Abstract
In nature, parasitic infections must be addressed as complex systems involving parasite-host relationships on a temporal and spatial scale. Since the parasites cover a great biological diversity, we can expect that wildlife are exposed simultaneously to different parasites. In this sense, the objective of this work was to determine the relationships between free-living mammals and their associated hemoparasites in the Brazilian Pantanal. We used the data published during 2017 and 2018 by de Sousa et al. regarding the detection of vector-borne pathogens (VBP), namely Anaplasma, Babesia, Bartonella, Cytauxzoon, Ehrlichia, Hepatozoon, Mycoplasma, and Theileria, in nine species of free-living mammals belonging to orders Carnivora, Rodentia, and Didelphimorphia. We assume as infected an individual positive on any of parasitological, molecular, and/or serological tests. We observed a strong association between the wild felid Leopardus pardalis with Cytauxzoon, the wild canid Cerdocyon thous with Hepatozoon, the small rodent Thrichomys fosteri with Bartonella, and the procyonid Nasua nasua with Mycoplasma and Theileria. Therefore, N. nasua, C. thous, T. fosteri, and the small rodent Oecomys mamorae can be considered key species for the maintenance of selected VBP in the Pantanal region, because they showed a high number of single and coinfections. Together, our results highlighted the importance of coinfection as a common phenomenon in nature.
Similar content being viewed by others
References
Agosta SJ (2006) On ecological fitting, plant-insect associations, herbivore host shifts, and host plant selection. Oikos 114:556–565. https://doi.org/10.1111/j.2006.0030-1299.15025.x
Agosta SJ, Klemens JA (2008) Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecol Lett 11:1123–1134. https://doi.org/10.1111/j.1461-0248.2008.01237.x
Almeida AP, Souza TD, Marcili A, Labruna MB (2013) Novel Ehrlichia and Hepatozoon agents infecting the crab-eating fox (Cerdocyon thous) in southeastern Brazil. J Med Entomol 50:640–646. https://doi.org/10.1603/me12272
Almeida-Neto M, Guimarães P, Guimarães PRJR, Loyola RD, Ulrich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239. https://doi.org/10.1111/j.0030-1299.2008.16644.x
André MR, Adania CH, Machado RZ, Allegretti SM, Felippe PA, Silva KF, Nakaghi AC, Dagnone AS (2009) Molecular detection of Cytauxzoon spp. in asymptomatic Brazilian wild captive felids. J Wildl Dis 45(1):234–237. https://doi.org/10.7589/0090-3558-45.1.234
Andreazzi CSDE, Rademaker V, Gentile R, Herrera HM, Jansen AM, D'andrea PS (2011) Population ecology of small rodents and marsupials in a semi-deciduous tropical forest of the southeast Pantanal, Brazil. Zoologia (Curitiba) 28(6):762–770. https://doi.org/10.1590/S1984-46702011000600009
Averbeck GA, Bjork KE, Packer C, Herbst L (1990) Prevalence of hematozoans in lions (Panthera leo) and cheetah (Acinonyx-jubatus) in Serengeti National Park and Ngorongoro crater, Tanzania. J Wildl Dis 26:392–394. https://doi.org/10.7589/0090-3558-26.3.392
Baneth G, Harrus S, Gal A, Aroch I (2015) Canine vector-borne co-infections: Ehrlichia canis and Hepatozoon canis in the same host monocytes. Vet Parasit 208:30–34. https://doi.org/10.1016/j.vetpar.2014.12.013
Bianchi RC, Campos RC, Xavier-Filho NL, Olifiers N, Gompper ME, Mourão G (2014) Intraspecific, interspecific, and seasonal differences in the diet of three mid-sized carnivores in a large neotropical wetland. Acta Theriol (Warsz) 59(1):13–23. https://doi.org/10.1007/s13364-013-0137-x
Blackwell AD, Martin M, Kaplan H, Gurven M (2013) Antagonism between two intestinal parasites in humans: the importance of co-infection for infection risk and recovery dynamics. Proc R Soc B 280:1671
Blanco YD, Hirsch BT (2006) Determinants of vigilance behavior in the ring tailed coati (Nasua nasua): the importance of within-group spatial position. Behav Ecol Sociobiol 61:173–182. https://doi.org/10.1007/s00265-006-0248-3
Brooks DR (1985) Historical ecology: a new approach to studying the evolution of ecological associations. Ann Missouri Bot Gard 72:660–680. https://doi.org/10.2307/2399219
Campião KM, Ribas A, Tavares LER (2015) Diversity and patterns of interaction of an anuran–parasite network in a neotropical wetland. Parasitology 142:1751–1757. https://doi.org/10.1017/S0031182015001262
Campos JBV, André MR, Gonçalves LR, Freschi CR, Santos FM, De Oliveira CE, Piranda EM, De Andrade GB, Macedo GC, Machado RZ, Herrera HM (2019) Assessment of equine piroplasmids in the Nhecolândia sub-region of Brazilian Pantanal wetland using serological, parasitological, molecular, and hematological approaches. Ticks Tick Borne Dis 10(3):714–721. https://doi.org/10.1016/j.ttbdis.2019.03.002
Cox FEG (2001) Concomitant infections, parasites and immune responses. Parasitology 122:S23–S38. https://doi.org/10.1017/s003118200001698x
Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695. http://igraph.sf.net. Accessed 15 Aug 2020
De Sousa KCM, Fernandes MP, Herrera HM, Benevenute JL, Santos FM, Rocha FL, Barreto WT, Macedo GC, Campos JB, Martins TF, De Andrade Pinto PC, Battesti DB, Piranda EM, Cançado PH, Machado RZ, André MR (2017a) Molecular detection of Hepatozoon spp. in domestic dogs and wild mammals in southern Pantanal, Brazil with implications in the transmission route. Vet Parasitol 237:37–46. https://doi.org/10.1016/j.vetpar.2017.02.023
De Sousa KCM, Herrera HM, Secato CT, Oliveira ADV, Santos FM, Rocha FL, Barreto WTG, Macedo GC, De Andrade Pinto PCE, Machado RZ, Costa MT, André MR (2017b) Occurrence and molecular characterization of hemoplasmas in domestic dogs and wild mammals in a Brazilian wetland. Acta Trop 171:172–181. https://doi.org/10.1016/j.actatropica.2017.03.030
De Sousa KCM, Calchi AC, Herrera HM, Dumler JS, Barros-Battesti DB, Machado RZ, André MR (2017c) Anaplasmataceae agents among wild mammals and ectoparasites in Brazil. Epidemiol Infect 145(16):3424–3437. https://doi.org/10.1017/S095026881700245X
De Sousa KCM, Do Amaral RB, Herrera HM, Santos FM, Macedo GC, De Andrade Pinto PCE, Barros-Battesti DM, Machado RZ, André MR (2018a) Genetic diversity of Bartonella spp. in wild mammals and ectoparasites in Brazilian Pantanal. Microb Ecol 76:544–554. https://doi.org/10.1007/s00248-017-1138-0
De Sousa KCM, Fernandes MP, Herrera HM, Freschi CR, Machado RZ, André MR (2018b) Diversity of piroplasmids among wild and domestic mammals and ectoparasites in Pantanal wetland, Brazil. Ticks Tick Borne Dis 2:245–253. https://doi.org/10.1016/j.ttbdis.2017.09.010
Dean RS, Helps CR, Jones TJG, Tasker S (2008) Use of real-time PCR to detect Mycoplasma haemofelis and ‘Candidatus Mycoplasma haemominutum’ in the saliva and salivary glands of hemoplasma infected cats. J Feline Med Surg 10:413–417. https://doi.org/10.1016/j.jfms.2007.12.007
R Development Core Team (2015) R: a language and environment for statistical computing. http://www.R-project.org. Accessed 27 Sept 2020
Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Homage to Linnaeus: how many parasites? How many hosts? Proc Natl Acad Sci U S A 105(Suppl1):11482–11489. https://doi.org/10.1073/pnas.0803232105
Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. R News 8:8–11
Dyer LA, Singer MS, Lill JT, Stireman JO, Gentry GL, Marquis RJ, Ricklefs RE, Greeney HF, Wagner DL, Morais HC, Diniz IR, Kursar TA, Coley PD (2007) Host specificity of Lepidoptera in tropical and temperate forests. Nature 448:696–699. https://doi.org/10.1038/nature05884
East ML, Wibbelt G, Lieckfeldt D, Ludwig A, Goller K, Wilhelm K, Schares G, Thierer D, Hofer H (2008) A Hepatozoon species genetically distinct from H. canis infecting spotted hyenas in the Serengeti ecosystem, Tanzania. J Wildl Dis 44(1):45–52. https://doi.org/10.7589/0090-3558-44.1.45
Furtado MM, Taniwaki SA, Metzger B, Dos Santos Paduan K, O'dwyer HL, De Almeida Jácomo AT, Porfírio GEO, Silveira L, Sollmann R, Tôrres NM, Ferreira Neto JS (2017) Is the free-ranging jaguar (Panthera onca) a reservoir for Cytauxzoon felis in Brazil? Ticks Tick Borne Dis 8(4):470–476. https://doi.org/10.1016/j.ttbdis.2017.02.005
Gonçalves LR, Favacho AR, Roque AL, Mendes NS, Fidelis Junior OL, Benevenute JL, Herrera HM, D'andrea PS, De Lemos ER, Machado RZ, André MR (2016) Association of Bartonella species with wild and synanthropic rodents in different Brazilian biomes. Appl Environ Microbiol 82(24):7154–7164. https://doi.org/10.1128/AEM.02447-1
Gutiérrez R, Krasnov B, Morick D, Gottlieb Y, Khokhlova IS, Harrus S (2015) Bartonella infection in rodents and their flea Ectoparasites: an overview. Vector Borne Zoonotic Dis 15:27–39. https://doi.org/10.1089/vbz.2014.1606
Hechinger RF, Lafferty K (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proc Biol Sci 271:1059–1066. https://doi.org/10.1098/rspb.2005.3070
Herrera HM, Rademaker V, Abreu UGP, D‘andrea PS, Jansen AM (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, Rademaker V, Mourão GM, Jansen AM (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
Hoberg EP, Brooks DR (2008) A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite systems. J Biogeogr 35:1533–1550. https://doi.org/10.1111/j.1365-2699.2008.01951.x
Hodžić A, Alić A, Duscher GG (2018) High diversity of blood-associated parasites and bacteria in European wild cats in Bosnia and Herzegovina: a molecular study. Ticks Tick Borne Dis. 9(3):589–593. https://doi.org/10.1016/j.ttbdis.2018.01.017
Janzen DH (1985) On ecological fitting. Oikos 45:308–310. https://doi.org/10.2307/3565565
Jermy T (1984) Evolution of insect-host plant relationships. Am Nat 124:609–630. https://doi.org/10.1086/284302
Johnson PTJ, De Roode JC, Fenton A (2015) Why infectious disease research needs community ecology. Science. 349:1259504. https://doi.org/10.1126/science.1259504
Kelley ST, Farrel DB (1998) Is specialization a dead end? The phylogeny of host use in Dendroctonus bark beetles (Scolytidae). Evolution 52:1731–1743. https://doi.org/10.1111/j.1558-5646.1998.tb02253.x
Kelly DW, Patterson RA, Towsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056. https://doi.org/10.1890/08-1085.1
Leps J, Smilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511615146
Levine ND (1968) Nematode parasites of domestic animals and of man. Burguess Publishing Company, Minneapolis, 477 p
Lindenfors P, Nunn CLK, Jones E, Cunningham AA, Sechrest W, Gittleman JL (2007) Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density. Glob Ecol Biogeogr 1:1–14. https://doi.org/10.1111/j.1466-8238.2006.00301.x
Marquitti FMD, Guimarães PR, Pires MM, Bittencourt LF (2014) MODULAR: software for the autonomous computation of modularity in large network sets. Ecography 37:221–224. https://doi.org/10.1111/j.1600-0587.2013.00506.x
McCully RM, Basson PA, Bigalke RD, De-Vos V, Young E (1975) Observations on naturally acquired hepatozoonosis of wild carnivores and dogs in the Republic of South Africa. Onderstepoort J Vet Res 42:117–134
Meerburg BG, Singleton GR, Kijlstra A (2009) Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 35:221–270. https://doi.org/10.1080/10408410902989837
Melo AL, Witter R, Martins TF, Pacheco TA, Alves AS, Chitarra CS, Dutra V, Nakazato L, Pacheco RC, Labruna MB, Aguiar DM (2016) A survey of tick-borne pathogens in dogs and their ticks in the Pantanal biome, Brazil. Med Vet Entomol 30(1):112–116. https://doi.org/10.1111/mve.12139
Nosil P, Mooers AØ (2005) Testing hypotheses about ecological specialization using phylogenetic trees. Evolution 59:2256–2263. https://doi.org/10.1554/05-169.1
Novotny V, Basset Y (2005) Host specificity of insect herbivores in tropical forests. Proc Royal Soc B 272:1083–1090. https://doi.org/10.1098/rspb.2004.3023
Ossani PC, Cirillo MA (2016) MVar.pt: Análise multivariada (Brazilian Portuguese). https://cran.r-project.org/web/packages/MVar.pt/index.html. Accessed 22 Mar 2020
Poulin R, Morand S (2004) Parasite biodiversity. Smithsonian Institution, Washington, DC. https://doi.org/10.1017/S003118200521908X
Radtke A, Mclennan DA, Brooks DR (2002) Resource tracking in North American Telorchis sp (Digenea: Plagiochiformes: Telorchidae). J Parasitol 88:874–879. https://doi.org/10.1645/0022-3395(2002)088[0874:RTINAT]2.0.CO;2
Rynkiewicz EC, Pedersen AB, Fenton A (2015) An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends Parasitol 31:212–221. https://doi.org/10.1016/j.pt.2015.02.005
Santos FM, Barreto WTG, De Macedo GC, Barros JHDS, Xavier SCDC, Garcia CM, Mourão G, De Oliveira J, Rimoldi AR, Porfírio GEO, De Andrade GB, Perles L, André MR, Jansen AM, Herrera HM (2019) The reservoir system for Trypanosoma (Kinetoplastida, Trypanosomatidae) species in large neotropical wetland. Acta Trop 199:105098. https://doi.org/10.1016/j.actatropica.2019.105098
Sasanelli M, Paradies P, Lubas G, Otranto D, de Caprariis D (2009) Atypical clinical presentation of coinfection with Ehrlichia, Babesia and Hepatozoon species in a dog. Vet Rec 164(1):22–23. https://doi.org/10.1136/vr.164.1.22
Seabloom EW, Borer ET, Gross K, Kendig AE, Lacroix C, Mitchell CE, Mordecai EA, Power AG (2015) The community ecology of pathogens: coinfection, coexistence and community composition. Ecol Lett 18:401–415. https://doi.org/10.1111/ele.12418
Silva MRLD, Mattoso CRS, Costa A, Saito ME, Tchaicka L, O'dwyer LH (2018) Rangelia vitalii and Hepatozoon canis coinfection in pampas fox Lycalopex ymnocercus from Santa Catarina State, Brazil. Rev Bras Parasitol Vet 27(3):377–383. https://doi.org/10.1590/s1984-296120180018
Silveira JA, Rabelo EM, Lacerda AC, Borges PA, Tomás WM, Pellegrin AO, Tomich RG, Ribeiro MF (2013) Molecular detection and identification of hemoparasites in pampas deer (Ozotoceros bezoarticus Linnaeus, 1758) from the Pantanal Brazil. Ticks Tick Borne Dis 4(4):341–345. https://doi.org/10.1016/j.ttbdis.2013.01.008
Supali T, Verweij JJ, Wiria AE, Djuardi Y, Hamid F, Kaisar MMM (2010) Transmission consequences of coinfection: cytokines writ large? Trends Parasitol 23:284–291. https://doi.org/10.1016/j.pt.2007.04.005
Syller J (2012) Facilitative and antagonistic interactions between plant viruses in mixed infections. Mol Plant Pathol 13:204–216. https://doi.org/10.1111/j.1364-3703.2011.00734.x
Vaumourin E, Vourc’h G, Gasqui P, Vayssier-Taussat M (2015) The importance of multiparasitism: examining the consequences of co-infections for human and animal health. Parasit Vector 8:545. https://doi.org/10.1186/s13071-015-1167-9
Viney ME, Graham AL (2013) Patterns and processes in parasite co-infection. Adv Parasitol 82:321–369. https://doi.org/10.1016/B978-0-12-407706-5.00005-8
Wahlberg N (2001) The phylogenetics and biochemistry of host plant specialization in melitaeine butterflies (Lepidoptera: Nymphalidae). Evolution 55:522–537. https://doi.org/10.1111/j.0014-3820.2001.tb00786.x
Wiegmann BM, Mitter C, Farrell B (1993) Diversification of carnivorous parasitic insects - extraordinary radiation or specialized dead-end? Am Nat 142:737–754. https://doi.org/10.1086/285570
Zieman EA, Jiménez FA, Nielsen CK (2017) Concurrent examination of bobcats and ticks reveals high prevalence of Cytauxzoon felis in Southern Illinois. J Parasitol 103(4):343–348. https://doi.org/10.1645/16-133
Funding
The first author received fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (88887.369261/2019-00). HMH and MRA are 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 research was financially supported by CAPES (Finance Code 001).
Author information
Authors and Affiliations
Contributions
Conceptualization: FMS, KCMS, RZM, MRA, and HMH; data curation: FMS and NYS; formal analysis: FMS and NYS; funding acquisition: RZM, MRA, and HMH; investigation: FMS, KCMS, NYS, RZM, MRA, and HMH; methodology: FMS, KCMS, and NYS; project administration: FMS; supervision: FMS; validation: FMS, KCMS, NYS, MRA, and HMH; visualization: FMS, NYS, MRA, and HMH; writing—original draft: FMS; writing—review and editing: FMS, KCMS, NYS, WAGN, SCL, RZM, MRA, and HMH
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
All field and laboratory procedures were performed in accordance with licenses granted by the Biodiversity Information and Authorization System of the Chico Mendes Institute for Biodiversity Conservation (SISBIO) (56912-2). This study was approved by the Ethics Committee for Animal Use of the Dom Bosco Catholic University, Campo Grande, MS (license number 001/2017).
Additional information
Section Editor: Elizabeth Marie Warburton
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Santos, F.M., de Sousa, K.C.M., Sano, N.Y. et al. Relationships between vector-borne parasites and free-living mammals at the Brazilian Pantanal. Parasitol Res 120, 1003–1010 (2021). https://doi.org/10.1007/s00436-020-07028-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-020-07028-0