Blood Parasites and Health Status of Hibernating and Non-Hibernating Noctule Bats (Nyctalus noctula)
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
21-12719S
Czech Science Foundation
PubMed
35630470
PubMed Central
PMC9143927
DOI
10.3390/microorganisms10051028
PII: microorganisms10051028
Knihovny.cz E-zdroje
- Klíčová slova
- Babesia vesperuginis, Chiroptera, Schizotrypanum, Trypanosoma dionisii, Trypanosoma vespertilionis, acid–base balance, blood chemistry, haematology,
- Publikační typ
- časopisecké články MeSH
Co-existence of bats with a wide range of infectious agents relates to their co-evolutionary history and specific physiology. Here, we examined blood samples collected during hibernation and the post-hibernation period to assess the influence of trypanosomes and babesias on the health status of 50 Noctule bats (Nyctalus noctula) using nested PCR. The impact of blood parasites on health was assessed by analysis of haematology and blood chemistry parameters in 21 bats. Prevalence of trypanosomes (Trypanosoma dionisii and T. vespertilionis) and babesia (Babesia vesperuginis) was 44% and 8%, respectively. Analysis of blood parameters indicated impact of babesia on acid-base balance. Blood chemistry parameters showed a significant decrease in total dissolved carbon dioxide and bicarbonate, increased anion gap, and no change in blood pH, suggesting compensated metabolic acidosis. Adverse effects of babesia were only apparent in hibernating bats. Our results suggest differences in the pathogenicity of trypanosomes and babesia in bats. While trypanosomes in general had no significant impact on the health status, we observed alterations in the blood acid-base balance in Babesia-infected bats during hibernation. Despite being infected, Babesia-positive bats survived hibernation without showing any clinical signs.
Bat Rehabilitation Center of Feldman Ecopark Lisne 62340 Kharkiv Ukraine
Department of Botany and Zoology Masaryk University 61137 Brno Czech Republic
Department of Parasitology Faculty of Science Charles University 12800 Prague Czech Republic
Institute of Vertebrate Biology Academy of Sciences of the Czech Republic 60365 Brno Czech Republic
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Calisher C.H., Childs J.E., Field H.E., Holmes K.V., Schountz T. Bats: Important reservoir hosts of emerging viruses. Clin. Microbiol. Rev. 2006;19:531–545. doi: 10.1128/CMR.00017-06. PubMed DOI PMC
Kosoy M., Bai Y., Lynch T., Kuzmin I.V., Niezgoda M., Franka R., Agwanda B., Breiman R.F., Rupprecht C.E. Bartonella spp. in Bats, Kenya. Emerg. Infect. Dis. 2010;16:1875–1881. doi: 10.3201/eid1612.100601. PubMed DOI PMC
Evans N.J., Brown K., Timofte D., Simpson V.R., Birtles R.J. Fatal Borreliosis in Bat Caused by Relapsing Fever Spirochete, United Kingdom. Emerg. Infect. Dis. 2009;15:1331–1333. doi: 10.3201/eid1508.090475. PubMed DOI PMC
García-Fraile P., Chudíčková M., Benada O., Pikula J., Kolařík M. Serratia myotis sp. nov. and Serratia vespertilionis sp. nov. isolated from bats hibernating in caves in the Czech Republic. Int. J. Syst. Evol. Microbiol. 2015;65:90–94. doi: 10.1099/ijs.0.066407-0. PubMed DOI
Blehert D.S., Maluping R.P., Green D.E., Berlowski-Zier B.M., Ballman A.E., Langenberg J.A. Acute pasteurellosis in wild big brown bats (Eptesicus fuscus) J. Wildl. Dis. 2014;50:136–139. doi: 10.7589/2012-02-063. PubMed DOI
Mühldorfer K. Bats and Bacterial Pathogens: A Review. Zoonoses Public Health. 2013;60:93–103. doi: 10.1111/j.1863-2378.2012.01536.x. PubMed DOI
Sebghati T.S., Engle J.T., Goldman W.E. Intracellular parasitism by Histoplasma capsulatum: Fungal virulence and calcium dependence. Science. 2000;290:1368–1372. doi: 10.1126/science.290.5495.1368. PubMed DOI
Gardner R.A., Molyneux D.H. Schizotrypanum in British bats. Parasitology. 1988;97:43–50. doi: 10.1017/S0031182000066725. PubMed DOI
Steindel M., Grisard E.C., de Carvalho Pinto C.J., Cordeiro F.D., Ribeiro-Rodriques R., Romanha A.J. Characterization of trypanosomes from the subgenus Schizotrypanum isolated from bats, Eptesicus sp. (Chiroptera: Vespertilionidae), captured in Florianópolis, Santa Catarina State, Brazil. J. Parasitol. 1998;84:601–607. doi: 10.2307/3284730. PubMed DOI
Lisboa C.V., Pinho A.P., Herrera H.M., Gerhardt M., Cupolillo E., Jansen A.M. Trypanosoma cruzi (Kinetoplastida, Trypanosomatidae) genotypes in neotropical bats in Brazil. Vet. Parasitol. 2008;156:314–318. doi: 10.1016/j.vetpar.2008.06.004. PubMed DOI
Hamilton P.B., Teixeira M.M.G., Stevens J.R. The evolution of Trypanosoma cruzi: The ‘bat seeding’ hypothesis. Trends Parasitol. 2012;28:136–141. doi: 10.1016/j.pt.2012.01.006. PubMed DOI
Hamilton P.B., Cruickshank C., Stevens J.R., Teixeira M.M.G., Mathews F. Parasites reveal movement of bats between the New and Old Worlds. Mol. Phylogenet. Evol. 2012;63:521–526. doi: 10.1016/j.ympev.2012.01.007. PubMed DOI PMC
Lima L., Espinosa-Álvarez O., Hamilton P.B., Neves L., Takata C.S.A., Campaner M., Attias M., de Souza W., Camargo E.P., Teixeira M.M.G. Trypanosoma livingstonei: A new species from African bats supports the bat seeding hypothesis for the Trypanosoma cruzi clade. Parasites Vectors. 2013;6:221. doi: 10.1186/1756-3305-6-221. PubMed DOI PMC
Cottontail V.M., Kalko E.K., Cottontail I., Wellinghausen N., Tschapka M., Perkins S.L., Pinto C.M. High local diversity of Trypanosoma in a common bat species, and implications for the biogeography and taxonomy of the T. cruzi clade. PLoS ONE. 2014;9:e108603. doi: 10.1371/journal.pone.0108603. PubMed DOI PMC
Hodo C.L., Goodwin C.C., Mayes B.C., Mariscal J.A., Waldrup K.A., Hamer S.A. Trypanosome species, including Trypanosoma cruzi, in sylvatic and peridomestic bats of Texas, USA. Acta Trop. 2016;164:259–266. doi: 10.1016/j.actatropica.2016.09.013. PubMed DOI PMC
Wang L.J., Han H.J., Zhao M., Liu J.W., Luo L.M., Wen H.L., Qin X.R., Zhou C.M., Qi H., Yu H., et al. Trypanosoma dionisii in insectivorous bats from northern China. Acta Trop. 2019;193:124–128. doi: 10.1016/j.actatropica.2019.02.028. PubMed DOI
Concannon R., Wynn-Owen K., Simpson V.R., Birtles R.J. Molecular characterization of haemoparasites infecting bats (Microchiroptera) in Cornwall, UK. Parasitology. 2005;131:489–496. doi: 10.1017/S0031182005008097. PubMed DOI
Gardner R.A., Molyneux D.H. Polychromophilus murinus: A malarial parasite of bats: Life-history and ultrastructural studies. Parasitology. 1988;96:591–605. doi: 10.1017/S0031182000080215. PubMed DOI
Corduneanu A., Hrazdilová K., Sándor A.D., Matei I.A., Ionică A.M., Barti L., Ciocănău M.A., Măntoiu D.S., Coroiu I., Hornok S., et al. Babesia vesperuginis, a neglected piroplasmid: New host and geographical records, and phylogenetic relations. Parasites Vectors. 2017;10:598. doi: 10.1186/s13071-017-2536-3. PubMed DOI PMC
Ranaivoson H.C., Héraud J.M., Goethert H.K., Telford S.R., III, Rabetafika L., Brook C.E. Babesial infection in the Madagascan flying fox, Pteropus rufus É. Geoffroy, 1803. Parasites Vectors. 2019;12:51. doi: 10.1186/s13071-019-3300-7. PubMed DOI PMC
Schaer J., Perkins S.L., Decher J., Leendertz F.H., Fahr J., Weber N., Matuschewski K. High diversity of West African bat malaria parasites and a tight link with rodent Plasmodium taxa. Proc. Natl. Acad. Sci. USA. 2013;110:17415–17419. doi: 10.1073/pnas.1311016110. PubMed DOI PMC
Minozzo G.A., da Silva Mathias B., Riediger I.N., de Oliveira Guimarães L., dos Anjos C.C., Monteiro E.F., dos Santos A.P., Biondo A.W., Kirchgatter K. First Molecular Detection of Polychromophilus Parasites in Brazilian Bat Species. Microorganisms. 2021;9:1240. doi: 10.3390/microorganisms9061240. PubMed DOI PMC
Munshi-South J., Wilkinson G.S. Bats and birds: Exceptional longevity despite high metabolic rates. Ageing Res. Rev. 2010;9:12–19. doi: 10.1016/j.arr.2009.07.006. PubMed DOI
Zhang G., Cowled C., Shi Z., Huang Z., Bishop-Lilly K.A., Fang X., Wynne J.W., Xiong Z., Baker M.L., Zhao W., et al. Comparative Analysis of Bat Genomes Provides Insight into the Evolution of Flight and Immunity. Science. 2013;339:456–460. doi: 10.1126/science.1230835. PubMed DOI PMC
O’Shea T.J., Cryan P., Cunningham A.A., Fooks A.R., Hayman D.T.S., Luis A.D., Peel A.J., Plowright R.K., Wood J.L.N. Bat flight and zoonotic viruses. Emerg. Infect. Dis. 2014;20:741–745. doi: 10.3201/eid2005.130539. PubMed DOI PMC
Flieger M., Bandouchova H., Cerny J., Chudickova M., Kolarik M., Kovacova V., Martinkova N., Novak P., Sebesta O., Stodulkova E., et al. Vitamin B-2 as a virulence factor in Pseudogymnoascus destructans skin infection. Sci. Rep. 2016;6:33200. doi: 10.1038/srep33200. PubMed DOI PMC
Carey H.V., Andrews M.T., Martin S.L. Mammalian hibernation: Cellular and molecular responses to depressed metabolism and low temperature. Physiol. Rev. 2003;83:1153–1181. doi: 10.1152/physrev.00008.2003. PubMed DOI
Storey K.B. Out Cold: Biochemical Regulation of Mammalian Hibernation—A Mini-Review. Gerontology. 2010;56:220–230. doi: 10.1159/000228829. PubMed DOI
Drew K.L., Osborne P.G., Frerichs K.U., Hu Y., Koren R.E., Hallenbeck J.M., Rice M.E. Ascorbate and glutathione regulation in hibernating ground squirrels. Brain Res. 1999;851:1–8. doi: 10.1016/S0006-8993(99)01969-1. PubMed DOI
Morin P., Jr., Ni Z., McMullen D.C., Storey K.B. Expression of Nrf2 and its downstream gene targets in hibernating 13-lined ground squirrels, Spermophilus tridecemlineatus. Mol. Cell. Biochem. 2008;312:121–129. doi: 10.1007/s11010-008-9727-3. PubMed DOI
Bouma H.R., Strijkstra A.M., Boerema A.S., Deelman L.E., Epema A.H., Hut R.A., Kroese F.G., Henning R.H. Blood cell dynamics during hibernation in the European Ground Squirrel. Vet. Immunol. Immunopathol. 2010;136:319–323. doi: 10.1016/j.vetimm.2010.03.016. PubMed DOI
Bouma H.R., Carey H.V., Kroese F.G.M. Hibernation: The immune system at rest? J. Leukoc. Biol. 2010;88:619–624. doi: 10.1189/jlb.0310174. PubMed DOI
Haitlinger R., Lupicki D. Arthropods (Acari, Siphonaptera, Heteroptera, Psocoptera) associated with Nyctalus noctula (Schreber, 1774) (Chiroptera: Vespertilionidae) in Southern Poland. Wiad. Parazytol. 2008;54:124–130. PubMed
Hornok S. Ixodes vespertilionis Koch, 1844 (Figs. 29–31) In: Estrada-Peña A., Mihalcs A.D., Petney T.N., editors. Ticks of Europe and North Africa. 1st ed. Springer; Berlin, Germany: 2017. pp. 97–107.
Lučan R.K., Bandouchova H., Bartonička T., Pikula J., Zahradníková A., Jr., Zukal J., Martínková N. Ectoparasites may serve as vectors for the white-nose syndrome fungus. Parasites Vectors. 2016;9:16. doi: 10.1186/s13071-016-1302-2. PubMed DOI PMC
George D.B., Webb C.T., Farnsworth M.L., O’Shea T.J., Bowen R.A., Smith D.L., Stanley T.R., Ellison L.E., Rupprecht C.E. Host and viral ecology determine bat rabies seasonality and maintenance. Proc. Natl. Acad. Sci. USA. 2011;108:10208–10213. doi: 10.1073/pnas.1010875108. PubMed DOI PMC
Callait M.P., Gauthier D. Parasite adaptation to hibernation in Alpine Marmots (Marmota marmota) In: Heldmaier G., Klingenspor M., editors. Life in the Cold: Eleventh International Hibernation Symposium. 1st ed. Springer; Berlin, Germany: 2000. pp. 139–146.
Coggins J.R., Tedesco J.L., Rupprecht C.E. Seasonal changes and overwintering of parasites in the bat, Myotis lucifugus (Le Conte) in a Wisconsin hibernaculum. Am. Midl. Nat. 1982;107:305–315. doi: 10.2307/2425381. DOI
Ramírez J.D., Tapia-Calle G., Muñoz-Cruz G., Poveda C., Rendón L.M., Hincapié E., Guhl F. Trypanosome species in neo-tropical bats: Biological, evolutionary and epidemiological implications. Infect. Genet. Evol. 2014;22:250–256. doi: 10.1016/j.meegid.2013.06.022. PubMed DOI PMC
Barnabe C., Brisse S., Tibayrenc M. Phylogenetic diversity of bat trypanosomes of subgenus Schizotrypanum based on multilocus enzyme electrophoresis, random amplified polymorphic DNA, and cytochrome b nucleotide sequence analyses. Infect. Genet. Evol. 2003;2:201–208. doi: 10.1016/S1567-1348(02)00130-2. PubMed DOI
Lima L., da Silva F.M., Neves L., Attias M., Takata C.S.A., Campaner M., de Souza W., Hamilton P.B., Teixeira M.M.G. Evolutionary insights from bat trypanosomes: Morphological, developmental and phylogenetic evidence of a new species, Trypanosoma (Schizotrypanum) erneyi sp. nov., in African bats closely related to Trypanosoma (Schizotrypanum) cruzi and allied species. Protist. 2012;163:856–872. doi: 10.1016/j.protis.2011.12.003. PubMed DOI
Gardner R.A., Molyneux D.H., Stebbings R.E. Studies on the prevalence of haematozoa of British bats. Mammal. Rev. 1987;17:75–80. doi: 10.1111/j.1365-2907.1987.tb00051.x. DOI
Gardner R.A., Molyneux D.H. Babesia vesperuginis: Natural and experimental infections in British bats (Microchiroptera) Parasitology. 1987;95:461–469. doi: 10.1017/S0031182000057887. PubMed DOI
Bower S.M., Woo P.T.K. The development of Trypanosoma (Schizotrypanum) hedricki in Cimex brevis (Hemiptera: Cimicidae) Can. J. Zool. 1981;59:546–554. doi: 10.1139/z81-078. DOI
Hornok S., Szőke K., Kováts D., Estók P., Görföl T., Boldogh S.A., Takács N., Kontschán J., Földvári G., Barti L., et al. DNA of Piroplasms of ruminants and dogs in Ixodid bat ticks. PLoS ONE. 2016;11:e0167735. doi: 10.1371/journal.pone.0167735. PubMed DOI PMC
Simpson V.R. Veterinary advances in the investigation of wildlife diseases in Britain. Res. Vet. Sci. 2000;69:11–16. doi: 10.1053/rvsc.2000.0384. PubMed DOI
Oliveira M.P.C., Cortes M., Maeda F.Y., Fernandes M.C., Haapalainen E.F., Yoshida N., Mortara R.A. Unique behavior of Trypanosoma dionisii interacting with mammalian cells: Invasion, intracellular growth, and nuclear localization. Acta Trop. 2009;110:65–74. doi: 10.1016/j.actatropica.2009.01.008. PubMed DOI
Pikula J., Bandouchova H., Kovacova V., Linhart P., Piacek V., Zukal J. Reproduction of Rescued Vespertilionid Bats (Nyctalus noctula) in Captivity: Veterinary and Physiologic Aspects. Vet. Clin. N. Am. Exot. Anim. Pract. 2017;20:665–677. doi: 10.1016/j.cvex.2016.11.013. PubMed DOI
Bandouchova H., Bartonička T., Berkova H., Brichta J., Kokurewicz T., Kovacova V., Linhart P., Piacek V., Pikula J., Zahradníková A., et al. Alterations in the health of hibernating bats under pathogen pressure. Sci. Rep. 2018;8:6067. doi: 10.1038/s41598-018-24461-5. PubMed DOI PMC
Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods. 2012;9:676–682. doi: 10.1038/nmeth.2019. PubMed DOI PMC
Seward E.A., Votýpka 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
Zintl A., Finnerty E.J., Murphy T.M., de Waal T., Gray J.S. Babesias of red deer (Cervus elaphus) in Ireland. Vet. Res. 2011;42:7. doi: 10.1186/1297-9716-42-7. PubMed DOI PMC
Basic Local Alignment Search Tool (BLAST) [(accessed on 23 April 2019)]; Available online: https://blast.ncbi.nlm.nih.gov/Blast.cgi,
Chimelli L., Scaravilli F. Trypanosomiasis. Brain Pathol. 1997;7:599–611. doi: 10.1111/j.1750-3639.1997.tb01077.x. PubMed DOI PMC
Köster L.S., Lobetti R.G., Kelly P. Canine babesiosis: A perspective on clinical complications, biomarkers, and treatment. Vet. Med. 2015;6:119–128. doi: 10.2147/VMRR.S60431. PubMed DOI PMC
Jacobson L.S., Lobetti R. Glucose, lactate, and pyruvate concentrations in dogs with babesiosis. Am. J. Vet. Res. 2005;66:244–250. doi: 10.2460/ajvr.2005.66.244. PubMed DOI
Leisewitz A.L., Jacobson L.S., de Morais H.S.A., Reyers F. The Mixed Acid-Base Disturbances of Severe Canine Babesiosis. J. Vet. Intern. Med. 2001;15:445–452. doi: 10.1111/j.1939-1676.2001.tb01573.x. PubMed DOI
Bartlett S.L., Abou-Madi N., Messick J.B., Birkenheuer A., Kollias G.V. Diagnosis and Treatment of Babesia odocoilei in Captive Reindeer (Rangifer tarandus tarandus) and Recognition of Three Novel Host Species. J. Zoo Wildl. Med. 2009;40:152–159. doi: 10.1638/2008-0011.1. PubMed DOI
Usinger R.L. Monograph of Cimicidae (Hemiptera—Heteroptera) 1st ed. Entomological Society of America; New York, NY, USA: 1966. pp. 10–33.
Manzano-Román R., Díaz-Martín V., de la Fuente J., Pérez-Sánchez R. Soft ticks as pathogen vectors: Distribution, surveillance and control. In: Shah M.M., editor. Parasitology. 1st ed. InTechOpen; London, UK: 2012. pp. 125–162.
Balvín O., Ševčík M., Jahelková H., Bartonička T., Orlova M., Vilímková J. Transport of bugs of the genus Cimex (Heteroptera: Cimicidae) by bats in western Palaearctic. Vespertilio. 2012;16:43–54.
Cardoso M.S., Reis-Cunha J.L., Bartholomeu D.C. Evasion of the Immune Response by Trypanosoma cruzi during Acute Infection. Front. Immunol. 2016;6:659. doi: 10.3389/fimmu.2015.00659. PubMed DOI PMC
Chauvin A., Moreau E., Bonnet S., Plantard O., Malandrin L. Babesia and its hosts: Adaptation to long-lasting interactions as a way to achieve efficient transmission. Vet. Res. 2009;40:37. doi: 10.1051/vetres/2009020. PubMed DOI PMC
Molyneux D.H. Trypanosomes of Bats. In: Kreier J.P., Baker J.R., editors. Parasitic Protozoa. 1st ed. Academic Press; New York, NY, USA: 1991. pp. 195–223.
Ponte-Sucre A. An Overview of Trypanosoma brucei Infections: An Intense Host–Parasite Interaction. Front. Microbiol. 2016;7:2126. doi: 10.3389/fmicb.2016.02126. PubMed DOI PMC
Lozano I.M.D., De Pablos L.M., Longhi S.A., Zago M.P., Schijman A.G., Osuna A. Immune complexes in chronic Chagas disease patients are formed by exovesicles from Trypanosoma cruzi carrying the conserved MASP N-terminal region. Sci. Rep. 2017;7:44451. doi: 10.1038/srep44451. PubMed DOI PMC
Linhart P., Bandouchova H., Zukal J., Votypka J., Kokurewicz T., Dundarova H., Apoznanski G., Heger T., Kubickova A., Nemcova M., et al. Trypanosomes in Eastern and Central European bats. Acta Vet. Brno. 2020;89:69–78. doi: 10.2754/avb202089010069. DOI