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Bol. Mus. Nac. Hist. Nat. Parag. Vol. 24, nº 1 (Jul. 2020): 5-14100-100

Diversity of and recorded with camera-traps in the Paraguayan Humid Chaco

Diversidad de mamíferos y aves registrados con cámaras trampa en el Chaco Húmedo Paraguayo

Andrea Caballero-Gini1,2,4, Diego Bueno-Villafañe1,2, Rafaela Laino1 & Karim Musálem1,3

1 Fundación Manuel Gondra, San José 365, Asunción, . 2 Instituto de Investigación Biológica del Paraguay, Del Escudo 1607, Asunción, Paraguay. 3 WWF. Bernardino Caballero 191, Asunción, Paraguay. 4Corresponding author. Email: [email protected]

Abstract.- Despite its vast extension and the rich fauna that it hosts, the Paraguayan Humid Chaco is one of the least studied in the country. In this study, we provide a list of birds and medium-sized and large mammals recorded with camera traps in Estancia Playada, a private property located south of Occidental region in the Humid Chaco of Paraguay. The survey was carried out from November 2016 to April 2017 with a total effort of 485 camera-days. We recorded 15 and 20 , among them the bare-faced curassow (Crax fasciolata), the (Myrmecophaga tridactyla), and the neotropical ( longicaudis); species that are globally threatened in different dregrees. Our results suggest that Estancia Playada is a site with the potential for the conservation of birds and mammals in the Humid Chaco of Paraguay. Keywords: Species inventory, Mammals, Birds, Cerrito, Presidente Hayes.

Resumen.- A pesar de su vasta extensión y la rica fauna que alberga, el Chaco Húmedo es una de las ecorregiones menos estudiadas en el país. En este estudio proporcionamos una lista de aves y mamíferos registrados con cámaras trampa en la Estancia Playada, una propiedad privada ubicada al sur de la región Occidental en la ecorregión del Chaco Húmedo de Paraguay. Los muestreos se llevaron a cabo entre noviembre de 2016 y abril de 2017 con un esfuerzo total de 485 días-cámara. Registramos 15 especies de mamíferos y 20 de aves, entre ellas el muitú (Crax fasciolata), el oso hormiguero gigante (Myrme- cophaga tridactyla) y la nutria neotropical (Lontra longicaudis) que están globalmente amenazadas a diferentes grados. Nuestros resultados sugieren que la Estancia Playada es un sitio con potencial para la conservación de aves y mamíferos en el Chaco Húmedo de Paraguay. Palabras clave: Inventario de especies, Cerrito, Presidente Hayes.

The Humid Chaco extends in , Boli- forests to exotic pastures for cattle ranching via, , and Paraguay (Olson et al., 2001). expansion (Baumann et al., 2017). The region In Paraguay, this ecoregion covers almost 13% comprises rich biodiversity, including at least of the territory, following the course of the Pa- 60 amphibian species, 104 of reptiles, 392 of raguay River and extending towards the South- birds and 129 mammals (Brusquetti & Lavilla, West (Mereles et al., 2013). The vegetation is 2006; Cacciali et al., 2016; Guyra Paraguay, composed of a mosaic of sub-humid forests, 2004; Rumbo, 2010). palm groves, savannas and aquatic vegetation Given this high diversity, this ecoregion (Mereles et al., 2013), which creates many should be considered a priority area for conser- different natural communities and houses great vation. However, the number of protected areas biodiversity (Ginzburg & Adámoli, 2006). covers only ~ 5% of its surface (Mereles et al., This region is considered a large producer of 2013; Cacciali et al., 2015). In Paraguay, Key cattle, which drives the conversion of native Biodiversity Areas (KBAs) are identified under grasslands (frequently flooded savannas) and the criteria for Important Bird Areas (IBAs),

Recibido: 18.i.2019 Aceptado: 12.xi.2019 Publicado online: 16.iii.2020 1680-4031/© 2020 Museo Nacional de Historia Natural del Paraguay. Este es un artículo de acceso abierto bajo la licencia CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/). 6 Boletín del Museo Nacional de Historia Natural del Paraguay Vol. 24, Nº 1 (Julio 2020)

Figure 1. Location of Estancia Playada. Maps of and Paraguay highlighting the study site. The enlarged area is showing the position of the camera traps and vegetal formations at Estancia Playada. but these are poorly represented in the Humid lands and vegetation formations are condi- Chaco and do not imply legal protection (Guyra tioned by topography and frequent flooding Paraguay, 2008; Eken et al., 2004). (Ginzburg & Adámoli, 2006) creating a mo- Although the mammal and bird composition saic of forests, subtropical forests, grasslands of the Humid Chaco is well known, few studies and marshes (Mereles et al., 2013). Rainfall exclusively focus on this region and most of averages 1200 mm per year, and the average them constitute new records for single species. temperature ranges between 24-25° C (Me- To contribute to the knowledge and documenta- reles et al., 2013). tion of birds and mammals of the Humid Chaco Data collection. We used 5 Bushnell Tro- in Paraguay, we present the results of six-month phy Cam HD Essential camera traps for mam- monitoring using camera traps in Cerrito (Pre- mal and bird detection from November 2016 sidente Hayes). to April 2017. Camera traps were installed 45 cm above the ground in trails used by cattle Materials and methods and were programmed to operate 24 hs per Study area. We carried out fieldwork at Estan- day. In order to obtain more information on cia Playada (24°57'59.88"S 57°21'56.12"W) the different assemblies in the study area we in Cerrito, Municipality of Benjamín Aceval, rotated camera traps in three different vegeta- Presidente Hayes Department (Fig. 1). This tion covers (Fig. 1): i) Wetlands and associated 4,000-ha private property is located in the riparian forests (W-RF), 186 camera-days, floodplain of the and its main ii) Mesoxerophytic semi-deciduous forests activity is extensive free-range cattle ranching (MXF), 120 camera-days, and iii) Floodable in low density (one unit every 2 hecta- sub-humid forest islets (FSF), 176 camera res) (Merenciano-González et al. 2018). Here, days. no evidence of clearings was found in the last Wetlands are floodable low areas that 100 years (Laino et al. 2017), maintaining its vary with the rainy season; the vegetation original vegetation cover, except for selective presents emergents of Typha, Cyperus and extraction of wood used for cattle ranching Thalia; in open waters, floating species of infrastructure (cabin construction, fencing, Pistia, Eichornia, Victoria among others and bridges). appear (Peña-Chocarro et al. 2006). Wetlands Predominant ecosystems here are wet- presents a ~50-100 m riparian forest fringe

Andrea Caballero-Gini, Diego Bueno-Villafañe, Rafaela Laino & Karim Musálem Boletín del Museo Nacional de Historia Natural del Paraguay Vol. 24, Nº 1 (Julio 2020) 7 2 5 3 1 3 1 3 3 8 11 39 70 28 22 10 15 15 18 20 records records Number of Number Endangered; EN: • • • • • • • • • • • • • FSF Wetlands and associated Wetlands • • • • • • • • • • • • W-RF Habitat W-RF: • • • • • • • • • • • • MXF LC LC LC LC LC LC LC LC LC LC LC LC LC LC LC NT VU DD VU IUCN Common name White-eared Opossum Anteater Giant Tamandua Southern Armadillo Nine-banded Crab-eating American South Crab-eating Geoffroy's Collared Capybara Azara's Agouti Tapeti tinamou Tataupa Chaco Bare-faced curassow White-tipped dove Floodable sub-humid forest islets). Conservation Status follows UICN criteria. UICN follows Status Conservation islets). forest sub-humid Floodable FSF: (Linnaeus, 1766) Linnaeus, 1758 (Linnaeus, 1758) Linnaeus, 1758 (Linnaeus, 1758) (Fischer, 1814) (Fischer, Lund, 1840 d'Orbigny & Gervais, 1844) (Cuvier, 1798) (Cuvier, (Temminck, 1815) (Temminck, Bonaparte, 1855 (Olfers, 1818) Lichtenstein, 1823 Scientific name (Wagler, 1830) (Wagler, (Linnaeus, 1766) Spix, 1825 (Linnaeus, 1758) (Linnaeus, 1758) (Linnaeus, 1766) Didelphis albiventris Myrmecophaga tridactyla tetradactyla Tamandua Dasypus novemcinctus thous Cerdocyon nasua cancrivorus Lontra longicaudis Eira barbara ( geoffroyi Pecari tajacu Mazama gouazoubira hydrochaeris Hydrochoerus azarae Dasyprocta Sylvilagus brasiliensis tataupa Crypturellus Ortalis canicollis Crax fasciolata Leptotila verreauxi Vulnerable. Mesoxerophytic semi-deciduous forests, semi-deciduous Mesoxerophytic VU: Family MXF: Species of mammals and birds recorded at Estancia Playada (Cerrito, Paraguay) and the number of records per habitat. ( habitat. per records of number the and Paraguay) (Cerrito, Playada Estancia at recorded birds and mammals of Species Didelphidae Myrmecophagidae Dasypodidae Tayassuidae Cervidae Caviidae Dasyproctidae Leporidae Tinamidae Columbidae Least Concern; Class Table 1 (start). Table forests, riparian LC: Mammalia Aves

Diversity of mammals and birds recorded with camera-traps in the Paraguayan Humid Chaco 8 Boletín del Museo Nacional de Historia Natural del Paraguay Vol. 24, Nº 1 (Julio 2020) 5 5 9 8 2 1 1 1 1 3 1 6 2 1 9 1 3 29 records records Number of Number Endangered; EN: • • • • • • • • • FSF Wetlands and associated Wetlands • • • • • • • • • • • W-RF Habitat W-RF: • • • • MXF LC LC LC LC LC LC LC LC LC LC LC LC LC LC LC LC LC LC IUCN Common name Greater ani Limpkin Giant wood- Grey-necked wood-rail Rufescent -heron Cocoi heron American black vulture Roadside hawk Spectacled owl toucan Toco Red-legged seriema Rufous Plush-crested Purplish Jay Rufous-bellied thrush Thrush Creamy-bellied Red-rumped cacique Golden-winged cacique Floodable sub-humid forest islets). Conservation Status follows UICN criteria. UICN follows Status Conservation islets). forest sub-humid Floodable FSF: (Vieillot, 1818) (Vieillot, Cabanis, 1850 (Linnaeus, 1766) (Gmelin, 1788) (Latham, 1790) (Vieillot, 1818) (Vieillot, (Vigors, 1825) (Vigors, (Boddaert, 1783) (Müller, 1776) (Müller, Scientific name Gmelin, 1788 Vieillot, 1819 Vieillot, (Linnaeus, 1766) Vieillot, 1818 Vieillot, (Linnaeus, 1766) (Bechstein, 1783) Müller, 1776 Müller, (Gmelin, 1788) Linnaeus, 1766 Crotophaga major Crotophaga Aramus guarauna ypecaha Aramides cajaneus lineatum Tigrisoma cocoi Ardea Coragyps atratus Rupornis magnirostris Pulsatrix perspicillata Ramphastos toco Cariama cristata Furnarius rufus chrysops Cyanocorax cyanomelas rufiventris Turdus amaurochalinus Turdus Cacicus haemorrhous Cacicus chrysopterus Vulnerable. Mesoxerophytic semi-deciduous forests, semi-deciduous Mesoxerophytic VU: Family MXF: Species of mammals and birds recorded at Estancia Playada (Cerrito, Paraguay) and the number of records per habitat. ( habitat. per records of number the and Paraguay) (Cerrito, Playada Estancia at recorded birds and mammals of Species Cuculidae Aramidae Rallidae Ardeidae Cathartidae Accipitridae Strigidae Ramphastidae Cariamidae Furnariidae Turdidae Icteridae Least Concern; Class Table 1 (end). Table forests, riparian LC:

Andrea Caballero-Gini, Diego Bueno-Villafañe, Rafaela Laino & Karim Musálem Boletín del Museo Nacional de Historia Natural del Paraguay Vol. 24, Nº 1 (Julio 2020) 9

Figure 2. Some of the mammal species found in the camera trap sampling at Estancia Playada. a) Myrmecophaga tri- dactyla, b) Cerdocyon thous, c) Nasua nasua, d) Procyon cancrivorus, e) Lontra longicaudis, f) Leopardus geoffroyi, g) Pecari tajacu, h) Hydrochoerus hydrochaeris, i) Sylvilagus brasiliensis. linked to periods of flooding (Peña-Chocarro De Angelo et al. (2015) and birds following et al. 2006, Maturo et al. 2005). Mata et al. (2006), Narosky and Yzurieta Mesoxerophytic semi-deciduous forests (2006), Erize et al. (2006), and Ridgely & Tu- or quebrachales are dominated by Schinopsis dor (2009). We tagged the photographs using balansae, Cesalpinea paraguayensis, and oc- DigiKam (www.digikam.org) and extracted the casionally Aspidosperma quebracho-blanco metadata with R package camtrapR (Niedballa (Mereles et al. 2005, Peña-Chocarro et al. 2006). et al. 2016). We considered as independent Flooded sub-humid forests (FSF) are pre- each record of each species separated by 24 sent in the Paraguay River floodplain and are hours (Torres-Porras et al. 2017). The study associated with palm groves of Copernicia focuses on birds and medium and large-sized alba (Perez de Molas 2016). Some tree species mammals; thus, we did not include domestic of the sub-humid forest are shared with the and humans in our counts. We per- riparian forest; however, these occur in islets, formed the species rarefaction curves with R surrounded by savannas rather than following package iNEXT (Hsieh et al. 2016). the course of streams or wetlands. We identified the photographed species of Results mammals using Eisenberg and Redford (1992), With a sampling effort of 485 camera-days, we

Diversity of mammals and birds recorded with camera-traps in the Paraguayan Humid Chaco 10 Boletín del Museo Nacional de Historia Natural del Paraguay Vol. 24, Nº 1 (Julio 2020) obtained 391 records of 15 species of native formes with three, and and Pele- mammals and 20 birds (Table 1, Figs 2 and 3). caniformes with two species each. The highest We failed in identifying to species level a bat numbers of records were for Aramides ypecaha and a bird. This latter was using an (n=29), Leptotila verreauxi (n=20) and Crax abandoned furnariid’s nest of thorns located 20 fasciolata (n=18). Coragyps atratus, Rupornis meters away from the camera trap. magnirostris, Pulsatrix perspicillata, Ramphas- Among mammals, the order was tos toco, Furnarius rufus and Turdus rufiventris the richest with six species, followed by Pilosa, were only recorded once during the study. The Artiodactyla and Rodentia, with two species record of the spectacle owl (Pulsatrix perspici- each. The species with the highest number of llata) is the first confirmation for the species in records were Cerdocyon thous (n=70), Dasypus Presidente Hayes Department in the Low Chaco novemcinctus (n=39) and Nasua nasua (n=28). (Hayes, 1995; Guyra Paraguay, 2004). On the other hand, Leopardus geoffroyi, Lontra According to the rarefaction graph, none of longicaudis and Didelphis albiventris were only the curves reached its asymptote; this is more recorded once. noticeable in the case of birds and particularly birds were the best-represented in the wetland area (Fig. 4). order with seven species, followed by Grui-

Figure 3. Some of the bird species found in the camera trap sampling at Estancia Playada, a) Ortalis canicollis, b) Crax fasciolata, c) Aramus guarauna, d) Aramides ypecaha, e) Tigrisoma lineatum, f) Ardea cocoi, g) Coragyps atratus, h) Pulsatrix perspicillata, i) Cariama cristata.

Andrea Caballero-Gini, Diego Bueno-Villafañe, Rafaela Laino & Karim Musálem Boletín del Museo Nacional de Historia Natural del Paraguay Vol. 24, Nº 1 (Julio 2020) 11

Figure 4. Species rarefaction curves for: a) mammals and b) bird species for each site (W-RF: Wetlands and associated riparian forests, MXF: Mesoxerophytic semi-deciduous forests, FSF: Floodable sub-humid forest islets).

Discussion in low numbers probably due to the low sam- Diversity of medium and large-sized mammals pling effort dedicated to these habitats. found in this study represents 19% of the to- In regard of the conservation status, almost tal recorded in the Humid Chaco ecoregion all the species recorded are listed as Least Con- (Rumbo, 2010). Carnivora had the highest cern according to the IUCN, except for Myr- richness among the mammals recorded, being mecophaga tridactyla which is categorized as Cerdocyon thous the most frequently recorded Vulnerable, Lontra longicaudis as Near Threa- species and, found in all habitats studied; this tened and Dasyprocta azarae as Data Deficient. species is commonly associated to areas with The first two species are considered threatened combination of forest patches, savannas and despite having wide ranges of distribution, grasslands (Maffei et al., 2007) and show a because of local extinctions mainly due to the cathemeral activity according to Huck et al. degradation of their habitats and the pressure (2017). Nasua nasua and Procyon cancrivorus by hunting (Miranda et al., 2014; Rheingantz & were also recorded frequently and in all types Trinca, 2015). Recently, the conservation status of vegetation, the latter associated with puddles of mammals was evaluated at the national level and other water bodies (Redford & Eisenberg, and Myrmecophaga tridactyla was also cate- 1992). Another species with numerous records gorized as Vulnerable. Other modifications are was Dasypus novemcinctus, which was asso- that Lontra longicaudis is listed as LC, as well ciated with humid forest habitats, as mentioned as Dasyprocta azarae, and the species Sylvila- by Neris et al. (2002) and was observed mainly gus brasiliensis was not evaluated (Asociación during the night. Records of felids were low, Paraguaya de Mastozoología & Secretaría del and the only species was Leopardus geoffroyi, Ambiente, 2017). this may be due to the short period and size of A record that is worth mentioning, although our sampling, and to the fact that probably fe- it was not obtained with the camera traps, is lids are in low density in the area because of the that of the maned Crhysocyon brachyurus, presence of cattle and humans. Additionally, which was observed at night in an internal ve- traces of concolor were recently found hicular path. We consider that this species was in a pasture area in the study site by locals, and not recorded with the camera traps because it its presence was later confirmed by camera trap is usually associated with grasslands (Dietz, data obtained later than those analyzed in this 1985) and this type of habitat was not analyzed study. Species associated with wetlands and in this study. other water bodies such as Lontra longicaudis Birds recorded with camera traps in our and Hydrochoerus hydrochaeris were recorded study site represent only 5% of all species ci- ted for the Humid Chaco in Paraguay (Guyra

Diversity of mammals and birds recorded with camera-traps in the Paraguayan Humid Chaco 12 Boletín del Museo Nacional de Historia Natural del Paraguay Vol. 24, Nº 1 (Julio 2020)

Paraguay, 2004). Bird size and distance to the Humberto Sánchez, Arne Lesterhuis and, Rob camera affect the triggering; also, temperature Clay for their help in identifying some species and flock size have an impact with larger flocks and Marcela Ferrreira for her help in photo being captured more often (Randler & Kalb, processing. We thank the Programa Nacional de 2018). This study provides the first record of Incentivo a los Investigadores (PRONII) from Pulsatrix perspicillata for the Presidente Hayes CONACYT. Department, which was considered as hypothe- Literature tical for the Humid (Low) Chaco region by Asociación Paraguaya de Mastozoología and Hayes (1995). Another remarkable result of our Secretaría del Ambiente. (2017). Libro study was the detection in high numbers of the Rojo de los Mamíferos del Paraguay: species Crax fasciolata which is categorized as especies amenazadas de extinción. Vulnerable due to loss of forest cover mainly in Asunción, Paraguay: Editorial Creatio. the Amazon region and to other factors such as 137 pp. hunting and edge effect (Birdlife International Birdlife International. (2016). Crax fasciola- 2016). Solitary individuals and groups of up to ta. The IUCN Red List of Threatened 5 were detected in the subtropical forest and Species 2016. [Consulted: 23.x.2019]. riparian forest (Laino et al. 2018), as suggested . was registered more frequently during daylight Brusquetti, F. & Lavilla, E.O. (2006). Lista and near water bodies. comentada de los Anfibios de Paraguay. Most species in the present study have Cuadernos de Herpetología, 20(2): geographic ranges that include the Humid 3–79. Chaco ecoregion, but this study confirms its Cacciali, P., Cabral, H. & Yanosky, A. (2015). presence, and given that wildlife inventories for Conservation implications of protected this region are still scarce, our work provides areas’ coverage for Paraguay’s reptiles. essential information for the area. The diversity Parks, 21(2): 87–105. found at Estancia Playada suggests that it may Cacciali, P., Norman, J.S., Aquino Ortíz, A.L., play a key role in the preservation of wildlife Fitzgerald, L. & Smith, P. (2016). The in addition to be an area of connectivity to Reptiles of Paraguay: Literature, dis- the IBA Estancia Rafaela (IBA code PY022). tribution, and an annotated taxonomic Therefore, we consider imperative to carry out checklist. Special Publication of the conservation efforts promoting the establish- Museum of Southwestern Biology, 11: ment of protected areas, since these represent 1–373. slightly modified natural environments, and De Angelo, C., Paviolo, A., Di Blanco, Y. & are very threatened by the lack of a land-use Di Bitetti, M. (2008). Guía de huellas de planning policy. los mamíferos de Misiones y otras áreas del Subtrópico de Argentina. Tucumán, Acknowledgments Argentina: Ediciones del Subtrópico. We are grateful to IDEA WILD for providing 120 pp. the camera traps for this research. We thank the Dietz, J.M. (1985). Chrysocyon brachyurus. help received by the staff of Estancia Playada Mammalian Species, 234: 1–4. and the American Chaco Research Center, also Eken, G., Bennun, L., Brooks, T.M., Darwall, to Lía Romero, Marcela Ferreira, Silvina Cha- W., Fishpool, L.D.D., Foster, M., parro, and Paloma Moreno for their help in the Knox, D., Langhammer, P., Matiku, P., installation of the trap cameras. We also thank Radford, E., Salaman, P., Sechrest, W.,

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Andrea Caballero-Gini, Diego Bueno-Villafañe, Rafaela Laino & Karim Musálem