Organochlorine pesticide exposure levels and haemoparasite infections as health parameters for leopards in South Africa

Abstract

Compared to aquatic ecosystems, limited information exists on associated health parameters influencing terrestrial vertebrates, specifically large carnivores, and discussions around wildlife health measures are currently still quite rare. The African leopard Panthera pardus pardus (Linnaeus, 1758), a popular species for research by ethologists and ecologists, has a noticeable gap in knowledge regarding health status and assessment. Therefore, the main aim of this study was to use a multi-disciplinary approach that combines relatively diverse parameters to establish an integrated approach to the health assessment of ex-situ (captive) and in-situ (wild) South African leopards. Peripheral blood is an informative, non-lethally sampled tissue that can reflect the functioning of a whole organism. Thus, three overarching whole blood-related aspects, namely haematology, haemoparasitology and organochlorine pesticide (OCP) concentrations, were integrated with a newly designed body condition (BC) scoring system, specific to big cats, to evaluate the interaction of these internal and environmental variables from a health parameter perspective. This study detailed haematological characteristics, confirming great variation in differential blood cell counts and morphologies in leopards, as had been reported for other felids. Differential leukocyte counts of leopards were in the same range as that of other big cats and wild leopards had higher leukocyte counts than captive leopards. Overall, neutrophils were the most numerous circulating leukocyte, followed by lymphocytes and eosinophils. Apicomplexan haemoparasites from the genus Hepatozoon Miller, 1908 (Apicomplexa: Adeleorina: Hepatozoidae) have been widely reported from wild carnivores in Africa, including non-specific reports from leopards, but descriptions of potential developmental stages in naturally infected leopards and associated haematophagous vectors are rare. This study presented detailed morphological and molecular descriptions of two, concurring new haemogregarine species, Hepatozoon luiperdjie Van As et al. 2020 and Hepatozoon ingwe Van As et al. 2020, along with their associated host cell effects. It also described the first morphological traits of potential hepatozoan life cycle stages within an Ixodes tick (Arthropoda: Ixodida: Ixodidae), collected from a naturally infected animal. No clinical symptoms that could be ascribed to hepatozoonosis were observed, confirming the asymptomatic nature of these infections in large carnivores. The first report on baseline OCP concentrations in the blood of African leopards, and relationships between OCP levels, was presented in this study. Captive leopards had a slightly higher mean ΣOCP concentration (901 pg/ml) than wild leopards (768 pg/ml) and OCPs accumulated in the following order DDTs (27%) > HCHs (21%) > Heptachlors (15%) > CHLs (15%) > Drins (14%) > HCB (8%). Finally, this study put forth a noteworthy interplay in the importance of body condition, haematological characteristics, haemogregarine infections and OCP burdens in captive and wild leopards. The most influential health factor for all leopards was neutrophil-to-lymphocyte ratios (NLRs), followed by other leukocyte counts (lymphocyte, neutrophil, and eosinophil counts in decreasing order of influence) and BC.

Body condition, NLR and OCP factors were the most influential variables for captive leopards, while differential leukocyte counts and haemoparasite infections were the most influential for wild leopards. The results from this study suggested the importance of focusing environmental parasitology studies on terrestrial environments. Ultimately, this thesis has shown that an integrated philosophy of leopard health, merging the variables identified in this study, is valuable as a future tool of health assessment.