Abstract
Parasitism is a dynamic ecological phenomenon that is constantly influenced by the environment and intrinsic factors of the host. We aimed to evaluate the influence of vegetation, environmental temperature, reproductive conditions, sex, and body condition (BC) on the detection of Trypanosoma spp. in the blood of Thrichomys fosteri in the Pantanal region, an enzootic area for trypanosomiasis. Whole blood was collected from the tip of the tail, and nPCR was performed for Trypanosoma spp. detection from the DNA extracted from the resultant blood clot. Statistical analyses were performed using generalized linear models. Our results showed that there is a greater probability of detection of Trypanosoma spp. in the bloodstream of animals with the highest BC values in periods with mild temperatures. Since T. fosteri is an abundant and common prey for carnivores, even in periods with low temperatures and consequent decrease in the reproduction and activities of the blood-sucking arthropod vectors, the maintenance of Trypanosoma spp. in the studied area would be guaranteed via predation (trophic network) of T. fosteri individuals with good BC and patent parasitemia. Furthermore, T. fosteri, which displays Trypanosoma spp. in the bloodstream, would be reproducing adequately because we found no influence between the reproductive condition and the detection of Trypanosoma spp. in T. fosteri. The caviomorph rodent T. fostei is an important species for the maintenance of Trypanosoma spp. in the Pantanal biome.
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Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723. https://doi.org/10.1109/TAC.1974.1100705
Antunes PC, Oliveira-Santos LGR, Tomas WM et al (2016) Disentangling the effects of habitat, food, and intraspecific competition on resource selection by the spiny rat, Thrichomys fosteri. J Mammal 97:1738–1744. https://doi.org/10.1093/jmammal/gyw140
Araújo A, Jansen AM, Bouchet F et al (2003) Parasitism, the Diversity of Life, and Paleoparasitology. Mem Inst Oswaldo Cruz 98:5–11
Barros JHS, Xavier SCC, Bilac D et al (2017) Identification of novel mammalian hosts and Brazilian biome geographic distribution of Trypanosoma cruzi TcIII and TcIV. Acta Trop 172:173–179. https://doi.org/10.1016/j.actatropica.2017.05.003
Bezerra CM, de Góes Cavalcanti LP, de Cássia Moreira de Souza R et al (2014) Domestic, peridomestic and wild hosts in the transmission of Trypanosoma cruzi in the Caatinga area colonised by Triatoma brasiliensis. Mem Inst Oswaldo Cruz 109:887–898. https://doi.org/10.1590/0074-0276140048
Bianchi R de C, Campos RC, Xavier-Filho NL et al (2014) Intraspecific, interspecific, and seasonal differences in the diet of three mid-sized carnivores in a large neotropical wetland. Acta Theriologica 59:13–23. https://doi.org/10.1007/s13364-013-0137-x
Botto-Mahan C, Bacigalupo A, Correa JP et al (2012) Field assessment of Trypanosoma cruzi infection and host survival in the native rodent Octodon degus. Acta Trop 122:164–167. https://doi.org/10.1016/j.actatropica.2011.12.003
Brandão EMV, Xavier SCC, Carvalhaes JG et al (2019) Trypanosomatids in small mammals of an agroecosystem in central brazil: another piece in the puzzle of parasite transmission in an anthropogenic landscape. Pathogens 8:1–17. https://doi.org/10.3390/pathogens8040190
Breazile JE (1987) Physiologic basis and consequences of distress in animals. J Am Vet Med Assoc 191:1212–1215
Briones MRS, Souto RP, Stolf BS, Zingales B (1999) The evolution of two Trypanosoma cruzi subgroups inferred from rRNA genes can be correlated with the interchange of American mammalian faunas in the Cenozoic and has implications to pathogenicity and host specificity. Mol Biochem Parasitol 104:219–232. https://doi.org/10.1016/S0166-6851(99)00155-3
de Andreazzi CS, Rademaker V, Gentile R et al (2011) Population ecology of small rodents and marsupials in a semi-deciduous tropical forest of the southeast Pantanal, Brazil. Zoologia 28:762–770. https://doi.org/10.1590/S1984-46702011000600009
D’Elía G, Myers P (2005) On Paraguayan Thrichomys (Hystricognathi: Echimyidae): the distinctiveness of Thrichomys fosteri Thomas, 1903. Therya 5:153–166. https://doi.org/10.12933/therya-14-182
Franke CR, Greiner M, Mehlitz D (1994) Monitoring of clinical, parasitological and serological parameters during an experimental infection of capybaras (Hydrochaeris hydrochaeris) with Trypanosoma evansi. Acta Trop 58:171–174
Graham AL, Shuker DM, Pollitt LC et al (2011) Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Funct Ecol 25:5–17. https://doi.org/10.1111/j.1365-2435.2010.01777.x
Haag J, O’hUigin C, Overath P (1998) The molecular phylogeny of trypanosomes: evidence for an early divergence of the Salivaria. Mol Biochem Parasitol 91:37–49. https://doi.org/10.1016/S0166-6851(97)00185-0
Hannibal W, Arguelho WC, Moreira JC, Aoki C (2019) Use of understory for frugivory by Thrichomys fosteri (Rodentia, echimyidae). Oecologia Australis 23:1100–1103. https://doi.org/10.4257/oeco.2019.2304.30
Herrera HM, Dávila AMR, Norek A et al (2004) Enzootiology of Trypanosoma evansi in Pantanal, Brazil. Vet Parasitol 125:263–275. https://doi.org/10.1016/j.vetpar.2004.07.013
Herrera HM, Rademaker V, Abreu UGP et al (2007) Variables that modulate the spatial distribution of Trypanosoma cruzi and Trypanosoma evansi in the Brazilian Pantanal. Acta Trop 102:55–62. https://doi.org/10.1016/j.actatropica.2007.03.001
Herrera HM, Rocha FL, Lisboa CV et al (2011) Food web connections and the transmission cycles of Trypanosoma cruzi and Trypanosoma evansi (Kinetoplastida, Trypanosomatidae) in the Pantanal Region, Brazil. Trans R Soc Trop Med Hyg 105:380–387. https://doi.org/10.1016/j.trstmh.2011.04.008
Hoare CA (1972) The trypanosomes of mammals. a zoological monograph. Blackwell Scientific Publications, Oxford
Jansen A, Roque A (2010) Domestic and wild mammalian reservoir. In: Telleria J, Tibayrene M (eds) American trypanosomiasis chagas disease – one hundred years of research, Elsevier. Elsevier, London, pp 249–276
Jansen AM, Xavier SCC, Roque ALR (2015) The multiple and complex and changeable scenarios of the Trypanosoma cruzi transmission cycle in the sylvatic environment. Acta Trop 151:1–15. https://doi.org/10.1016/j.actatropica.2015.07.018
Jansen AM, Xavier SCDC, Roque ALR (2018) Trypanosoma cruzi transmission in the wild and its most important reservoir hosts in Brazil. Parasit Vectors 11:1–25. https://doi.org/10.1186/s13071-018-3067-2
le Morvan C, Troutaud D, Deschaux P (1998) Differential effects of temperature on specific and nonspecific immune defences in fish. J Exp Biol 201:165–168
Lukeš J, Butenko A, Hashimi H et al (2018) trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. Trends Parasitol 34:466–480. https://doi.org/10.1016/j.pt.2018.03.002
Mazerolle MJ (2020). AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c). R package version 2.3-1
Menezes JFS, Mourão GM, Kotler BP (2018) Understory cover increases patch use in rodent Thrichomys fosteri. Ethol Ecol Evol 30:267–276. https://doi.org/10.1080/03949370.2017.1354921
Nantes WAG, Barreto WTG, Santos FM et al (2019) The influence of parasitism by Trypanosoma cruzi in the hematological parameters of the white ear opossum (Didelphis albiventris) from Campo Grande, Mato Grosso do Sul, Brazil. Int J Parasitol Parasites Wildl 9:16–20. https://doi.org/10.1016/j.ijppaw.2019.03.015
Nantes WAG, Santos FM, de Macedo GC et al (2021) Trypanosomatid species in Didelphis albiventris from urban forest fragments. Parasitol Res 120:223–231. https://doi.org/10.1007/s00436-020-06921-y
Nascimento FF, Lazar A, Menezes AN et al (2013) The role of historical barriers in the diversification processes in open vegetation formations during the miocene/pliocene using an ancient rodent lineage as a model. PLoS ONE 8. https://doi.org/10.1371/journal.pone.0061924
O’Donoghue P (2017) Haemoprotozoa: Making biological sense of molecular phylogenies. Int J Parasitol Parasites Wildl 6:241–256. https://doi.org/10.1016/j.ijppaw.2017.08.007
Porfirio G, Sarmento P, Leal S, Fonseca C (2016) How is the jaguar Panthera onca perceived by local communities along the Paraguai River in the Brazilian Pantanal? Oryx 50:163–168. https://doi.org/10.1017/S0030605314000349
Poulin R (2007) Evolutionary Ecology of Parasites, 2nd edn. Princeton University Press, Princeton
Rademaker V, Herrera HM, Raffel TR et al (2009) What is the role of small rodents in the transmission cycle of Trypanosoma cruzi and Trypanosoma evansi (Kinetoplastida Trypanosomatidae)? A study case in the Brazilian Pantanal. Acta Trop 111:102–107. https://doi.org/10.1016/j.actatropica.2009.02.006
Rodrigues MS, Lima L, Xavier SCDC et al (2019) Uncovering Trypanosoma spp. diversity of wild mammals by the use of DNA from blood clots. Int J Parasitol Parasites Wildl 8:171–181. https://doi.org/10.1016/j.ijppaw.2019.02.004
Roque ALR, D’Andrea PS, De Andrade GB, Jansen AM (2005) Trypanosoma cruzi: Distinct patterns of infection in the sibling caviomorph rodent species Thrichomys apereoides laurentius and Thrichomys pachyurus (Rodentia, Echimyidae). Exp Parasitol 111:37–46. https://doi.org/10.1016/j.exppara.2005.05.003
Roque ALR, Jansen AM (2014) Wild and synanthropic reservoirs of Leishmania species in the Americas. Int J Parasitol Parasites Wildl 3:251–262
Roy BA, Kirchner JW (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51–63. https://doi.org/10.1111/j.0014-3820.2000.tb00007.x
Sano NY, Herrera HM, de Oliveira Porfirio GE, Santos FM (2021) Understory use by terrestrial small mammals in an unflooded forest patch in the Pantanal floodplain. Mammalia 85:164–167. https://doi.org/10.1515/mammalia-2020-0016
Santos FM, Barreto WTG, de Macedo GC et al (2019) The reservoir system for Trypanosoma (Kinetoplastida, Trypanosomatidae) species in large neotropical wetland. Acta Tropica 199. https://doi.org/10.1016/j.actatropica.2019.105098
Santos FM, de Macedo GC, Barreto WTG et al (2018) Outcomes of Trypanosoma cruzi and Trypanosoma evansi infections on health of Southern coati (Nasua nasua), crab-eating fox (Cerdocyon thous), and ocelot (Leopardus pardalis) in the Brazilian Pantanal. PLoS ONE 13. https://doi.org/10.1371/journal.pone.0201357
Schleich CE, Zenuto RR, Cutrera AP (2015) Immune challenge but not dietary restriction affects spatial learning in the wild subterranean rodent Ctenomys talarum. Physiol Behav 139:150–156. https://doi.org/10.1016/j.physbeh.2014.11.023
Sesti-Costa R, Ignacchiti MDC, Chedraoui-Silva S et al (2012) Chronic cold stress in mice induces a regulatory phenotype in macrophages: correlation with increased 11β-hydroxysteroid dehydrogenase expression. Brain Behav Immun 26:50–60. https://doi.org/10.1016/j.bbi.2011.07.234
Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321. https://doi.org/10.1016/0169-5347(96)10039-2
Silva ES, Gontijo CMF, Melo MN (2005) Contribution of molecular techniques to the epidemiology of neotropical Leishmania species. Trends Parasitol 21:550–552. https://doi.org/10.1016/j.pt.2005.09.008
Simpson AGB, Stevens JR, Lukeš J (2006) The evolution and diversity of kinetoplastid flagellates. Trends Parasitol 22:168–174. https://doi.org/10.1016/j.pt.2006.02.006
Smith A, Clark P, Averis S et al (2008) Trypanosomes in a declining species of threatened Australian marsupial, the brush-tailed bettong Bettongia penicillata (Marsupialia: Potoroidae). Parasitology 135:1329–1335. https://doi.org/10.1017/S0031182008004824
Stevens J, Gibson W (1999) The evolution of salivarian trypanosomes. Mem Inst Oswaldo Cruz 94:225–228. https://doi.org/10.1590/S0074-02761999000200019
Team R Development Core (2018) A language and environment for statistical computing. R Foundation for Statistical Computing 2:https://www.R-project.org
Wright RK, Cooper EL (1981) Temperature effects on ectotherm immune responses. Dev Comp Immunol 5:117–122. https://doi.org/10.1016/0145-305X(81)90016-1
Xavier SCC, Vaz VC, D’Andrea PS et al (2007) Mapping of the distribution of Trypanosoma cruzi infection among small wild mammals in a conservation unit and its surroundings (Northeast-Brazil). Parasitol Int 56:119–128. https://doi.org/10.1016/j.parint.2007.01.003
Yang Y-G, Shang G-Z, Wu X-Q et al (2021) Effects of parasites and predators on nociception: decreases analgesia reduces overwinter survival in root voles (Rodentia: Cricetidae). Zoologia 38:1–9. https://doi.org/10.3897/zoologia.38.e67845
Funding
First author thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the fellowship (88887.369261/2019–00). HMH is fellowship researchers from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (308768/2017–5 and 302420/2017–7). NYSM, WAGN and SCL are in receipt of a fellowship from CAPES (88887.194498/2018–00, 88887.149231/2017–00, 71/700.169/2020, respectively). This study was funded by Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul —FUNDECT (grant PRONEX 006/2015), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior — CAPES (Finance Code 001), and Conselho Nacional de Desenvolvimento Científico e Tecnológico — CNPq (406547/2018–1).
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Conceptualization: FMS, NYS, MAG, and HMH; data curation: FMS and NYS; formal analysis: FMS and NYS; funding acquisition: CEO, MAG, AMJ, and HMH; investigation: FMS, NYS, SCL, WAGN, IPMS, GSS, ALAM, CEO, MAG, AMJ, and HMH; methodology: FMS, NYS, CEO, MAG, AMJ, and HMH; project administration: FMS; supervision: FMS; validation: FMS, NYS, CEO, MAG, AMJ, and HMH; visualization: FMS, NYS, CEO, MAG, AMJ, and HMH; writing – original draft: FMS and NYS; writing – review & editing: FMS, NYS, SCL, WAGN, IPMS, GSS, ALAM, CEO, MAG, AMJ, and HMH.
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All field procedures and laboratory studies were conducted under a license granted by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio license number 70946–3). The present study was approved by the Ethics Committee for Animal Use of Universidade Católica Dom Bosco, Campo Grande, MS (CEUA UCDB license number 013/2020).
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Santos, F.M., Sano, N.Y., Liberal, S.C. et al. The influence of abiotic and biotic variables on the patent parasitemias of Trypanosoma spp. in Thrichomys fosteri (Rodentia: Echimyidae) in the southern Pantanal. Parasitol Res 121, 1719–1724 (2022). https://doi.org/10.1007/s00436-022-07522-7
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DOI: https://doi.org/10.1007/s00436-022-07522-7