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Parasites of Caiman Yacare Daudin, 1802 (Crocodylia: Alligatoridae) in the Tacana Indigenous Territory (Beni River Basin), Bolivia

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Parasites of Caiman Yacare Daudin, 1802 (Crocodylia: Alligatoridae) in the Tacana Indigenous Territory (Beni River Basin), Bolivia Neotropical Hydrobiology and Aquatic Conservation (2021) Vol. 2 (1): 38-61 Hidrobiología Neotropical y Conservación Acuática (2021) Vol . 2 (1): 38-61 Parasites of Caiman yacare Daudin, 1802 (Crocodylia: Alligatoridae) in the Tacana Indigenous Territory (Beni River basin), Bolivia Parásitos de Caiman yacare Daudin, 1802 (Crocodylia: Alligatoridea) SCIENTIFIC ARTICLE en el Territorio Indígena Tacana (cuenca del río Beni), Bolivia ARTÍCULO ORIGINAL Jose Luis MOLLERICONA1*, Gustavo ÁLVAREZ1, Vanessa RAMOS2, Amilcar MAIDANA2, Saúl CALLANCHO3, Robert WALLACE1 & Guido MIRANDA1 1 Wildlife Conservation Society, Greater Madidi–Tambopata Landscape Conservation Program, #340 Citation/ Citación: Mollericona Gabino Villanueva Street, Calacoto, La Paz, Bolivia J.L., Alvarez G., Ramos V., Maidana 2 A., Callancho S., Wallace R., El Alto Public University, School of Veterinary Medicine and Zootechnicians, Sucre s/n Avenue, Villa Miranda G. (2021). Parasites of Esperanza área, El Alto, Bolivia. 3 Caiman yacare Daudin, 1802 El Alto Public University, School of Enginneering and Applied Zootechnicians, Sucre s/n Avenue, Villa (Crocodylia: Alligatoridae) in the Esperanza área, El Alto, Bolivia. Tacana Indigenous Territory (Beni *Corresponding author: [email protected] River basin), Bolivia. Neotropical Hydrobiology and Aquatic Conservation, 2 (1): 38-61 Received/Recibido: 31 October ABSTRACT 2020/31 de Octubre 2020 Accepted/Aceptado: 13 May The yacaré caiman (Caiman yacare) is of great nutritional and 2021/13 de Mayo 2021 economic importance for Indigenous people. The sustainability of the Published/Publicado: 15 June national yacare caiman conservation management program in Bolivia 2021/15 de Junio 2021 is measured by population censuses. To learn about the parasites in Copyright: © Editorial INIA caimans and establish further criteria for the management and use of the species, samples of 113 caimans were collected during annual Acceso abierto/Open access article harvests by the Cachichira community in the Tacana Indigenous Territory in the Abel Iturralde province of the La Paz Department between 2017 and 2019. Laboratory analyses showed nine endoparasite species with varying prevalence (Alofia platycephala 96.5%, Capillariidae 7.1%, Dujardinascaris sp. 0.9%, Eimeria paraguayensis 31%, Eimeria caimani 12.4%, Micropleura vazi 10.6%, Polyacanthorhynchus rhopalorhynchus 42.5%, Sebekia oxycephala 40.7%, an unidentified Trematode species 0.9%) and one ectoparasite species (Amblyomma crassum 0.9%). The Kruskal-Wallis statistic showed a significant difference in parasitic prevalence between all sampled individuals (p <0.001), and between individuals harvested in streams (p <0.001) and lagoons (p <0.001). A correspondence analysis of parasite composition revealed that 38 Parasites of Caiman yacare Mollericona et al. (2021) Dujardinascaris sp. presented a very close association to lagoons, and trematodes were associated with streams. Parasite-host associations and caiman behavior are discussed. This study constitutes the first record of parasites in Caiman yacare for the La Paz Department in Bolivia. Keywords: Host-parasite relationships, prevalence, sustainable use RESUMEN El lagarto (Caiman yacare) es de gran importancia para los indígenas por su aporte nutricional y económico. La sostenibilidad del programa nacional de manejo y conservación del lagarto en Bolivia se mide mediante censos de población. Para conocer los parásitos en los lagartos y establecer más criterios sobre el manejo y uso de la especie, se recolectaron muestras de 113 lagartos durante las cosechas anuales por la comunidad Cachichira en el Territorio Indígena Tacana en la provincia Abel Iturralde del Departamento de La Paz entre 2017 y 2019. Los análisis de laboratorio registraron nueve especies de endoparásitos con prevalencias variables (Alofia platycephala 96,5%, Capillariidae 7,1%, Dujardinascaris sp. 0,9%, Eimeria paraguayensis 31%, Eimeria caimani 12,4%, Micropleura vazi 10,6%, Polyacanthorhynchus rhopalorhynchus 42,5%, Sebekia oxycephala 40,7%, una especie no identificada de trematodos 0,9% y una especie de ectoparásito (Amblyomma crassum 0,9%). La estadística de Kruskal-Wallis mostró una diferencia significativa en las prevalencias parasitarias entre todos los individuos muestreados (p <0,001) y entre los individuos recolectados en arroyos (p <0,001) y lagunas (P <0,001). Un análisis de correspondencia de la composición de parásitos reveló que Dujardinascaris sp. presentó una asociación muy estrecha con las lagunas, y los trematodos se asociaron con los arroyos. Se discuten las asociaciones parásito-huésped y el comportamiento de los lagartos. Este estudio constituye el primer registro de parásitos en Caiman yacare para el Departamento de La Paz en Bolivia. Palabras clave: Relaciones huésped-parásito, prevalencia, uso sostenible INTRODUCTION The yacaré caiman (Caiman yacare Daudin 1802) is one of six Alligatoridae species found in Bolivia (Pacheco 1996, Rueda-Almonacid et al. 2007), and is distributed in the lowlands of the Beni, Pando, Santa Cruz, Cochabamba, La Paz and Tarija 39 Parasites of Caiman yacare Mollericona et al. (2021) departments (Rodríguez 2006, CIPTA/WCS 2010). In the 1960s, hunting pressure caused population declines of the species, leading to its inclusion in Appendix II of the International Convention for Wildlife Trafficking (CITES) and the regulation of its commercial use. The yacaré caiman is currently classified as “Least Concern” in Bolivia according to the national red list (Cortez 2009). Wild yacaré caiman populations in Bolivia are now subject to management for meat and hides, within the National Program for Caiman Conservation and Sustainable Use, authorized by the General Directorate of Biodiversity and Protected Areas (DGBAP) (CIPTA/WCS 2010, Miranda-Chumacero et al. 2010, Rivera et al. 2016), and the sustainable use of caiman has become a conservation strategy for the species and its habitats (Garcia & Rojas 2014). A legal economic value for the yacaré caiman provides further incentive to the stakeholders where the caiman lives to protect this resource, and together with the correct application of the norms, procedures and regulations within the management plan, including the restriction of the harvest in unauthorized bodies of water and the illegal sale of hides, encourages a transparent management (Llobet 2002, Aparicio & Ninon 2005). This initiative shows that the responsible management of the resource, supported by the authorities and valued by the market, achieves benefits for the communities and supports conservation (Miranda et al. 2010, Alvarez et al. 2018). The yacaré caiman is an economically important species for many Indigenous People. The Tacana Indigenous People prioritized the sustainable use of caiman within their Life Plan for the Tacana Indigenous Territory which focuses on natural resource management in the La Paz Department of Bolivia. Since 2007, the Matusha Aidha (meaning yacaré caiman in Tacana) Association organized and conducted the sustainable management of caiman for the annual harvest of meat, hides and by- products, such as oil and other parts for handicrafts (CIPTA/WCS 2010). In 2018, the participating Tacana communities implemented a mobile slaughterhouse, meeting authority requirements, including a formal health registration (No. 1396/2018 SENASAG), which allows vacuum packed and frozen meat to be extracted for supermarkets and restaurants, with meat sales now the main harvest income (Miranda 2020). The Matusha Aidha Association continues to develop pioneering studies on the genetics, biology and health, generating further inputs for its sustainable management. Caimans host a variety of parasites that are acquired by ingestion of intermediate hosts (as part of the diet), attachment to the skin, or by the accidental consumption of plants or feces which have infective stages (Ávila 2009). Several studies on the parasitic fauna of caiman in South America (Supplementary Table 1) described either new species, or focused on parasitic ecology. However, only a few parasitic records exist in Bolivia: Alofia platycephala, Hepatozoon caimani, Micropleura vazi and Polyacanthorhynchus rhopalorhynchus (Mollericona & Limachi 2011, Mollericona et al. 2018). For yacaré caiman it is important to document parasitic species and assess possible zoonosis to humans due to the consumption of fresh and dehydrated meat. Although there are no reports of direct transmission of caiman parasites to humans, one case of human dermatitis caused by Sebekia was recorded in Costa Rica (Mairena et al. 1989). 40 Parasites of Caiman yacare Mollericona et al. (2021) Given the importance of caiman populations for Indigenous People in terms of traditional use and sustainable management, here we present information about parasite diversity in Caiman yacare in the Tacana Indigenous Territory, Bolivia. MATERIALS AND METHODS The research was carried out between September and October in 2017, 2018 and 2019, in water bodies near the Cachichira community, located on the Beni river within the Tacana Indigenous Territory in the San Buenaventura municipality and Abel Iturralde province of the La Paz Department (13°56’14.32” S, 67°32’31.31” W). Sampled animals were part of the harvest from the sustainable caiman use program in the Tacana Indigenous Territory through the approved management plan and administrative resolution VMABCCDF N° 025/18 issued by the national authority. A total of 113 individuals ranging between 154 and 266 cm of ventral length were
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