Hemoparasites in a wild primate: Infection patterns suggest interaction of Plasmodium and Babesia in a lemur species

Abstract

Hemoparasites can cause serious morbidity in humans and animals and often involve wildlife reservoirs. Understanding patterns of hemoparasite infections in natural populations can therefore inform about emerging disease risks, especially in the light of climate change and human disruption of natural ecosystems. We investigated the effects of host age, sex, host group size and season on infection patterns of Plasmodium sp., Babesia sp. and filarial nematodes in a population of wild Malagasy primates, Verreaux's sifakas (Propithecus verreauxi), as well as the effects of these infections on hematological variables. We tested 45 blood samples from 36 individuals and identified two species of Plasmodium, one species of Babesia and two species of filarial nematodes. Plasmodium spp. and Babesia sp. infections showed opposite patterns of age-dependency, with babesiosis being prevalent among young animals, while older animals were infected with Plasmodium sp. In addition, Babesia sp. infection was a statistically significant negative predictor of Plasmodium sp. infection. These results suggest that Plasmodium and Babesia parasites may interact within the host, either through cross-immunity or via resource competition, so that Plasmodium infections can only establish after babesiosis has resolved. We found no effects of host sex, host group size and season on hemoparasite infections. Infections showed high prevalences and did not influence hematological variables. This preliminary evidence supports the impression that the hosts and parasites considered in this study appear to be well-adapted to each other, resulting in persistent infections with low pathogenic and probably low zoonotic potential. Our results illustrate the crucial role of biodiversity in host-parasite relationships, specifically how within-host pathogen diversity may regulate the abundance of parasites.

Wild African great apes as natural hosts of malaria parasites: current knowledge and research perspectives

“…infection levels in younger individuals also seem to confer protection against Plasmodium spp. infections, possibly via shared resource competition (Springer et al, 2015). Inhibition of Plasmodium cynomolgi infection by Babesia microti was also previously described in experimental rhesus macaques (van Duivenvoorde et al, 2010;Voorberg-vd Wel et al, 2008).…”

Sleeping site ecology, but not sex, affect ecto- and hemoparasite risk, in sympatric, arboreal primates (Avahi occidentalis and Lepilemur edwardsi)

“…The top hit was an unnamed filarial nematode, which had been found in another lemur species, the Verreaux’s sifaka ( Propithecus verreauxi ) (query coverage: 47%, identity: 96%, E-value: 0; GenBank accession no. : LN869520) [ 43 ].…”

“…Unfortunately, only microfilaria DNA from one sample of L. edwardsi , taken in the rainy season, could be successfully sequenced. The generated sequence was most similar to sequences derived from microfilariae found in Verreaux’s sifakas ( Propithecus verreauxi ), belonging to the family Onchocercidae with no further assigned name [ 43 ]. To date, these are the only two sequences from Malagasy filarial nematodes which are available in the NCBI GenBank.…”

“…Filarial nematodes have a long prepatent period and once developed, they persist in their host for several months, possibly concealing a seasonal effect. In Kirindy Forest, a habitat with comparable seasonal conditions to those in Ankarafantsika National Park, Verreaux’s sifakas ( Propithecus verreauxi ) hosting microfilaria also showed no effect of seasonality on infection [ 43 ]. However, when looking at the level of microfilaremia as a proxy for infection intensity, the model containing the factor season in L. edwardsi differed significantly from the null model, indicating higher infection intensity in the rainy season (cf.…”

Blood transcriptomes reveal novel parasitic zoonoses circulating in Madagascar's lemurs

“…Phylogenetic analyses of these parasites reveal genetic similarity to species found in domestic cats, cattle and rodents, data that suggest host-spillover events mediated by tick vectors on Madagascar (figure 2; electronic supplementary material, tables S1 and S2). This observation is further supported by the recent discovery of Babesia canis, a species commonly associated with domesticated dogs, circulating in Propithecus verreauxi from western Madagascar [20]. In the light of these results, veterinarians and human health officials working in Madagascar, or with patients who have originated from or travelled to Madagascar, should consider a broader array of tick-borne pathogens when diagnosing illness.…”