Uganda's diverse small mammalian fauna thrives due to its rich habitat diversity, which hosts a wide range of blood parasites, including trypanosomes, particularly the subgenus Herpetosoma typical for rodent hosts. We screened a total of 711 small mammals from various habitats for trypanosomes, with 253 microscopically examined blood smears and 458 tissue samples tested by nested PCR of the 18S rRNA gene. Of 51 rodent and 12 shrew species tested, microscopic screening reaches 7% overall prevalence (with four rodent species positive out of 15 and none of the shrew species out of four), while nested PCR indicated a prevalence of 13% (17 rodent and five shrew species positive out of 49 and 10, respectively). We identified 27 genotypes representing 11 trypanosome species, of which the majority (24 genotypes/9 species) belong to the Herpetosoma subgenus. Among these, we detected 15 new genotypes and two putative new species, labeled AF24 (found in Lophuromys woosnami) and AF25 (in Graphiurus murinus). Our finding of three new genotypes of the previously detected species AF01 belonging to the subgenus Ornithotrypanum in two Grammomys species and Oenomys hypoxanthus clearly indicates the consistent occurrence of this avian trypanosome in African small mammals. Additionally, in Aethomys hindei, we detected the putative new species of the subgenus Aneza. Within the T. lewisi subclade, we detected eleven genotypes, including six new; however, only the genotype AF05b from Mus and Rattus represents the invasive T. lewisi. Our study has improved our understanding of trypanosome diversity in African small mammals. The detection of T. lewisi in native small mammals expands the range of host species and highlighting the need for a broader approach to the epidemiology of T. lewisi.

Africa Centre of Excellence for Innovative Rodent Pest Management and Biosensor Technology Development (ACE IRPM and BTD Institute of Pest Management Centre Sokoine University of Agriculture Morogoro Tanzania

Department of Microbiology and Immunology Busitema University Mbale Uganda

Department of Parasitology Faculty of Science Charles University Prague Czech Republic

Department of Wildlife Management Sokoine University of Agriculture Morogoro Tanzania

Department of Zoology Entomology and Fisheries Science Makerere University Kampala Uganda

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic

Institute of Vertebrate Biology of the Czech Academy of Sciences Květná 8 603 65 Brno Czech Republic

Zobrazit více v PubMed

Adams ER, Hamilton PB, Gibson WC. African trypanosomes: celebrating diversity. Trends Parasitol. 2010;26:324–328. doi: 10.1016/j.pt.2010.03.003. PubMed DOI

Alsarraf M, Bednarska M, Mohallal EM, Mierzejewska EJ, Behnke-Borowczyk J, Zalat S, Gilbert F, Welc-Falęciak R, Kloch A, Behnke JM, Bajer A (2016) Long-term spatiotemporal stability and dynamic changes in the haemoparasite community of spiny mice (Acomys dimidiatus) in four montane wadis in the St. Katherine Protectorate, Sinai Egypt. Parasit Vectors 9:195. 10.1007/s00248-014-0390-9 PubMed PMC

Baláž I, Ševčík M, Tulis F, Zigová M, Dudich A. Diversity, distribution and changes in communities of fleas on small mammals along the elevational gradient from the Pannonian Plain to the Carpathian Mountains. Parasitology. 2020;148:63–73. doi: 10.1017/S0031182020002024. PubMed DOI PMC

Bryja J, Mikula O, Šumbera R, Meheretu Y, Aghova T, Lavrenchenko L, Mazoch V, Oguge N, Mbau SJ, Welegerima K, Amundala N, Colyn M, Leirs H, Verheyen E. Pan-African phylogeny of Mus (subgenus Nannomys) reveals one of the most successful mammal radiations in Africa. BMC Evol Biol. 2014;14:256. doi: 10.1186/s12862-014-0256-2. PubMed DOI PMC

Chao A, Chiu CH (2016) Species richness: estimation and comparison. Wiley StatsRef: Statistics Reference Online. 10.1002/9781118445112.stat03432.pub2

Dahesh SM, Mikhail MW. Surveillance of Trypanosoma spp. of rodents and studies in their transmission probability by fleas in some rural Egyptian areas. J Egypt Soc Parasitol. 2016;46:157–166. doi: 10.12816/0026161. PubMed DOI

Dobigny G, Poirier P, Hima K, Cabaret O, Gauthier P, Tatard C, Costa JM, Bretagne S. Molecular survey of rodent-borne Trypanosoma in Niger with special emphasis on T. lewisi imported by invasive black rats. Acta Trop. 2011;117:183–188. doi: 10.1016/j.actatropica. PubMed DOI

Dybing NA, Jacobson C, Irwin P, Algar D, Adams PJ. Ghosts of Christmas past?: Absence of trypanosomes in feral cats and black rats from Christmas Island and Western Australia. Parasitol Open. 2016;2:E4. doi: 10.1017/pao.2016.1. DOI

Egan SL, Taylor CL, Austen JM, Banks PB, Ahlstrom LA, Ryan UM, Irwin PJ, Oskam CL. Molecular identification of the Trypanosoma (Herpetosoma) T. lewisi clade in black rats (Rattus rattus) from Australia. Parasitol Res. 2020;119:1691–1696. doi: 10.1007/s00436-020-06653-z. PubMed DOI

Fox I, Thillet CJ. Incidence of Trypanosoma lewisi in Puerto Rican bats. J Parasit. 1962;48:123. doi: 10.2307/3275425. PubMed DOI

Gibson W (2017) Kinetoplastea. In: Archibald J, Simpson A, Slamovits C (eds) Handbook of the Protists. Springer, Cham, pp 1089–1138. 10.1007/978-3-319-28149-0_7

Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI

Hamilton PB, Stevens JR. Classification and phylogeny of Trypanosoma cruzi. In: Telleria J, Tibayrenc M, editors. American Trypanosomiasis Chagas Disease: One Hundred Years of Research. Amsterdam: Elsevier; 2017. pp. 321–344.

Hamilton PB, Gibson WC, Stevens JR. Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Mol Phylogenet Evolut. 2007;44:15–25. doi: 10.1016/j.ympev.2007.03.023. PubMed DOI

Hamilton PB, Adams ER, Njiokou F, Gibson WC, Cuny G, Herder S. Phylogenetic analysis reveals the presence of the Trypanosoma cruzi clade in African terrestrial mammals. Infect Genet Evol. 2009;9:81–86. doi: 10.1016/j.meegid.2008.10.011. PubMed DOI

Hoare CA. The trypanosomes of mammals. A zoological monograph: Blackwell Scientific Publications, Oxford; 1972.

Hortal J, Borges PAV, Gaspar C. Evaluating the performance of species richness estimators: sensitivity to sample grain size. J Anim Ecol. 2006;75:274–287. doi: 10.1111/j.1365-2656.2006.01048.x. PubMed DOI

Jenkins PD, Clive DPL, BM, Descriptions of new species of Crocidura (Soricomorpha: Soricidae) from mainland Southeast Asia, with synopses of previously described species and remarks on biogeography. Bull Am Mus Nat Hist. 2009;331:356–405. doi: 10.1206/582-10.1. DOI

Kasozi KI, Zirintunda G, Ssempijja F, Buyinza B, Alzahrani KJ, Matama K, Nakimbugwe HN, Alkazmi L, Onanyang D, Bogere P, Ochieng JJ, Islam S, Matovu W, Nalumenya DP, Batiha GE, Osuwat LO, Abdelhamid M, Shen T, Omadang L, Welburn SC. Epidemiology of trypanosomiasis in wildlife-implications for humans at the wildlife interface in Africa. Front Vet Sci. 2021;8:621699. doi: 10.3389/fvets.2021.621699. PubMed DOI PMC

Katakweba AAS (2020) The prevalence of haemoparasites in rodents and shrews trapped from domestic and peridomestic houses in Morogoro municipality, Tanzania. A hidden public health threat. Tanzan Vet J p 36

Kaufer A, Ellis J, Stark D, Barratt J. The evolution of trypanosomatid taxonomy. Parasit Vectors. 2017;10:287. doi: 10.1186/s13071-017-2204-7. PubMed DOI PMC

Kiffner C, Stanko M, Morand S, Khokhlova IS, Shenbrot GI, Laudisoit A, Leirs H, Hawlena H, Krasnov BR. Sex-biased parasitism is not universal: evidence from rodent-flea associations from three biomes. Oecologia. 2013;173:1009–1022. doi: 10.1007/s00442-013-2664-1. PubMed DOI

Kostygov AY, Karnkowska A, Votýpka J, Tashyreva D, Maciszewski K, Yurchenko V, Lukeš J. Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses. Open Biol. 2021;11:200407. doi: 10.1098/rsob.200407. PubMed DOI PMC

Lainson R, Brígido MC, Silveira FT. Blood and intestinal parasites of squirrels (Rodentia: Sciuridae) in Amazonian Brazil. Mem Inst Oswaldo Cruz. 2004;99:577–579. doi: 10.1590/S0074-02762004000600008. PubMed DOI

Lun ZR, Wen YZ, Uzureau P, Lecordier L, Lai DH, Lan YG, Desquesnes M, Geng GQ, Yang TB, Zhou WL, Jannin JG, Simarro PP, Truc P, Vincendeau P, Pays E. Resistance to normal human serum reveals Trypanosoma lewisi as an underestimated human pathogen. Mol Biochem Parasitol. 2015;199:58–61. doi: 10.1016/j.molbiopara.2015.03.007. PubMed DOI

Mafie E, Saito-Ito A, Kasai M, Hatta M, Rivera PT, Ma XH, Chen ER, Sato H, Takada N. Integrative taxonomic approach of trypanosomes in the blood of rodents and soricids in Asian countries, with the description of three new species. Parasitol Res. 2019;118:97–109. doi: 10.1007/s00436-018-6120-3. PubMed DOI

Maia da Silva F, Marcili A, Ortiz PA, Epiphanio S, Campaner M, CataoDias JL, Shaw JJ, Camargo EP, Teixeira MM. Phylogenetic, morphological and behavioural analyses support host switching of Trypanosoma (Herpetosoma) lewisi from domestic rats to primates. Infect Genet Evol. 2010;10:522–529. doi: 10.1016/j.meegid.2010.02.005. PubMed DOI

Mawanda P, Rwego I, Kisakye JJ, Sheil D. Rodents as potential hosts and reservoirs of parasites along the edge of a Central African forest: Bwindi impenetrable national park, South Western Uganda. Afr Health Sci. 2020;20:1168–1178. doi: 10.4314/ahs.v20i3.20. PubMed DOI PMC

Mayaux P, Pekel JF, Desclée B, Donnay F, Lupi A, Achard F, Clerici M. State and evolution of the African rainforests between 1990 and 2010. Philos Trans R Soc Lond, b, Biol Sci. 2013;368:20120300. doi: 10.1098/rstb.2012.0300. PubMed DOI PMC

Meerburg BG, Singleton GR, Kijlstra A. Rodent-borne diseases and their risks for public health. Crit Rev Microbio. 2009;35:221–270. doi: 10.1080/10408410902989837. PubMed DOI

Meliyo JL, Kimaro DN, Msanya BM, Mulungu LS, Hieronimo P, Kihupi NI, Gulinck H, Deckers JA. Predicting small mammal and flea abundance using landform and soil properties in a plague endemic area in Lushoto District, Tanzania. Tanzan J Health Res. 2014;16:161–172. doi: 10.4314/thrb.v16i3.3. PubMed DOI

Mello DA. Trypanosoma (Megatrypanum) amileari n. sp., isolated from Oryzomys eliurus (Wagner 1845) (Rodentia-Cricetidae) Ann Parasitol Hum Comp. 1979;54:489–494. doi: 10.1051/parasite/1979545489. PubMed DOI

Monique LW, Anang SA, Emily JR, Heru H, Rizaldi TJP, Karen MCR, Susan LP, Kevin CR. Native and introduced trypanosome parasites in endemic and introduced murine rodents of Sulawesi. J Parasitol. 2020;106:523–536. doi: 10.1645/19-136. PubMed DOI

Noyes HA, Ambrose P, Barker F, Begon M, Bennet M, Bown KJ, Kemp SJ. Host specificity of Trypanosoma (Herpetosoma) species: evidence that bank voles (Clethrionomys glareolus) carry only one T. (H.) evotomys 18S rRNA genotype but wood mice (Apodemus sylvaticus) carry at least two polyphyletic parasites. Parasitology. 2002;124:185–190. doi: 10.1017/s0031182001001019. PubMed DOI

Ortiz PA, Garcia HA, Lima L, da Silva FM, Campaner M, Pereira CL, Jittapalapong S, Neves L, Desquesnes M, Camargo EP, Teixeira MMG. Diagnosis and genetic analysis of the worldwide distributed Rattus-borne Trypanosoma (Herpetosoma) lewisi and its allied species in blood and fleas of rodents. Infect Genet Evol. 2018;63:380–390. doi: 10.1016/j.meegid.2017.09.001. PubMed DOI

Pinto CM, Ocana-Mayorga S, Lascano MS, Grijalva MJ. Infection by trypanosomes in marsupials and rodents associated with human dwellings in Ecuador. J Parasitol. 2006;92:1251–1255. doi: 10.1645/GE-886R.1. PubMed DOI

Plumptre AJ, Ayebare S, Behangana M, Forrest TG, Hatanga P, Kabuye C, Kirunda B, Kityo R, Mugabe H, Namaganda M, Nampindo S, Nangendo G, Nkuutu ND, Pomeroy D, Tushabe H, Prinsloo S. Conservation of vertebrates and plants in Uganda: identifying key biodiversity areas and other sites of national importance. Conserv Sci Pract. 2019;1:e7. doi: 10.1111/csp2.7. DOI

Pumhom P, Pognon D, Yangtara S, Thaprathorn N, Milocco C, Douangboupha B, Herder S, Chaval Y, Morand S, Jittapalapong S, Desquesnes M. Molecular prevalence of Trypanosoma spp. in wild rodents of Southeast Asia: influence of human settlement habitat. Epidemiol Infect. 2014;142:1221–1230. doi: 10.1017/S0950268813002161. PubMed DOI PMC

Pumhom P, Morand S, Tran A, Jittapalapong S, Desquesnes M. Trypanosoma from rodents as potential source of infection in human-shaped landscapes of South-East Asia. Vet Parasit. 2015;208:174–180. doi: 10.1016/j.vetpar.2014.12.027. PubMed DOI

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

Salzer JS, Pinto CM, Grippi DC, Williams-Newkirk AJ, Peterhans JK, Rwego IB, Carroll DS, Gillespie TR. Impact of anthropogenic disturbance on native and invasive trypanosomes of rodents in forested Uganda. EcoHealth. 2016;13:698–707. doi: 10.1007/s10393-016-1160-6. PubMed DOI

Sato H, Al-Adhami BH, Une Y, Kamiya H. Trypanosoma (Herpetosoma) kuseli sp. n. (Protozoa: Kinetoplastida) in Siberian flying squirrels (Pteromys volans) Parasitol Res. 2007;101:453–461. doi: 10.1007/s00436-007-0504-0. PubMed DOI

Schwan TG, Lopez JE, Safronetz D, Anderson JM, Fischer RJ, Maïga O, Sogoba N. Fleas and trypanosomes of peridomestic small mammals in sub-Saharan Mali. Parasit Vectors. 2016;9:541. doi: 10.1186/s13071-016-1818-5. PubMed DOI PMC

Seward EA, Voty’pka J, Kment P, Lukeš J, Kelly S. Description of Phytomonas oxycareni n. sp. From the salivary glands of Oxycarenus lavaterae. Protist. 2017;168:71–79. doi: 10.1016/j.protis.2016.11.002. PubMed DOI

Simo G, Njitchouang GR, Njiokou F, Cuny G, Asonganyi T. Trypanosoma brucei s.l.: Microsatellite markers revealed high level of multiple genotypes in the mid-guts of wild tsetse flies of the Fontem sleeping sickness focus of Cameroon. Exp Parasitol. 2011;128:272–278. doi: 10.1016/j.exppara.2011.02.023. PubMed DOI

Svobodová M, Dolnik OV, Čepička I, Rádrová J. Biting midges (Ceratopogonidae) as vectors of avian trypanosomes. Parasit Vectors. 2017;10:224. doi: 10.1186/s13071-017-2158-9. PubMed DOI PMC

Tatard C, Garba M, Gauthier P, Hima K, Artige E, Dossou DKHJ, Gagaré S, Genson G, Truc P, Dobigny G. Rodent-borne Trypanosoma from cities and villages of Niger and Nigeria: a special role for the invasive genus Rattus? Acta Trop. 2017;171:151–158. doi: 10.1016/j.actatropica.2017.03.027. PubMed DOI

Truc P, Büscher P, Cuny G, Gonzatti MI, Jannin J, Joshi P, Juyal P, Lun ZR, Mattioli R, Pays E, Simarro PP, Teixeira MMG, Touratier L, Vincendeau P, Desquesnes M. Atypical human infections by animal trypanosomes. Plos Negl Trop Dis. 2013;7:e2256. doi: 10.1371/journal.pntd.0002256. PubMed DOI PMC

Valkiūnas G, Iezhova TA, Carlson JS, Sehgal RN. Two new Trypanosoma species from African birds, with notes on the taxonomy of avian trypanosomes. J Parasitol. 2011;97:924–930. doi: 10.1645/GE-2796.1. PubMed DOI

Votýpka J, Stříbrná E, Modrý D, Bryja J, Bryjová A, Lukeš J. Unexpectedly high diversity of trypanosomes in small sub-Saharan mammals. Int J Parasitol. 2022;52:647–658. doi: 10.1016/j.ijpara.2022.06.002. PubMed DOI

Wanyonyi MG, Ngeiywa M, Chemwolo LK, Ng’wena GM. Roles of rodent species, age, and sex in determining the prevalence and intensity of Trypanosoma and Plasmodium parasites in rodents of Kakamega Forest area in Western Kenya. Afr J Health Sci. 2013;25:2.

Wyatt KB, Campos PF, Gilbert MTP, Kolokotronis SO, Hynes WH, DeSalle R, Daszak P, MacPhee RDE, Greenwood AD. Historical mammal extinction on Christmas Island (Indian Ocean) correlates with introduced infectious disease. Plos One. 2008;4(10):1371. doi: 10.1371/journal.pone.0003602. PubMed DOI PMC