protocols for Field and Laboratory Rodent Studies. Bangkok, Thailand: Kasetsart University Press.Google Scholar
Ivoke, N (2009) Studies on the seasonal variations and prevalence of helminth fauna of the black rat, Rattus rattus (L) (Rodentia: Muridae) from different microhabitats in Nsukka, Nigeria. Animal Research International 6, 1063–1071.Google Scholar
Jia, W, Yan, H, Lou, Z, Ni, X, Dyachenko, V, Li, H and Littlewood, DTJ (2012) Mitochondrial genes and genomes support a cryptic species of tapeworm within Taenia taeniaeformis. Acta Tropica 123, 154–163.Google Scholar
Jones, A and Pybus, MJ (2001) Taeniasis and echinococcosis. In Samuel, WM, Pybus, MJ and Kocan, AA (eds), Parasitic Diseases of Wild Mammals, 2nd Edn. Ames, USA: Iowa State University Press, pp. 150–192.Google Scholar
Julius, RS, Schwan, EV and Chimimba, CT (2018) Helminth composition and prevalence of indigenous and invasive synanthropic murid rodents in urban areas of Gauteng Province, South Africa. Journal of Helminthology 92, 445–454.Google Scholar
Keats Shwab, E, Zhu, XQ, Majumdar, D, Pena, HFJ, Gennari, SM, Dubey, JP and Su, C (2014) Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology 141, 453–461.Google Scholar
Lavikainen, A, Haukisalmi, V, Lehtinen, MJ, Henttonen, H, Oksanen, A and Meri, S (2008) A phylogeny of members of the family Taeniidae based on the mitochondrial cox1 and nad1 gene data. Parasitology 135, 1457–1467.Google Scholar
Lavikainen, A, Iwaki, T, Haukisalmi, V, Konyaev, SV, Casiraghi, M, Dokuchaev, NE, Galimberti, A, Halajian, A, Henttonen, H, Ichikawa-Seki, M, Itagaki, T, Krivopalov, AV, Meri, S, Morand, S, Näreaho, A, Olsson, GE, Ribas, A, Terefe, Y and Nakao, M (2016) Reappraisal of Hydatigera taeniaeformis (Batsch, 1786) (Cestoda: Taeniidae) sensu lato with description of Hydatigera kamiyai n. sp. International Journal for Parasitology 46, 361–374.Google Scholar
Lecompte, E, Fichet-Calvet, E, Daffis, S, Koulémou, K, Sylla, O, Kourouma, F, Doré, A, Soropogui, B, Aniskin, V, Allali, B, Kan, SK, Lalis, A, Koivogui, L, Günther, S, Denys, C and ter Meulen, J (2006) Mastomys natalensis and lassa fever, West Africa. Emerging Infectious Diseases 12, 1971–1974.Google Scholar
Liccioli, S, Kutz, SJ, Ruckstuhl, KE and Massolo, A (2014) Spatial heterogeneity and temporal variations in Echinococcus multilocularis infections in wild hosts in a North American urban setting. International Journal for Parasitology 44, 457–465.Google Scholar
Mahon, J (1954) Tapeworms from the Belgian Congo. Tervuren, Belgium: Annales du Musée Royal du Congo Belge.Google Scholar
McManus, DP (2006) Molecular discrimination of taeniid cestodes. Parasitology International 55, S31–S37.Google Scholar
Meerburg, BG, Singleton, GR and Kijlstra, A (2009) Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35, 221–270.Google Scholar
Mello, ÉM, Furtado, LFV, Rabelo, ÉML and Pinto, HA (2018) DNA barcoding of metacestodes found in the Guerlinguetus ingrami (Rodentia: Sciuridae) reveals the occurrence of Hydatigera taeniaeformis sensu stricto (Cyclophyllidea: Taeniidae) in the Americas. Parasitology International 67, 115–118.Google Scholar
Nadler, SA and Pérez-Ponce de León, G (2011) Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138, 1688–1709.Google Scholar
Nakao, M, Lavikainen, A, Iwaki, T, Haukisalmi, V, Konyaev, S, Oku, Y, Okamoto, M and Ito, A (2013) Molecular phylogeny of the genus Taenia (cestoda: Taeniidae): proposals for the resurrection of Hydatigera Lamarck, 1816 and the creation of a new genus Versteria. International Journal for Parasitology 43, 427–437.Google Scholar
Nelson, GS and Rausch, RL (1963) Echinococcus infections in man and animals in Kenya. Annals of Tropical Medicine & Parasitology 57, 136–149.Google Scholar
Sall-Dramé, R, Brouat, C, Bâ, CT and Duplantier, JM (2010) Variation in cestode assemblages of Mastomys and Arvicanthis species (rodents: Muridae) from Lake Retba in Western Senegal. Journal of Parasitology 96, 675–680.Google Scholar
Southwell, T and Kirshner, A (1937) Description of a polycephalic cestode larva from Mastomys erythroleucus, and its probable identity. Annals of Tropical Medicine & Parasitology 31, 37–42.Google Scholar
Theis, JH and Schwab, RG (1992) Seasonal prevalence of Taenia taeniaeformis: relationship to age, sex, reproduction and abundance of an intermediate host (Peromyscus maniculatus). Journal of Wildlife Diseases 28, 42–50.Google Scholar
Udonsi, JK (1989) Helminth parasites of wild populations of the black rat, Rattus rattus (L.), from urban, rural residential and other ecological areas of Nigeria. Acta Parasitologica Polonica 34, 107–116.Google Scholar
Wanas, MQ, Shehata, KK and Rashed, AA (1993) Larval occurrence of Hydatigera taeniaeformis Batsch (1786) (Cestoda: Taeniidae) in the liver of wild rodents in Egypt. Journal of the Egyptian Society of Parasitology 23, 381–388.Google Scholar
Young, HS, McCauley, DJ, Dirzo, R, Nunn, CL, Campana, MG, Agwanda, B, Otarola-Castillo, ER, Castillo, ER, Pringle, RM, Veblen, KE, Salkeld, DJ, Stewardson, K, Fleischer, R, Lambin, EF, Palmer, TM and Helgen, KM (2017) Interacting effects of land use and climate on rodent-borne pathogens in central Kenya. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160116.Google Scholar
Zhang, G, Chen, J, Yang, Y, Liu, N, Jiang, W, Gu, S, Wang, X and Wang, Z (2014) Utility of DNA barcoding in distinguishing species of the family Taeniidae. Journal of Parasitology 100, 542–546.Google Scholar