Hematology and Serum Chemistry of Free-Ranging Jaguars (Panthera onca) from a Floodplain Forest Site in Amazonia, Brazil

Jaguars (Panthera onca), the largest terrestrial predator within their geographic range, play an essential role in their ecosystems (Cullen 2006). They are classified globally as Near Threatened (Quigley et al. 2017). The Amazon region is one of the few biomes with viable, long-term populations (Soares-Filho et al. 2006).

Hematologic and biochemical values are important for the assessment of wild populations (García et al. 2010). There has been only one previous such study on Brazilian free-ranging jaguars, from the southern Pantanal (Widmer et al. 2012). We describe hematologic and biochemical parameters for jaguars in the Mamirauá Sustainable Development Reserve (2°51′S, 64°55′W) in Brazil, exclusively comprised of flooded forests (várzea) in the Amazon River floodplain. Mamirauá's jaguars remain in the flooded forest throughout the high-water season (3–4 mo), living in the canopy, feeding on arboreal prey, and breeding and raising cubs (Ramalho et al. 2021).

Between 2012 and 2018, we captured 13 jaguars with snare traps (Frank et al. 2003) set on trails and checked every 6 h. Captures occurred January to March, early in the flooding season, when jaguars are probably more easily captured due to less available land for movement. We captured eight males and five females, age >3 yr (estimated by the wear and staining of the teeth; Supplementary Material Table S1). Captured jaguars were darted with mean 8.95 mg/kg tiletamine and zolazepam (Zoletil®, Virbac, São Paulo, Brazil). Anesthetized animals were weighed and heart rate, respiratory movements, temperature, capillary refill time, and oxygen saturation were monitored by a veterinarian every 10 min. Information on the animal's clinical condition, sex, age, weight, and biometric measurements were recorded.

Blood was collected from the femoral vein using Vacutainer needles 25×8 mm (21 ga ×1; BD Biosciences, São Paulo, Brazil) nearly 20 min after immobilization, 4 mL into a K3 tube (Labor Import, Polymed, São Paulo, Brazil) containing ethylenediaminetetraacetic acid for complete blood count and stored on ice packs until analysis, and 10 mL was collected in tubes without anticoagulants (BD Vacutainer, Becton Dickinson and Company, Franklin Lakes, New Jersey, USA) to obtain serum for biochemical evaluation; these were stored at room temperature (∼27 C) until clot formation, then centrifuged (centrifuge 80-2b, Centrilab®, São Paulo, Brazil), with separated serum kept on ice packs until processing. All analyses were performed within 24 h of collection in a commercial laboratory (Laboratório de Análises Clínicas Especializadas, Tefé, Amazonas, Brazil). All jaguars were fitted with radio collars for monitoring (see Supplementary Material).

Hematocrit (Ht) was determined by microcentrifugation (SH 120, Centrilab). Red blood cells (RBC), platelets, and total leukocytes (WBC) were counted by an automated analyzer (ABX Pentra 60, HORIBA ABX, São Paulo, Brazil); the differential leukocyte count was evaluated from blood smears stained with May-Grunwald-Giemsa. The hematimetric indices were calculated using a classic formula (Thrall 2012). Hemoglobin (He) and biochemical variables were measured using a semi-automatic biochemical device (Thermoplate Basic TP Analyzer Basic, Bioclin®, Belo Horizonte, Brazil) using commercial kits.

We calculated mean, SD, 95% confidence interval (CI), and parameter range for all hematologic and biochemical parameters. We tested for parameter differences between sexes using a Student's t-test for parametric data and a Mann-Whitney U-test for nonparametric data. We assessed normality of the data with a Kolmogorov-Smirnov test, homogeneity with a Levene's test, and checked for the presence of outliers with boxplots and Cleveland dot plots.

All jaguars had good body weight and condition, pink mucous membranes, and no detected ectoparasites. All had edema of the snared paw; an anti-inflammatory gel (DM Gel, Vetnil, São Paulo, Brazil) was applied to the affected area. One jaguar (ID11) was pregnant, one (ID3) had palpable hepatomegaly, and one (ID5) had healing wounds (2.0-cm long and 2.5-cm deep) of undefined cause on the forelimbs, plus periodontal disease.

Most jaguars showed higher lymphocytes, monocytes, eosinophils, aspartate aminotransferase (AST), and alanine aminotransferase (ALT) compared with previous means described for free-ranging and captive jaguars (Table 1). Female ID11 and male ID3 were found to be outliers for alkaline phosphatase (ALP) and AST, respectively, and so were excluded from the test for differences between sexes (Table S1). In general, males tended to have higher values than the females (Table 2); these differences were significant for He (t=2.79, P=0.01) and ALP (t=3.28, P=0.01). However, when including the outlier (ID11) for the ALP, we found males and females did not differ significantly (t=–1.02, P=0.33). Removal of outliers for the AST did not affect the results. Jaguars were monitored after capture for 14–458 d.

During monitoring, five individuals died: two killed by local people and three from unknown causes. The others were monitored throughout radio collar battery life. Dead animals could not be located soon enough for necropsy. However, two of the dead animals (ID3 and ID5; Table S2) were those with abnormal clinical findings when captured.

According to previously described parameters for jaguars (Hawkey and Hart 1986; Widmer et al. 2012), ID3 showed increased lymphocytes, AST, and ALT, and decreased albumin. The oldest individual (ID5) showed decreased Ht and He, decreased neutrophils, creatinine, and albumin, and increased AST and ALT.

Hematologic and biochemical profiles with increased lymphocytes, monocytes, eosinophils, AST, and ALT have been found in wild-caught felids such as red lynx (Lynx rufus) and Bornean leopard cat (Prionailurus bengalensis borneoensis) and were attributed to the acute stress caused by capture; intense physical exertion due to pulling against the trap (Fuller 1985) suggesting muscle injury or hepatocellular damage (Allison 2012a, b), which has been previously described for jaguars (Widmer et al. 2012).

We also found significantly higher RBC counts in males than in females. Such a difference has previously been described for Iberian lynx (Lynx pardinus; Beltrán et al. 1991), cougars, tigers, leopards, and jaguars (Hawkey and Hart 1986).

We found lower RBC counts than in previous jaguar studies (Table 1). This might be related to relatively small prey: Mamirauá's jaguars have peculiar feeding habits, feeding mostly on medium-sized prey such as primates and sloths during the flooded season and caimans during the dry season (Ramalho et al. 2021). Florida panthers (Puma concolor coryi) feeding on smaller prey also showed lower reference values for RBC, He, and Ht compared to panthers feeding on larger prey (Dunbar 1997). Our finding of higher ALP values in males than in females is unexplained. Increased ALP was not associated with immaturity (Nájera et al. 2014) or with healing bone fractures (Allison 2012b); none of our jaguars were immature or had any evidence of fractures. In future analyses, it may be important to perform other diagnostic tests to identify the causes of increased ALP activity in males. Higher ALP also has been observed in a pregnant lynx (Lynx rufus; Fuller et al. 1985), which may explain the high ALP observed in the outlier pregnant jaguar (ID11).

We provide the first health assessment associated with clinical condition and movement monitoring for Amazonian jaguars. Most of the individuals were healthy and one was pregnant, suggesting that this jaguar population remains healthy and with reproductive success (Ramalho et al. 2021). Our hematologic and biochemical findings for Amazonian jaguars may improve jaguar health assessments across the biome.

This work was supported by a doctoral grant from the Coordination for the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; CAPES process 88882.328004/2019-01) and by the Gordon and Betty Moore Foundation, which supported the Mamirauá Sustainable Development Institute (IDSM process 5344). We thank all the researchers of the research group in Ecology and Conservation of Felines in the Amazon (Projeto Iauaretê), mainly Marcos Roberto Monteiro de Brito for helping with the jaguar movement data, João Valsecchi, Diego Melo, and Rafael Rabelo for the reviews and discussions, and all field assistants from Mamirauá Reserve who participated in the capture expeditions, including Railgler dos Santos (In memoriam). We also thank the Infrastructure, Logistics, and Administrative IDSM team for the field logistic support. All procedures were approved by the Chico Mendes Institute for Biodiversity Conservation (Instituto Chico Mendes de Conservação da Biodiversidade; ICMBio/SISBIO 11095-6) and by the Ethics Committee on the Use of Animals da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo (Comissão de Ética no Uso de Animais; CEUA/FMVZ/USP 3810160517).

Supplementary material for this article is online at http://dx.doi.org/10.7589/JWD-D-21-00012.