Neotropical Hydrobiology and Aquatic Conservation (2021) Vol. 2 (1): 38-61 Hidrobiología Neotropical y Conservación Acuática (2021) Vol . 2 (1): 38-61

Parasites of yacare Daudin, 1802 (Crocodylia: ) in the Tacana Indigenous Territory ( basin),

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, , , Bolivia J.L., Alvarez G., Ramos V., Maidana 2 A., Callancho S., Wallace R., 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 and establish further criteria for the management and use of the , 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 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, , 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 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 used for this study. Samples were taken in 11 water bodies in three different habitats: stream (Moa, Pata de Gallo, Rectangular, Tarene), lake (Moa, Moa Sur) and lagoon (Colorado, Colorado Majal, Majal, Tres Hamacas, Tres Hamacas 3) (Table 1).

TABLE 1. Water bodies sampled Water body Site Latitude Longitude in the Cachichira community, Tacana Indigenous Territory. Lagoon Colorado -13.937311 -67.542030 Colorado-Majal -13.941361 -67.545133 Majal -13.950346 -67.560200 Tres Hamacas -13.911051 -67.539801 Tres Hamacas 3 -13.901946 -67.543590 Lake Moa -14.064136 -67.591261 Moa Sur -14.115347 -67.587063 Stream Moa -14.017145 -67.592031 Pata de gallo -13.915872 -67.530403 Rectangular -14.021411 -67.584144 Tarene -13.809097 -67.52914

After obtaining meat and hide by-products, we searched for adult parasites in the thoracic cavity by making an incision at the level of the sternum, and examined the lungs for endoparasites. The last portion of the large intestine was also dissected to collect feces (Tantaleán 2010). Endoparasites were collected with precision tweezers and placed in petri dishes where they were washed in distilled water and then fixed

41 Parasites of Caiman yacare Mollericona et al. (2021)

and preserved in 75% ethanol. Stool samples (15g) were collected from the rectum and deposited in plastic bottles with 10% formaldehyde. All parasitic samples were labeled for identification and sent to the Wildlife Conservation Society laboratory in La Paz. Stool samples were analyzed using coprological enrichment methods (flotation and sedimentation) to search for parasite eggs and oocysts. Adult parasites were diaphanized with Amann’s Lactophenol and metric measurements (mm) were taken with a binocular light microscope Olympus C 33. Taxonomic keys were used to morphologically identify endoparasites (Travassos 1933, Aquino-Shuster & Duszynski 1989, Vicente et al. 1993, Santos et al. 1996, Moravec & Spratt 1998, Junker 2002). Ectoparasites were collected directly from the back of individuals upon arrival at the harvesting center. These specimens were deposited in a plastic test tube and preserved in 75% ethanol. Ectoparasites were examined using a stereomicroscope, measured with the Motic Version 2.0 program, and identified using taxonomic keys (Robinson 1926, Voltzit 2007). Statistical analyses were performed in the R environment (RDevelopmentCoreTeam 2019), using Kruskal-Wallis to compare richness and prevalence, and a correspondence analysis and a non-parametric multi- dimensional scaling analysis (NMDS) to analyze species composition.

RESULTS

Ten parasite species (Fig. 4-7) were identified in 113 caimans sampled from three water body types (stream, n = 25; lake, n = 10; lagoon, n = 78), including nine endoparasites (Alofia platycephala Lorhman 1889, Capillariidae, Sebekia oxycephala Diesing 1835, Dujardinascaris sp., Micropleura vazi Travassos 1933, Eimeria caimani Aquino-Shuster & Duszynski 1989, E. paraguayensis Aquino- Shuster & Duszynsk 1989, Polyacanthorhynchus rhopalorhynchus Diesing 1850, and an unidentified trematode egg), as well as one ectoparasite (Amblyomma crassum Robinson 1926). The majority of individuals (97.4%) presented parasitic infestation. The highest prevalence was for A. platycephala (96.5%), P. rhopalorhynchus (42.5%), and S. oxycephala (40.7%), with lower percentages for Dujardinarcaris sp., and the unidentified trematode (0.9%) (Table 2). The species richness of parasites found in the three types of water bodies was not significantly different (χ2 = 0.6639, df = 2, p = 0.7175). Significant differences were found in the prevalence of parasite species (χ2 = 67.7, df = 8, p <0.0001, Fig. 1). The prevalence values are separated in groups: i) High - A. platycephala (96.5%), ii) Medium - P. rhopalorhynchus (42.5%), S. oxycephala (40.7%), E. paraguayensis (31%), iii) Low - E. caimani (12.4%), M. vazi (10.6%), Capillariidae (7.1%) and iv) Very Low - Dujardinascaris sp. (0.9%), and the unidentified trematode (0.9%).

42 Parasites of Caiman yacare Mollericona et al. (2021)

TABLE 2. Prevalence Water body type of parasites in Caiman yacare in different water Parasite species Stream Lagoon Lake Total bodies: + = number + % + % + % + % of positive cases, % = percentage infestation. Alofia platycephala 23 92 76 97.4 10 100 109 96.5 Sebekia oxycephala 8 32 36 46.2 2 20 46 40.7 Micropleura vazi 0 0 12 15.4 0 0 12 10.6 Capillariidae 0 0 7 9 1 10 8 7.1 Dujardinascaris 0 0 1 1.3 0 0 1 0.9 Polyacanthorinchus rhopalorhynchus 17 68 26 33.3 5 50 48 42.5 Eimeria paraguayensis 7 28 25 32.1 3 30 35 31 Eimeria caimani 4 16 9 11.5 1 10 14 12.4 Trematode (Digenea) 1 4 0 0 0 0 1 0.9 Amblyomma sabanerae 0 0 1 1.3 0 0 1 0.9

100

A.platycephala 75 Capillariidae sp Dujardinascaris sp E. caimani 50 E. paraguayensis M. vazi Prevalence (%) P. rhopalorhynchus 25 S. oxycephala Trematoda

0

FIGURE 1. Total prevalence of Caiman yacare parasites (X2=67.699, df=8, p<0.0001). The black centre line denotes the median value (50th percentile), the box indicates the 25th to 75th percentiles, the whiskers mark the 5th and 95th percentiles, and values beyond these upper and lower bounds are considered outliers, marked by black dots.

43 Parasites of Caiman yacare Mollericona et al. (2021)

Parasite prevalence within specific water bodies (Fig. 2a and 2b) showed a similar pattern to the global analysis, both in streams (χ2 = 29.7, df = 8, p = 0.0002) and in lagoons (χ2 = 26.5, df = 8, p = 0.0009). In both water bodies, A. platycephala (96.1%), S. oxycephala (42.7%), P. rhopalorhynchus (41.8%), and E. paraguayensis (31.1%) presented high to medium prevalence, compared to other species such as E. caimani (12.6%), M. vazi (11.7%), Capillariidae (6.8%), Dujardinascaris sp. (0.9%) and the unidentified trematode (0.9%). a) 100

75 A.platycephala E. caimani 50 E. paraguayensis P. rhopalorhynchus

Prevalence (%) S. oxycephala 25 Trematoda

0

b) 100

75 A.platycephala Capillariidae sp Dujardinascaris sp 50 E. caimani E. paraguayensis

Prevalence (%) M. vazi 25 P. rhopalorhynchus S. oxycephala

0 44 Parasites of Caiman yacare Mollericona et al. (2021)

c) 100

75 A.platycephala Capillariidae sp 50 E. caimani E. paraguayensis

Prevalence (%) P. rhopalorhynchus 25 S. oxycephala

0

FIGURE 2. Total prevalence of Caiman yacare parasites a) harvested from streams (X2=29.73, df=8, p=0.0002); b) harvested from lagoons (X2=26.468, df=8, p=0.0009); c) harvested from lakes (X2=13.64, df=8, p=0.0916). See Figure 1 for explanation of box whisker plots.

We did not detect a significant difference in the prevalence of parasites that inhabit lakes (χ2 = 13.64, df = 8, p = 0.092, Fig. 2c), although this may be due to a small sample size in this habitat. The correspondence analysis (Fig. 3) revealed that the composition of the parasite communities is very similar in all habitats. However, Dujardinascaris sp. is especially associated with lagoons, and the unidentified trematode is mostly associated with streams. Finally, we registered an ixodid specimen, identified as Amblyomma crassum, representing the first Bolivian record in C. yacare.

DISCUSSION

The present study is the first to document the parasites of Caiman yacare in the Tacana Indigenous Territory in Bolivia, revealing 10 new parasite records. These findings are similar to other studies conducted in South America (Table 1), although the species richness is low compared to studies in (Catto 1991, Catto & Amato 1994, Catto 2000, Junker & Boomker 2006, Brito et al. 2012, Tellez 2013), where 37 parasites species were reported. In (Goldberg et al. 1991) nine parasites

45 Parasites of Caiman yacare Mollericona et al. (2021)

species were reported, in (Troiano et al. 1996, Fernández et al. 2016) two species, and one in (Dubois 1988, Tellez et al. 2013). The low species richness could be related to the presence of intermediate hosts that are part of the caiman diet, as well as habitat type (Lopes 2016). In the present study, the harvest area is characterized by low levels of human activity, and there is no alteration in the community structure of wild animals, possibly related to the absence of intermediate hosts that increase the parasitic richness in the study area (Viera 2011). Parasite prevalence was high for A. platycephala (96.5%) and S. oxycephala (40.7%), compared with previous studies in Argentina (Troiano et al. 1996) where a A. plathycephala prevalence of 80% was registered for Caiman yacare.

FIGURE 3. Plots of the two canonical axes of a correspondence analysis on caiman parasites of the Tacana Indigenous 2 Territory. Laguna Tres Hamacas Dujardinascaris sp

Arroyo Rectangular 1 Arroyo Moa Laguna Colorado Majal

E. caimani Lago Moa Sur E. paraguayensis P. rhopalorhynchus 0 Lago Moa S. oxycephala A. platycephala Capillariidae sp CA2 Arroyo Tarene Laguna Colorado M. vaz i Laguna Majal

-1

Laguna Tres Hamacas 3

-2

Arroyo Pata de gallo Trematoda sp.

-3

-2 0 2 CA1

46 Parasites of Caiman yacare Mollericona et al. (2021)

Another study on S. oxycephala in Brazil (Vicentin 2009), from two fish species (Pygocentrus nattereri Kner 1858 and Serrasalmus marginatus Valenciennes 1837), that are part of the caiman’s diet in the study area (Miranda et al. in prep), recorded a lower prevalence of 29.6% and 7.7%, respectively. The pentastomids A. platycephala and S. oxycephala require fish as intermediate hosts to complete their biological cycle, including: Electrophorus electricus Linnaeus 1766, Serrasalmus nattereri Gunther 1864, Serrasalmus marginatus Valenciennes 1837, Synbranchus marmoratus Bloch 1795, Stenarchus albifrons Bloch & Schneider 1801, Pseudoplatystoma corruscans Spix & Agassiz 1829, Potamotrygon motoro Muller & Henle 1841, P. fasciatum Linnaeus 1766, Pseudoplatystoma spp., Phalloceros harpagos Lucinda 2008, Poecilia reticulata Peters 1859, Pygocentrus nattereri Kner 1858, P. piraya Muller & Troschel 1848, Salmo tamuco Kner 1860, Salminus brasiliensis Cuvier 1816, Silurus pintado Natterer 1836, Hoplias malabarius Bloch 1794 (Amin et al. 1996, Brito et al. 2012, Castro et al. 2014, Moreira et al. 2014, Silva et al. 2015). Of the 17 species of fish described as intermediate hosts for pentastomids, 12 species are present in Bolivia (Sarmiento et al. 2014). More than 50 fish species were recorded in the study area, including species identified as intermediate hosts of pentastomids: Serrasalmus spp., Pygocentrus nattereri, Pseudoplatystoma sp., Potamotrygon sp., and Salminus brasiliensis (CIPTA/WCS 2010). There are no local studies that detail the diversity of fish as intermediate hosts of pentastomids, which would help to better understand the relationship between parasites, fish as intermediate hosts and the definitive hosts. About the pathology, the studies show that pentastomids can lead to multifocal granulomatous inflammation of the lung parenchyma, mainly associated with secondary infections by Aeromonas sp. bacteria, or fungal infiltration, as well as thickening of the alveolar septa (Junker et al. 1999). In high infestations, the host may present respiratory failure, massive necrotic lesions, and hemorrhage (Cardoso et al. 2014). The 42.5% prevalence for P. rhopalorhynchus is lower than one study in Brazil (Catto 1991) with 72.4% in 64 caimans evaluated, but higher than another on Caiman crocodilus with 16.7% in 6 animals evaluated. The prevalence of P. rhopalorhynchus. in the fish species Hoplias malabaricus (Bloch 1794) was 50% (Amin et al. 1996) slightly higher than that registered for the sampled caiman. Acanthocephalan parasites require intermediate hosts such as micro- crustaceans, including ostracods and copepods (Santana et al. 2017). Fish host P. rhopalorhynchus cystachanths in viscera (Amin et al. 1996). Thus, parasite groups with the highest prevalence, such as acanthocephalans and pentastomids, are transmitted by intermediate hosts that form a common part of the caiman diet, as well as their coevolutionary history (Catto 1991, Goldberg et al. 1991). Acanthocephalan infestations can develop pathologies such as chronic inflammatory responses, mechanical trauma caused by the proboscis, with subsequent fibrosis and the formation of nodules, similar to the inflammatory response triggered by an inanimate irritant body, sometimes causing the death of the host (Nuñez & Drago 2017). In intermediate hosts such as fish, they invade the liver causing hepatocytosis necrosis of the connective tissue, as well as tissue hemorrhages (Amin et al. 1996). 47 Parasites of Caiman yacare Mollericona et al. (2021)

For nematodes, we registered a prevalence of 10.6% for M. vazi, 7.1% for Capillariidae and 0.9% for Dujardinascaris sp. The prevalence registered for M. vazi is higher than the prevalence recorded in Paraguay (Goldberg et al. 1991), where a prevalence of 1% for M. vazi and 2% for D. paulista in 115 samples was registered. Other studies in Brazil recorded higher prevalence: 78.1% for M. vazi, 32.8% for Dujardinascaris sp., and 17.1% for Capillaria sp. in 64 caimans (Catto 1991), and 16.7% for D. longispicula (Lopes 2016). A Caiman latirostris stool study in hatcheries reported a 13.9% prevalence for Capillaria sp., and 10% for Dujardinascaris sp. (Batista et al. 2011, Batista et al. 2012). In Mexico, free-living Crocodylus acutus had a prevalence of 76% for D. helicina (Nácar-Muñoz et al. 2016). In this study, the taxonomic identity of the nematodes of the family Capillariidae could not be determined due to the absence of adult individuals. However, these parasites were recorded in , with Amphibiocapillaria parasitizing turtles and lizards, Paracapillaria recorded in snakes and other poikilothermic vertebrates (amphibians and fish), and Paratrichosoma and Crocodylocapillaria exclusively found in crocodilians (Moravec & Spratt 1998). Gastrointestinal nematode infestations in are usually asymptomatic, but can occasionally be associated with diseases such as gastric ulcers and the lack of development of the young (Dujardinascaris sp.), as well as intestinal obstruction in high infestations (Zhao et al. 2015, Lopes 2016). The Capillaridae family can form zigzag skin pathways on the skin of hosts, damaging the quality of potential hides (Huchzermeyer 2003). Other nematodes in reptiles can present clinical signs such as lethargy, anorexia, wasting, anemia, diarrhea, intestinal obstruction and peritonitis (Machin 2015). In protozoa, we registered a prevalence of 31% for E. paraguayensis and 12.4% for E. caimani, as compared to previous studies that reported 19% for E. caimani, 12% for E. paraguayensis, and 64% with mixed infestation in 69 C. yacare in Paraguay (Aquino-Shuster & Duszynski 1989). Similar studies in Brazil in Melanosuchus niger registered a prevalence of 74% for E. paraguayensis (Viana et al. 2013). In C. latirostris a prevalence of 62.2% was reported for Eimeria sp. (Batista et al. 2011, Batista et al. 2012). Eimeria protozoans are specific parasites with a direct biological cycle, with adult carrier animals infesting other individuals (Bowman et al. 2004), as well as food contaminated with caiman feces (Batista et al. 2011). A high density of animals, especially overcrowding, enables the direct transmission of oocysts between caiman (Batista et al. 2012). In the present study, the caiman sampled were adults which would be the reservoirs for the transmission of Eimeria oocysts. The protozoans Eimerias sp., are more pathogenic in young caiman, causing death in high infestations, decreasing feeding activity, affecting reproduction, and becoming one of the main diseases of captive crocodiles. The clinical signs are generally observed in immunosuppressed young and adult animals in which diarrhea, dehydration and death can occur (Machin 2015, Zhao et al. 2015). A study on trematodes in Caiman crocodilus yacare in Brazil reported a prevalence of 26.5% to 68.7% in 64 caimans (Catto & Amato 1994) and another study reported a prevalence of 33.3% for the trematode Proterodiplostomum globulare in Caiman crocodilus crocodilus (Lopes 2016). These values are very high in comparison to our

48 Parasites of Caiman yacare Mollericona et al. (2021)

recorded prevalence (0.9%). This could be related to the presence of intermediate hosts that act in the transmission of parasites (Lopes 2016). The places where the least parasitic infestation has been recorded in Caiman crocodilus (Linneus 1758) are areas with little anthropogenic activity, as well as in captivity with adequate management conditions (Rojas et al. 2011). Trematodes in crocodiles do not generally cause disease, but could be associated with delays in growth rates (Zhao et al. 2015). The significant differences registered on parasitic prevalence separate into three groups: the pentastomid parasites A. platycephala, S. oxycephala; acanthocephalans P. rhopalorhynchus and protozoa E. caiman; and finally, the nematodes and the trematode. The acanthocephalans, nematodes, trematodes and pentastomids are parasite groups with a long coevolutionary history with crocodilians (Catto 1991). Most helminths use intermediate hosts that form part of the host’s diet and parasite infestation is related to feeding habits. Crocodilians are opportunistic predators that ingest the most abundant prey (Santos et al. 1996), and studies on C. yacare indicate that the diet is composed of aquatic insects, mollusks, crustaceans, fish and, to a lesser extent, birds, mammals and amphibians (Rodríguez 2006, CIPTA/WCS 2010). Between the most prevalent parasites in streams and lagoons are pentastomids and acanthocephalans, these parasites require intermediate hosts such as fish and micro crustaceans that are commonly part of the caiman diet. This may also be influenced by the non-migratory behavior of caimans (De la Quintana et al. 2020, Pouilly & Miranda in prep), as well as high caiman concentrations and high densities of intermediate hosts in remaining water bodies during the dry season which would promote greater parasite infestations (Catto 1991). The correspondence analysis shows that the composition of parasite communities is very similar in all habitats. However, Dujardinascaris sp. is especially associated with lagoons and the unidentified trematode is mostly associated with streams, which may be explained by the habitat requirements of their intermediate hosts. Dujardinascaris sp. is cosmopolitan in distribution and requires fish and amphibians as intermediate hosts, which are then consumed by crocodilians to complete their biological cycle (Goldberg et al. 1991, Lopes 2016). Similarly, trematode metacercariae are found in fish eaten by caiman (Catto 1991). Fish diversity in stream and lagoons varies, and specificity in the development of parasite immature stages might be expected. All parasites recorded in the present study are common to C. yacare except for the ixodid A. crassum which commonly parasitizes tortoises and turtles, such as Chelonoidis denticulata Linnaeus 1766, Kinosternon leucostomum Duméril & Duméril 1851, and Rhinoclemmys annulata Gray 1860 (Osorno 1939, Acevedo-Gutiérrez et al. 2020). Ixodids, such as Amblyomma sp., A. dissimile and A. rotundatum, are known to parasitize lizards (Almeida 2006, Tellez 2013, Nava et al. 2017). In the present study we unusually recorded A. crassum in a female, possibly as an accidental relation between parasite-host related to the terrestrial movements of C. yacare that would cause a greater exposure of caimans to ticks (Acosta et al. 2019). The nesting season of C. yacare (August-November) coincides with the harvesting season, and females are found in vegetation bordering water bodies,

49 Parasites of Caiman yacare Mollericona et al. (2021)

which would facilitate parasitism (Rodríguez 2006), however, further studies are required to understand the ixodid-host association. Records of ixodids that parasitize crocodilians include A. dissimile, A. rotundatum, and Amblyomma sp. (Guglielmone & Nava 2010, Morais et al. 2010, Tellez 2013, Charruau et al. 2016, Acosta et al. 2019). As obligate blood-suckers, ixodids constitute reservoirs for pathogens such as fungi, bacteria, viruses, rickettsia and protozoans that can be transmitted between wild reptiles (Charruau et al. 2016, Rodríguez et al. 2019). Ixodids do not usually feed on caimans in natural conditions (Huchzermeyer 2003, Acosta et al. 2019), which could limit pathogen transmission. In conclusion, we registered nine endoparasite species and one species of ectoparasite in C. yacare harvested in the Tacana Indigenous Territory in Bolivia, which are common to the parasitic fauna of caiman documented in previous studies. The pentastomids Polyacanthorhynchus and protozoans were the most prevalent parasites, with significant differences observed between streams and lagoons. Dujardinascaris sp. shows a close association with lagoons, and the unidentified trematode with streams. The results may be related to the consumption of intermediate hosts such as fish and micro-crustaceans that are part of the caiman diet, along with the non-migratory behavior of the caiman, facilitating a close relationship of the parasites with the host. The presence of endoparasites identified in the lungs and intestines of caimans suggests a close relationship between the fish that constitute their food and act as intermediate hosts for parasites and facilitate transmission in caiman. There is still no information about whether the registered parasites could affect human health, although the parasite Sebekia sp. has caused human dermatitis. The identified endoparasites were located only in the lungs and digestive tract, and not in the muscle tissue used by the indigenous communities of the Tacana Indigenous Territory. Due to human consumption of meat, complementary studies should be designed to allow us to understand the relationship between host parasites and whether they could have zoonotic relevance. However, no endoparasites have been recorded in meat destined for human consumption, underlining its potential as an alternative source of protein for indigenous communities, as well as for the population in general. The sustainable management of this resource benefits the conservation of the species and its habitat.

SUPPLEMENTARY MATERIAL

Supplementary Table 1. List of parasites reported in Caiman yacare in South America.

ACKNOWLEDGMENTS

The diagnostic work was funded by Wildlife Conservation Society within the framework of the Great Madidi-Tambopata Landscape Conservation Program.

50 Parasites of Caiman yacare Mollericona et al. (2021)

We thank the Matusha Aidha Caiman Managers Association and the Cachichira community of the Tacana Indigenous Territory for their support during fieldwork. We are grateful to Mr. Eduardo Cavina Cartagena for his collaboration in all sampling procedures. We also thank Alberto A. Guglielmone for his support in the identification of the parasites.

REFERENCES

Acevedo-Gutiérrez l.Y., Paternina I.E. Pérez-Pérez J.C. Londoño A.F., López G., Rodas J.D. 2020. Garrapatas duras (Acari: Ixodidae) de Colombia, una revisión a su conocimiento en el país. Acta Biológica Colombiana, 25: 126-139. Acosta I.C.L., Martins T.F., Nóbrega Y.C., Mantovani T.C., Silva-Soares T., Santos M.R.D., Tadokoro C.E., Labruna M.B. 2019. First record of Amblyomma rotundatum Koch, 1844 (Acari: Ixodidae) parasitizing wild Caiman latirostris (Reptilia: Crocodylidae) in the Atlantic rainforest biome, Southeastern Brazil. Herpetology Notes, 12: 9-11. Almeida R.S. 2006. Trypanosoma sp. (Protozoa: Kinetoplastida) em Caiman yacare (: Alligatoridae), no de Mato Grosso do Sul –Região Miranda Abobral. Tese (Mestre) Pós Graduação em Ecologia e Conservação da Universidade Federal de Mato Grosso do Sul, Campo Grande, Brasil, 48 p. Alvarez G., Miranda G., Lara K., Cavinas K., Cartagena R., Wallace R. 2018. Experiencia de aprovechamiento y comercialización de carne de Caiman yacare en la TCO Tacana I. I Congreso Boliviano de Herpetología, La Paz –Bolivia. 2018. Amin O.M., Heckmann R.A., Inchausty V., Vasquez R. 1996. Immature Polyacanthorhynchus rhopalorhynchus (: Polyacanthorhynchidae) in Venton, Hoplias malabaricus (Pisces) from Moca Vie River, Bolivia, with Notes on its Apical Organ and Histopathology. Journal of The Helminthological Society of Washington, 63: 115-119. Aparicio J., Rios J.N. 2005. Los planes de manejo comunitario: una nueva iniciativa para el aprovechamiento del lagarto (Caiman yacare) en el norte del departamento de La Paz, Bolivia. Memorias: Manejo de Fauna Silvestre en Amazonia y Latinoamérica. 1-10. Aquino-Shuster A.L., Duszynski D.W. 1989.Coccidian parasites (Apicomplexa: Eimeriidae) from two species of caimans, Caiman yacare Daudin and Caiman latirostris Daudin (Alligatoridae), from Paraguay. The Journal of Parasitology, 75: 348-352. Ávila R.W. 2009. Padrões de infecção por helmintos em comunidades de lagartos do Brasil Central. Tese (Doutor) Institutp de Biocências, Cãmpus de Botucatu, UNESP, Universidade Estadual Paulista “Júlio de Mesquita Filoh” Campus de Botucatu, Brasil, 220 p. Ávila R.W., Da Silva R.J. 2013. Helminths of lizards from municipality of Aripuanã, in the southern Amazon region of Brazil. Journal of Helminthology, 87: 12-16. Batista A.M.B., Da Costa Pereira M.A.V., Vita G.F., Barros S.C.W., Barbosa C.G. 2011. Diagnóstico coproparasitológico de jacarés (Caiman latirostris Daudin, 1802) criados comercialmente no Estado do Rio de Janeiro. ARS Veterinaria, Jaboticabal, SP, 27: 102-110. Batista A.M.B., Da Costa Pereira M.A.V., Vita G.F., Barbosa C.G., Silva Antonio I.M., Barros S.C.W., Magalhȃes A.R., Freitas J.P. 2012. Levantamento qualitativo de generos de parasitos em amostras fecais de jacarés criados comercialmente em sistema fechado no estado do Rio de Janeiro. Pesquisa Veterinária Brasileira, 32: 1045-1049. 51 Parasites of Caiman yacare Mollericona et al. (2021)

Bowman D.D., Lynn R.C., Eberhard M.L. 2004. Georgis Parasitología para Veterinarios. S.L. Elsevier. Madrid, España. 440 p. Brito S.V., Almeida W.O., Anjos L.A., Silva R.J. 2012. New host records of Brazilian pentastomid species. Brazilian Journal of Biology, 72: 393-396. Cardoso A.M.C., Souza A.J.S., Menezes R.C., Pereira W.L.A., Tortelly R. 2014. Pulmonary lesions associated with parasitism by Sebekia oxycephala (Pentastomida) in free-ranging black caimans (Melanosuchus niger Spix, 1825) from the Brazilian Amazon. Pesquisa Veterinaria Brasileira, 34: 1002-1006. Castro O., Venzal J.M., Felix M.L. 2014. Registro de larva de Leiperia gracilis (Pentastomida, Sebekidae) en un dorado, Salminus brasiliensis (Characidae), en el río Uruguay. Boletín de la Sociedad Zoológica del Uruguay, 23: 30-35. Catto J.B. 1991. Taxonomia e ecología dos helmintos parasitos de Caiman crocodilus yacare (Crocodylia: Alligatoridae) no Pantanal Mato-Grossense.Tese (doutor) Instituto de Biologia Departamento de Biologia , Universidade Federal Rural Do Rio de Janeiro, Rio de Janeiro, Brasil, 169 p. Catto J.B. 2000. Endoparasitos de animais domésticos e silvestres do Pantanal: Helmintos, Acantocéfalos, Pentastomídeos e Protozoários. In: III Simpósio sobre Recursos Naturais e Socioeconômicos do Pantanal os Desafios do Novo Milênio, Corumbá, 2000. p. 1-17. Catto J.B., Amato F.R. 1994. Helminth community structure of the caiman, Caiman crocodilus yacare (Crocodylia, Alligatoridae) in the Brazilian “Pantanal”. Revista Brasileira de Parasitologia Veterinária, 3: 109-118. Catto J.B., Amato J.F.R. 1994. Proterodiplostome parasites (Digenea, Proterodiplostomidae) of the caiman, Caiman crocodilus yacare (Reptilia, Crocodylia) in the Pantanal Mato- Grossense, Brazil, with the description of two new species. Memorias Instituto Oswaldo Cruz, 89: 539-551. CIPTA/WCS. 2010. Manejo del lagarto por el pueblo Takana. La Paz-Bolivia, 28 p. CIPTA/WCS. 2010. La pesca en el territorio Takana. La Paz-Bolivia, 62 p. Cortez C. 2009. Reptiles Pp. 232. En: Ministerio de Medio Ambiente y Agua 2009. Libro Rojo de la Fauna Silvestre de Vertebrados de Bolivia. La Paz, Bolivia. Charruau P., Pérez-Flores J., Cedeño-Vásquez J.R., Gonzales-Solis D., Gonzáles-Desales G.A., Monroy-Vilchis O., Desales-Lara M.A. 2016. Occurrence of Amblyomma dissimile on wild crocodilians in southern Mexico. Diseases of Aquatic Organisms, 121: 167-171. De la Quintana P., Aparicio J., Pacheco L.F. 2020. Home range and habitat use of two sympatric crocodylians (Melanosuchus niger and Caiman yacare) under changing habitat conditions. Amphibia-Reptilia: 1-9. Fernández L., Moleón M.S., Poletta G., Siroski P. 2016. Presencia de pentastómidos (Sebekia sp.) en yacare negro (Caiman yacare) en la provincia de Corrientes, Argentina. En: IV Jornada de Difusión de la Investigación y Extensión, Santa Fe-Argentina, 2016. P. 1-2. Garcia V., Rojas D. 2014. Aprovechameinto de la carne de lagarto (Caiman yacare) en el departamento del Beni, Bolivia. Instituto Nacional de Innovación Agropecuaria y Forestal- INIAF, 1-8. Goldberg S.R., Bursey C.R., Aquino-Shuster A.L. 1991. Gastric nematodes of the Paraguayan caiman, Caiman yacare (Alligatoridae). The Journal of Parasitology, 77: 1009-1011. Guglielmone A.A., Nava S. 2010. Hosts of Amblyomma dissimile Koch, 1844 and Amblyomma rotundatum Koch, 1844 (Acari: Ixodidae). Zootaxa 0000, 1-23.

52 Parasites of Caiman yacare Mollericona et al. (2021)

Huchzermeyer F. 2003. Crocodiles – husbandry and diseases, CABI Publishing, Cambridge. 352 p. Junker K., Boomker J., Bolton L. 1999. Pentastomid infections in Nile crocodiles (Crocodylus niloticus) in the Kruger National Park, South Africa, with a description of the males of Alofia simpsoni. Onderstepoort Journal of Veterinary Research, 66: 65-71. Junker K. 2002. A study on the Pentastomida parasitising crocodilian and chelonian final host, with special emphasis on the South African pentastome fauna. Thesis (doctoral) Department of Ecology Parasitology at the University of Karlsruhe, Baden-Wurtemberg, 212 p. Junker K., Boomker J. 2006. A check-list of the pentastomid parasites of crocodilians and freshwater chelonians. Onderstepoort Journal of Veterinary Research, 73: 27-36. Lopes M.C. 2016. Helmintos gastrointestinais de jacarés Caiman crocodilus crocodilus Linnaeus, 1758 provenientes da Amazonia Brasileira. Tese (Doutora)- Programa de Pós- Graduação em Ciência Animal Tropical da Universidade Federal do Tocantins Araguaína To, Tocantins, 69 p. Llobet A. 2002. Programa de conservación y aprovechamiento sostenible del lagarto (Caiman yacare) en Bolivia. Taller internacional Sobre Regulación, Manejo y Comercio de Caiman yacare. 3 al 5 de octubre de 2002. Gainesvile, USA, 1-12. Machin R.A. 2015. Common gastrointestinal parasites in reptiles. In Practice, 37: 469-475. Mairena H., Solano M., Venegas, W. 1989. Human dermatitis caused by a nymph of Sebekia. American Journal of Tropical Medicine and Hygiene, 41: 352-354. Miranda-Chumacero G., Estívariz A., Wallace R., Fessy A., Quenevo C. 2010. Resultados de la primera cosecha manejada de Caiman yacare en la TCO Takana (Norte de Bolivia): Implicaciones para la sostenibilidad y regulaciones del manejo. Revista Boliviana de Ecología y Conservación Ambiental, 28: 131-144. Miranda G. 2020. El manejo de una gran especie por un gran pueblo. La experiencia de manejo del lagarto por el Pueblo Indígena Tacana. WCS – CIPTA – Matusha Aidha, 2020. Disponible en: http://arcg.is/1Hyz8j0. accessed 07/10/2020. Mollericona J.L., Limachi R. 2011. Informe técnico de laboratorio: Estudio de endoparásitos en especies silvestres cazados para subsistencia en el departamento de La Paz, Beni- Bolivia, 59 p. Mollericona J.L., Álvarez G., Miranda G. 2018. Estudio de parásitos en Caiman yacare en la cuenca del río Beni. In: I CONGRESO DE HERPETOLOGÍA, La Paz, Bolivia, p. 1-19. Morais D.H., Strussmann C., de Carvalho V.T., Kawashita-Ribeiro R.A. 2010. First record of Amblyomma rotundatum Koch, 1844 (Acari: Ixodidae) parasitizing palpebrosus Cuvier, 1807 (Reptilia: Crocodylidae), in the western border of Pantanal, Mato Grosso de Sul, Brazil. Herpetology Notes, 3: 133-134. Moreira L.H.A., Takemoto R.M., Pagotto J.P.A., Pavanelli G.C. 2014. Endoparasites community structure of three fish species in tributary streams of the river Pirapó, Paraná state, Brazil. Neotropical Helminthology, 8: 97-109. Moravec F., Spratt D. 1998. Crocodylocapillaria longiovata n. gen., n sp. (Nematoda: Capillariidae) from the stomach of crocodiles in Australia and New Guinea. The Journal of Parasitology, 84: 426-430. Nácar-Muñoz J., León-Regagnon V., Cifuentes-Lemus J.L., Hernández-Hurtado H., Hernández- Hurtado P., Chávez-Dagostino R.M. 2016. Dujardinascaris helicina (Nematoda: Ascarididae)

53 Parasites of Caiman yacare Mollericona et al. (2021)

parásito de Crocodylus acutus (Reptilia: Crocodylidae) en Puerto Vallarta, Jalisco, México. Revista Mexicana de Biodiversidad, 87: 1010-1014. Nava S., Venzal J.M., Gonzáles-Acuña D., Martins T.F., Guglielmone A. 2017. A. Ticks of the Southern Cone of America: Diagnosis, Distribution, and Hosts with , Ecology and Sanitary Importance. London: United Kingdom, Elsevier, 374 p. Nuñez V., Drago F. 2017. Acanthocephala. p. 112-127. En: Drago F.B. Macroparásitos Diversidad y Biología. Editorial de la Universidad de La Plata, Buenos Aires, Argentina. Osorno M.E. 1939. Las Garrapatas de la República de Colombia. Comunicación de la Academia Nacional de Medicina, 57-103. Pacheco L.F. 1996. Plan de acción de los caimanes de Bolivia. Ecología en Bolivia, 27: 43-53. Rivera S.J., Pacheco L.F., Achá D., Molina C.I., Miranda-Chumacero G. 2016. Low total mercury in Caiman yacare (Alligatoridae) as compared to carnivorous, and non-carnivorous fish consumed by Amazonian indigenous communities. Environmental Pollution, 1-6. Robinson L.E. 1926. Ticks A monograph of the Ixodoidea. Part, IV The Genus Amblyomma. Cambridge at The University Press, 342 p. Rodríguez V. 2006. Información de mercado para los subproductos del lagarto (Caiman yacare). Información para la comercialización de recursos de la biodiversidad en el Territorio Indígena y Parque Nacional Isiboro-Sécure (TIPNIS). Proyecto: MAPZA-GTZ-GFA- SERNAP. La Paz-Bolivia, 183 p. Rodríguez E.V., Mollericona J.L., Nallar R. 2019. Garrapatas del género Amblyomma (Acari: Ixodidae) parasitando a tayasuidos silvestres (Tayassu pecari y Pecari tajacu) en la Reserva de la Biósfera Pilón Lajas, Beni-Bolivia. Ecología en Bolivia, 54: 98-108. Rojas G., Alvis R., Pino J., Shiga B. 2011. Presencia de Hepatozoon caimani (Apicomplexa: Hepatozoidae) en el “caiman blanco” Caiman crocodilus (Linneus 1758) en un zoológico de Lima, Perú. Revista de Investigaciones Veterinarias del Perú, 22: 56-60. Rueda-Almonacid J.V., Carr J.L., Mittermeier R.A., Rodríguez-Mahecha J.V., Mast R.B., Vogt R.C., Rhodin A.G.J., de la Ossa-Velásquez J., Rueda J.N., Mittermeier C.G. 2007. Las tortugas y los cocodrilianos de los países andinos del trópico. Serie de guías tropicales de campo N°6. Conservación Internacional. Editorial Panamericana, Formas e Impresos. Bogotá, Colombia. 538 pp. Santana H.P., Morey G.M., Lima J.P., Malta J.C. 2017. Influencia de metazoários parasitas na norte de juvenis de Arapaima gigas (Schinz, 1822) criados em uma piscicultura na Amazonia Brasileira. Revista Brasileira de Zoociencias, 18: 77-90. Santos S.A., Nogueira M.S., Pinheiro M.S., Campos Z., Magnusson W.E., Mourao G.M. 1996. Diets of Caiman crocodilus yacare from different habitats in the Brazilian Pantanal. Herpetological Journal, 6: 111-117. Sarmiento J., Bigorne R., Carvajal-Vallejos F.M., Mladonado M., Leclak E., Oberdorff T. 2014. Peces de Bolivia / Bolivian Fishes. IRD-BioFresh (EU), Plural editores, Bolivia, 211 p. Self J.T., Rego A.A. 1985. Reassessments and revisions of certain genera and species of the family Sebekidae (Pentastomida) including description of Sebekia microhamus n.sp. Systematic Parasitology, 7: 33-41. Silva L.A.F., Morais D.H., Aguilar A., Almeida W.O., Silva R.J. 2015. First record of Sebekia oxycephala (Pentastomida: Sebekidae) infecting Helicops infrataeniatus (Reptilia: Colubridae), São Paulo State, Brazil. Brazilian Journal of Biology, 75: 497-498. Tantaleán M. 2010. Manual de diagnóstico parasitológico en animales silvestres. Brigada Fauna Silvestre, Animal Place Perú, Instituto Peruano de la Biodiversidad, Lima, Perú. 29 p. 54 Parasites of Caiman yacare Mollericona et al. (2021)

Travassos L. 1933. Sobre os filarideos dos crocodillos sul-americanos. Memorias do Instituto Oswaldo Cruz, 27: 159-167. Tellez M. 2013. A checklist of host-parasite interaction of the order Crocodylia. Press Berkeley Los Angeles London, 390 p. Troiano J.C., Martínez F., Bravo-Ferrer M.T. 1996. Alofia platycephala; pentastomid word in lung of Caiman crocodylus yacare. In: Proceedings of the 13th Working Meeting of the Crocodiles Specialist Group-IUCN-The World Conservation Unión, Gland, Switzerland p. 337-341. Viana L.A., Paiva F., Coutinho M.E., Lourenço De Oliveira R. 2010. Hepaozoon caimani (Apicomplexa: Hepatozoidae) in wild caiman, Caiman yacare, from The Pantanal Region, Brazil. The Journal of Parasitology, 96: 83-88. Viana L.A., Motta A.G., Coutinho M.E., Rocha C.F.D. 2013. Eimeria spp. (Apicomplexa: Eimeriidae) in black caiman Melanosuchus niger (Crocodilia: Alligatoridae) from the Amazon Region, Brazil, with a description of two new coccidian species. Acta Protozoologica, 52: 283-289. Vicente J.J., Rodrigues H.O., Gomes D.C., Pinto R.M. 1993. Nematóides do Brasil. Parte III: Nematóides de Répteis. Revista Brasileira de Zoologia, 10: 19-168. Vicentin W. 2009. Composição e estrutura das infracomunidades de metazoários endoparásitos de Pygocentrus nattereri kner, 1858 e Serrasalmus marginatus Valenciennes, 1837 (Characiformes - Serrasalminae), espécies simpátricas no rio Negro, Pantanal, Brasil. Tese (Mestre) Programa de Pós-Graduacao em Ecologia e Conservação, Universidade Federal de Mato Grosso de Sul, Campo Grande. 89 p. Viera F.M. 2011. Helmintos parasitos de mamíferos carnívoros silvestres no municipio de Juiz de Fora, Zona da Mata do Estado de Minas Gerais, Brasil. Tese doutorado em Biologia Animal, Universidad Federal Rural do Rio de Janeiro, Rio de Janeiro. 86 p. Voltzit O.V. 2007. A review of neotropical Amblyomma species (Acari: Ixodidae). Acarina, 15: 3-134. Zhao J., Zhou Y., Wang S., Tu G., Tang X., Wu X. 2015. Preliminary report on the intestinal parasites and their diversity in captive Chinese . Nutrición Hospitalaria, 31: 813- 819.

55 Parasites of Caiman yacare Mollericona et al. (2021)

a) b) c)

FIGURE 4. a) Alofia platycephala female anterior extreme, U-shaped oral cavity; b) A. platycephala male anterior extreme; c) Sebekia oxycephala female anterior extreme, ring buccal cavity.

a) b)

FIGURE 5. a) Polyacanthorynchus rhopalorhynchus female anterior extreme; b) Micropleura vazi female anterior extreme.

56 Parasites of Caiman yacare Mollericona et al. (2021)

a) b)

c)

FIGURE 6. a) Amblyomma crassum female dorsal view; b) female ventral view; c) female observing the upper spur on the coxa II.

57 Parasites of Caiman yacare Mollericona et al. (2021)

FIGURE 7. Eggs and oocysts of parasites in Caiman a) b) yacare: a) Capillariidae, b) Dujardinascaris sp., c) Polyacanthorhynchus rhopalorhynchus, d) Trematode, e) Eimeria paraguayensis, f) E. caimani.

c) d)

e) f)

58 Parasites of Caiman yacare Mollericona et al. (2021)

SUPPLEMENTARY TABLE 1. List of parasites reported in Caiman yacare in South America.

Parasite species Location/Tissue Countries Bibliographic reference Digenea

Stephanoprora jacarentinga Freitas & Lent 1938 Intestine Brazil (Catto 2000) Caimanicola marajoara Teixeira de Freitas & Lent Intestine Brazil (Catto & Amato 1994, Catto 2000) 1938 Proctocaecum dorsale Catto & Amato 1993 Intestine Brazil (Catto & Amato 1994, Catto 2000) Pachypsolus sclerops Travassos 1922 Intestine Brazil (Catto 2000) Pseudotelorchis caimanis Catto & Amato 1993 Intestine Brazil (Catto & Amato 1994, Catto 2000) Pseudotelorchis yacare Catto & Amato 1993 Intestine Brazil (Catto & Amato 1994, Catto 2000) Odhneriotrema microcephala Travassos 1922 Stomach Brazil (Catto 2000) Cyathocotyle brasiliensis Ruiz & Leao 1945 Intestine Brazil (Catto 2000) Cystodiplostomum hollyi Dubois 1936 Intestine Brazil (Catto & Amato 1994, Catto 2000) Herpetodiplostomum caimancola Dollfus 1935 Intestine Brazil (Catto & Amato 1994, Catto 2000) Paradiplostomum abbreviatum Brandes 1888 Intestine Brazil (Catto & Amato 1994, Catto 2000) Prolecithodiplostomum constrictum Dubois 1936 Intestine Brazil (Catto & Amato 1994, Catto 2000) Proterodiplostomum breve Catto & Amato 1994 Intestine Brazil (Catto & Amato 1994, Catto 2000) Proterodiplostomum globulare Catto & Amato 1994 Intestine Brazil (Catto & Amato 1994, Catto 2000) Proterodiplostomum longum Brandes 1888 Intestine Peru (Dubois 1988, Tellez et al. 2013) Proterodiplostomum medusae Dubois 1936 Intestine Brazil (Catto & Amato 1994, Catto 2000) Proterodiplostomum tumidulum Dubois 1936 Intestine Brazil (Catto & Amato 1994, Catto 2000) Nematoda Eustrongylides sp. Jagerskiold 1909 Stomach Paraguay (Goldberg et al. 1991) Paratrichosoma sp. Ashford & Muller 1978 Abdominal cavity Brazil (Catto & Amato 1994) Contracaecum sp. Railliet & Henry 1912 Stomach Paraguay (Goldberg et al. 1991) Brazil, Brevimulticaecum baylisi Travassos 1933 Stomach (Goldberg et al. 1991, Catto & Amato 1994) Paraguay Brazil, Brevimulticaecum stekhoveni Baylis 1947 Stomach (Goldberg et al. 1991, Catto & Amato 1994) Paraguay Dujardinascaris chabaudi Diaz-Ungria & Gallardo Stomach Brazil (Catto & Amato 1994, Catto 2000) 1968 Dujardinascaris longispiculas Travassos 1933 Stomach Brazil (Travassos 1933, Catto 2000) Brazil, Dujardinascaris paulista Travassos 1933 Intestine-Stomach (Goldberg et al. 1991, Catto & Amato 1994) Paraguay

59 Parasites of Caiman yacare Mollericona et al. (2021)

Brazil, Ortleppascaris alata Baylis 1947 Stomach (Goldberg et al. 1991, Catto & Amato 1994) Paraguay Brazil, Micropleura vazi Travassos 1933 Abdominal cavity (Goldberg et al. 1991, Catto & Amato 1994) Paraguay Acanthocephala Polyacanthorhynchus rhopalorhynchus Diesing Intestine Brazil (Goldberg et al. 1991, Catto & Amato 1994) 1850 Pentastomida

Argentina, (Troiano et al. 1996, Junker & Boomker Alofia platycephala Lorhman 1889 Lungs Brazil 2006) Leipeira gracilis Diesing 1835 Windpipe Brazil (Catto 2000) Sebekia oxycephala Diesing 1835 Lungs Brazil (Catto 2000) Apicomplexa Brazil, (Aquino-Shuster & Duszynski, 1989, Hu- Eimeria caimani Aquino-Shuster & Duszynski 1989 Intestine Paraguay chzermeyer 2003, Viana & Marques 2005) Eimeria paraguayensis Aquino-Shuster & Duszynski Brazil, (Aquino-Shuster & Duszynski 1989, Hu- Intestine 1989 Paraguay chzermeyer 2003, Viana & Marques 2005) Hepatozoon caimani Carini 1909 Blood Brazil (Lainson et al. 2003, Viana et al. 2010) (Nunes & Ochiro 1990, Viana & Marques Trypanosoma sp. Gruby 1843 Blood Brazil 2005) Arthropoda Amblyomma sp. Koch 1837 Skin Brazil (Viana & Marques 2005) Amblyomma rotundotum Koch 1844 Skin Brazil (Almeida 2006) Amblyomma dissimile Koch 1884 Skin Brazil (Nava et al. 2017) Neoptera Culex fatigans Wiedmann 1828 Skin Brazil (Lainson et al. 2003) Annelida Placobdella sp. Blanchard 1893 Skin Brazil (Almeida 2006)

60