Diversity and prevalence of zoonotic infections at the animal-human interface of primate trafficking in Peru

Abstract

Wildlife trafficking creates favorable scenarios for intra- and inter-specific interactions that can lead to parasite spread and disease emergence. Among the fauna affected by this activity, primates are relevant due to their potential to acquire and share zoonoses - infections caused by parasites that can spread between humans and other animals. Though it is known that most primate parasites can affect multiple hosts and that many are zoonotic, comparative studies across different contexts for animal-human interactions are scarce. We conducted a multi-parasite screening targeting the detection of zoonotic infections in wild-caught monkeys in nine Peruvian cities across three contexts: captivity (zoos and rescue centers, n = 187); pet (households, n = 69); and trade (trafficked or recently confiscated, n = 132). We detected 32 parasite taxa including mycobacteria, simian foamyvirus, bacteria, helminths, and protozoa. Monkeys in the trade context had the highest prevalence of hemoparasites (including Plasmodium malariae/brasilianum, Trypanosoma cruzi, and microfilaria) and enteric helminths and protozoa were less common in pet monkeys. However, parasite communities showed overall low variation between the three contexts. Parasite richness (PR) was best explained by host genus and the city where the animal was sampled. Squirrel (genus Saimiri) and wooly (genus Lagothrix) monkeys had the highest PR, which was ~2.2 times the PR found in tufted capuchins (genus Sapajus) and tamarins (genus Saguinus/Leontocebus) in a multivariable model adjusted for context, sex, and age. Our findings illustrate that the threats of wildlife trafficking to One Health encompass exposure to multiple zoonotic parasites well-known to cause disease in humans, monkeys, and other species. We demonstrate these threats continue beyond the markets where wildlife is initially sold; monkeys trafficked for the pet market remain a reservoir for and contribute to the translocation of zoonotic parasites to households and other captive facilities where contact with humans is frequent. Our results have practical applications for the healthcare of rescued monkeys and call for urgent action against wildlife trafficking and ownership of monkeys as pets.

Fig 1. Map of Peru showing the distribution of the study population by context and city.

Pie charts are proportional to the number of monkeys sampled in each city, whether at government-regulated captive facilities (Captivity, black), at households (Pet, light blue), or at markets (Trade, pink). Insert shows the location of Peru in South America. See Table 2 for further details.

Fig 2. Prevalence of zoonotic parasites in captive monkeys in Peru.

Bars and dots correspond to the prevalence of each parasite type in the sampled population (red) and among animal-human contexts (grey). Vertical lines indicate 95% confidence intervals. Horizontal lines preceded by an asterisk indicate significant difference between categories (p<0.05). MTBC: Mycobacterium tuberculosis complex; n: number of individuals tested for each parasite type.

Fig 3. Parasite community similarities among animal-human contexts.

Principal component (PC) analysis showing the variance in parasite presence among host genera and context in two dimensions. The symbols represent the parasite community of each monkey genus at each animal-human context, and the distance between them illustrates their dissimilarity. Ellipses correspond to the 95% confidence interval for each context.

Fig 4. Risk factors for Parasite Richness (PR) in captive, pet, and traded monkeys in Peru.

Incidence Rate Ratio (IRR) for PR calculated using a negative binomial regression model adjusted by the maximum possible detection of the tests carried on each monkey. IRR: adjusted incidence rate ratio; 95% C.I.: 95% confidence interval; ref: reference group. Dots and lines correspond, respectively, to the adjusted IRR and 95% C.I. of the full model.