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Parasitology Research (2024) 123:88
https://doi.org/10.1007/s00436-023-08101-0
RESEARCH
Detection ofTrypanosoma evansi injaguars (Panthera onca): insights
fromtheBrazilian Pantanal wetland
RenataFagundes‑Moreira1· ViniciusBaggio‑Souza1· JoaresAdenilsonMay‑Junior1,2,3· LauraBerger1·
LinaCrespoBilhalva1· AdeyldesOliveiraReis1· LeonardoSartorello2· LilianE.Rampim2·
MarcosAntônioBezerra‑Santos4· DomenicoOtranto4,5· JoãoFabioSoares1
Received: 21 November 2023 / Accepted: 16 December 2023
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2024
Abstract
Trypanosoma evansi is a widespread and neglected zoonotic parasite that affects domestic and wild animals, causing a
disease commonly known as “surra.” The Brazilian Pantanal wetland is recognized as an enzootic area for this protozoan,
yet recognizing the importance of reservoir hosts also in order to prevent zoonotic outbreaks. This study aimed to assess the
occurrence of T. evansi in jaguars (Panthera onca) from the Brazilian Pantanal wetland and explore associated clinical and
hematological manifestations. A total of 42 animals were screened by PCR and sequenced for species identification when
positive. Trypanosoma evansi was detected in six free-ranging jaguars (six positive animals of 42 captures and 16 recap-
tures), representing the first molecular evidence of such infection in this animal species. Our findings suggest that jaguars
may act as reservoir hosts of T. evansi in the Brazilian Pantanal wetland. The better understanding of the role of wildlife
in the epidemiology of T. evansi is also of importance to future reintroduction and translocation programs toward wildlife
conservation efforts.
Keywords Hemoparasite· Protozoan· Wild felids· Tripanossomiasis· Brazil
Introduction
Trypanosoma evansi, the etiological agent of a neglected
disease known as “surra” or in Portuguese “mal das cadei-
ras,” affects a wide range of domestic and wild animals
(Franke etal. 1994; Silva etal. 1995; Herrera etal. 2004),
with sporadic cases also reported in humans (Joshi etal.,
2005; Powar etal. 2006). Previous studies have documented
that many animal species, such as cattle (Franke etal. 1994),
horses (Rodrigues etal. 2005), dogs (Echeverria etal. 2019;
Nguyen etal., 2021), tigers (Upadhye and Dhoot, 2000),
camels (Desquesnes etal. 2008), and bats (Herrera etal.
2004), and even humans may be susceptible to T. evansi
infection. In addition, a zoo outbreak was reported in India,
which many felid species, including jaguars (Panthera
onca), died due to T. evansi (Sinha etal., 1971).
The Brazilian Pantanal biome has been identified as an
enzootic area for T. evansi (Nunes etal. 1993). Therefore,
understanding the ecology of this protozoan in the region is
advocated, especially considering the potential wild reser-
voir hosts (Herrera etal. 2004).
The ecosystem complexity and its biodiversity require a
comprehensive approach to disease ecology, including stud-
ies about potential disease reservoirs among both common
and endangered wildlife species. The jaguar, as one of the
apex predators in South America, merits particular attention,
and although its susceptibility to the infection has been dem-
onstrated in captive animals (Sinha etal., 1971; Khan etal.,
2023), the role of free ranging jaguars in the transmission
dynamics of T. evansi remain understudied. Under the above
Handling Editor: Una Ryan
* João Fabio Soares
joao.soares@ufrgs.br
1 Laboratório de Protozoologia e Rickettsioses Vetoriais,
Faculty ofVeterinary, Universidade Federal doRio Grande
doSul (UFRGS), PortoAlegre, RioGrandedoSul, Brazil
2 Onçafari Association, SãoPaulo, Brazil
3 Panthera Corporation, NewYork, USA
4 Department ofVeterinary Medicine, University ofBari,
Valenzano, Italy
5 Department ofVeterinary Clinical Sciences, City University
ofHong Kong, KowloonTong, HongKong
Parasitology Research (2024) 123:88
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88 Page 2 of 5
circumstances, this study aimed to assess the occurrence of
T. evansi infection in free-ranging jaguars within the Brazil-
ian Pantanal wetland.
Material andmethods
The study was conducted in the municipality of Miranda,
Mato Grosso do Sul state, Brazil, within the Pantanal biome,
between 2013 and 2023 (Fig.1). Jaguars were captured
using foot snares (May-Junior etal. 2021) to collect bio-
logical samples and set GPS/VHF radio collars. The radio
collars had drop-off system after 12 months, so recaptures
were not necessary to remove it. In all animals, we assessed
the health parameters, including mucosal color, capillary
refill, hematocrit, blood smear, rectal temperature, and
weight (kg); also, radio or GPS collars were set when pos-
sible, according to both collar availability and jaguar size.
Only a young female jaguar was not set a radio collar, as
she was young and too small (50 kg). Ethical procedures
were approved by the Ministry of Environment under license
number #42093-1.
Blood samples were collected and processed using the
PureLink® Genomic DNA Mini Kit (Invitrogen™, Carls-
bad, CA, USA) to extract genomic DNA (200 μL volume)
following the manufacturer’s instructions. Molecular detec-
tion of T. evansi involved the use of two specific primer pro-
tocols. Firstly, an assay was caried out to amplify a 315-bp
fragment following Ventura etal. (2002). Subsequently, an
assay was conducted to amplify a ~ 540-bp ITS-1 fragment,
as described by Desquesnes etal. (2001). Blood samples
from experimentally infected mice and naturally infected
dogs were used as positive controls. In order to evaluate the
quantity and quality of the extracted DNA, a NanoDrop™
spectrophotometer at an absorbance of 260/280 nm was
used.
One random sample was selected to retrieve sequence.
Amplicons of the expected size were purified and sequenced
in both directions using the Big Dye Terminator v.3.1 chem-
istry in a 3130 Genetic Analyzer (Applied Biosystems, Cali-
fornia, USA) equipped with an automated sequencer (ABI-
PRISM 377). The resulting sequence was aligned using the
fast Fourier transform algorithm in MAFFT (Katoh etal.
2019) and subsequently compared with reference sequences
available in the GenBank database using the Basic Local
Alignment Search Tool (BLAST). The sequence was submit-
ted to the GenBank database under the accession number:
OR797837.
Results
Six (four females and two males) out of 58 captures
(42 animals and 16 recaptures) scored positive at PCR
(Table1) (Supplementary Table1), representing an occur-
rence of 14.28% (6/42). At the BLAST analysis, the
Fig. 1 Geographical location of the studied area in the Brazilian territory
Parasitology Research (2024) 123:88
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Page 3 of 5 88
evaluated sequence showed 100% nucleotide identity with
T. evansi (Accession number: AB551922.1, AY912279.1,
AF306775.1). The jaguars did not suffer for major clinical
changes at the time of capture. However, two females (bPon
424 and bPon 440) had capillary refill in 2 (bPon 424) and
1.5 s (bPon 440) and presented a senile aspect with white
hair and loss of muscle mass in their hind limbs, probably
associated with aging, as bPon 424 was more than 10 years
old and bPon 440, more than 12 years old. Jaguars main-
tained a regular PCV (Table1), according to the parameters
for the species in the studied region (40.7 ± 5.0—calculus
made from 37 monitored jaguars—data not shown). All
blood smears evaluated through optical microscopy were
negative for Trypanosoma sp.
Discussion
In this study, we report the occurrence of T. evansi in free-
ranging jaguars from the Pantanal wetland in Brazil. While
the role of this animal species in the epidemiology of this
parasite is unknown, the finding herein reported is of impor-
tance since their involvement in the maintenance of T. evansi
in nature.
The absence of clinical signs compatible with T. evansi
infection in animals herein evaluated contrasts with find-
ings from captive jaguars (Sinha etal. 1971), and domestic
cats, that shows clinical signs and positive in blood smears
(Priyowidodo etal. 2023), suggesting that free-ranging indi-
viduals may exhibit a distinct response to this protozoan
infection. Immunotolerance to trypanosomes in carnivores
remains a complex and understudied phenomenon. How-
ever, extrinsic factors, such as the exposure to high chal-
lenges through predation of infected prey and invertebrate
vectors, have been associated with resistance (Murray etal.
1982; Kasozi etal. 2021). In the context of our study popu-
lation of free-ranging jaguars, it is likely that they exhibit
trypanotolerance, mainly considering Pantanal region is an
enzootic area for T. evansi (Herrera etal. 2004). In a simi-
lar scenario, Serengeti lions, which are frequently exposed
to multiple trypanosome species through tsetse fly bites
and the consumption of infected meat, have demonstrated
cross-immunity to Trypanosoma brucei, enabling them to
eliminate the infection after exposure (Welburn etal. 2008).
Furthermore, it is worth noting that one male (bPon 495),
initially tested positive upon capture, scored negative during
a 3-year interval recapture. This observation suggests either
the suppression of the infection or a reduction of trypano-
somiasis to undetectable levels by PCR. This highlights
the complexities of pathogen-host interactions and under-
scores the need for thorough species-specific investigations.
In addition, the jaguar population of this study presents a
high prevalence of infection by Cytauxzoon sp. (Fagundes-
Moreira etal. 2022). The synergism between infections of
distinct pathogens, associated with environmental changes,
had important effects on the populations of African large
felids (Munson etal. 2008).
One of the possible transmission routes to jaguars may
be the ingestion of reservoir preys, once oral transmission
was already suggested in the Indian zoo outbreak (Sinha
etal. 1971, Khan etal., 2023) and proved in dogs and mice
(Raina etal. 1985; Bazolli etal. 2002); additionally, leop-
ards (Panthera pardus) are reservoirs to T. brucei and were
also suspected to be orally infected by its prey (Anderson
etal. 2011). For example, tapirs (Tapirus terrestris) and
capybaras (Hydrochaerus hydrochaeris) are common prey
for jaguars, being also considered reservoirs of T. evansi
in the Pantanal wetlands, with high parasitemia recorded
in capybaras (Franke etal. 1994; Herrera et al. 2004;
Rademaker etal. 2009; Fundación Rewilding Argentina,
2020). The transmission of T. evansi to domestic animals
is commonly associated with tabanid bites (Desquesnes
etal. 2005, Kamidi etal., 2017), but it may also be the
case for wildlife reservoirs. For example, previous studies
Table 1 Captures and
recaptures of Trypanosoma
evansi positive free-ranging
jaguars (Panthera onca)
Kg, kilogram; PCV, packed cell volume; %, percent; nt, not tested
Sample Gender Capture Weight (Kg) PCV (%) Detection of
T. evansi
Month Year
bPon424 Female September 2017 92 nt +
bPon440 Female June 2014 110 38 −
January 2017 100 nt −
November 2018 86.4 38 +
bPon495 Male July 2017 ~ 120 nt +
June 2020 127 nt −
bPon498 Female September 2017 50.7 nt +
bPon509 Female November 2018 60 42 +
bPon522 Male February 2021 96.2 40 +
Parasitology Research (2024) 123:88
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88 Page 4 of 5
demonstrated that tabanid species (e.g., Tabanus importu-
nus, Tabanus occidentalis), associated with T. evansi, were
more prevalent during the rainy season, from September to
the first days of March (Silva etal., 1995; Barros, 2001),
which also coincides with capybaras breeding period
(Aldana-Domínguez etal. 2002). Accordingly, in this
study, five out of six T. evansi positive jaguars were diag-
nosed during the rainy season. Therefore, the increase of
vectors and the availability of “easier” prey (younger and
susceptible capybaras) acting as reservoirs may represent
an important factor in T. evansi transmission to jaguars.
The implications of these findings are far-reaching for
wildlife conservation efforts, especially considering the
critical role of jaguars in the ecological balance of the Pan-
tanal wetland ecosystem. Importantly, our results should
be incorporated into risk assessments for reintroduction or
translocation programs of jaguars and other South Ameri-
can wildlife to prevent accidental pathogen introduction to
a susceptible population and potential disease outbreaks
(Viggers etal. 1993).
Conclusion
Our findings from the Pantanal demonstrate the presence
of subclinical T. evansi in South American free-ranging
jaguars. As our understanding of the relationships between
pathogens, hosts, and the environment continues to grow,
the importance of interdisciplinary research in developing
effective conservation strategies remains undeniable. There-
fore, further studies on the impact of T. evansi on jaguars are
advocated to better understand the risks associated and guide
the safeguarding of biodiversity and long-term survival of
this endangered species.
Supplementary Information The online version contains supplemen-
tary material available at https:// doi. org/ 10. 1007/ s00436- 023- 08101-0.
Acknowledgements The authors would like to thank the Refúgio
Ecológico Caiman, Onçafari Association, Log Nature, Zoetis Inc., and
Leatherman for the support in the conduction of the study. In addi-
tion, the authors thank Viviane Noll Louzada Flores and Livia Perles
(University of Bari, Italy) for the support on the molecular analysis.
Author contributions RFM: Conceptualization, Investigation, Meth-
odology, Writing—original draft preparation. VBS: Formal Analysis,
Methodology, Writing—review and editing. JAMJ: Investigation,
Methodology, Writing—review and editing. LB: Conceptualization,
Formal Analysis, Investigation, Methodology. LCB: Investigation,
Methodology. AOR: Investigation, Methodology. LS: Investigation,
Methodology. LER: Investigation, Methodology. MABS: Investiga-
tion, Methodology, Writing—review and editing. DO: Conceptualiza-
tion, Methodology, Supervision, Writing— review and editing. JFS:
Conceptualization, Investigation, Methodology, Project administration,
Supervision, Writing—review and editing.
Funding This work received support from Fundação de Amparo à
Pesquisa do Rio Grande do Sul (FAPERGS) (Finance code:19/2551–
0001842–8), Conselho Nacional de Desenvolvimento Científico e Tec-
nológico (CNPq), and Coordenação de Aperfeiçoamento de Pessoal de
Nível Superior (CAPES) (Finance code 001). The coauthors MABS
and DO were supported by the EU funding within the MUR PNRR
Extended Partnership initiative on Emerging Infectious Diseases (Pro-
ject no. PE00000007, INF-ACT). The coauthor JFS is funded by CNPq
(Grant #312576/2021-8). This article is based on the development of
activities carried out by RFM during the Programa Institucional de
Internacionalização (CAPES-PRINT) sandwich doctoral period at the
Department of Veterinary Medicine, University of Bari, Italy.
Data availability No datasets were generated or analyzed during the
current study.
Declarations
Ethics approval The procedures herein described were conducted in
accordance with the Brazilian Institute of the Environment and Renew-
able Natural Resources-IBAMA (Authorization n. 42093-1) and the
Research Committee of the Federal University of Rio Grande do Sul-
Compesq (Authorization n. 38198).
Consent to participate Not applicable.
Consent for publication Not applicable.
Competing interests The authors declare no competing interests.
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