Primate Conservation 2021 (35)
Paraguayan Primatology: Past, Present and Future
Paul Smith1,2, Sergio D. Ríos3,4 and Rebecca L. Smith2,5
1FAUNA Paraguay, Encarnación, Itapúa, Paraguay 2Para La Tierra, Pilar, Ñeembucú, Paraguay 3Museo Nacional de Historia Natural del Paraguay, San Lorenzo, Paraguay 4Departamento de Arqueología y Paleontología, Secretaría Nacional de Cultura, Asunción, Paraguay 5School of Biological Sciences, University of Aberdeen, Scotland, UK
Abstract: With just five species, the Paraguayan primate fauna is less diverse than its neighbours and, perhaps as a result of this, few biologists have chosen the country for their primate studies. Consequently, the ecological data available for three of the five species that occur in the country is scant, and most of what we know about the other two is based on studies carried out in other countries. This paper collates specimen and literature data about this group to serve as a basis to encourage future research and to correct persistent errors and contradictions. Primate specimens in all the major Paraguayan collections and all significant specimens in international collections were examined. Specimen data were collated and supplemented with litera- ture and photographic data. Distribution data is provided according to a hierarchy of record reliability of examined specimens, specimens that we have not examined, literature records, photographic records and reliable sightings in the wild. Five species have been confirmed to be present in Paraguay, with an additional species (Callithrix jacchus) that is feral/introduced, and four species cited in the literature in error. Relevant discussion and distribution maps are provided for each species. The vast majority of primate specimens were collected at least 35 years ago, and the specimen record may no longer represent current distributions given the rapidly changing landscape in the country. We conclude that the available data on the distributions of Paraguayan primates are highly biased towards two species (Alouatta caraya and Sapajus cay), yet even these are poorly known, and despite most primatological studies to date being focused on the Chaco region (where diversity is greatest), we still lack basic occurrence data or an understanding of the ecological requirements and seasonal movements of most species. However, primatological research in Paraguay has experienced a renaissance in the past five years, and a brief rundown of projects that are currently underway is provided.
Key words: Alouatta caraya, Aotus azarae, Mico melanurus, Plecturocebus pallescens, Sapajus cay, distributions, taxonomy
Introduction Paraguayan primates. We also provide information on cur- rent primatological work being carried out in the country. The primate fauna of Paraguay is relatively poor in diversity with just five species in five families (Fig. 1), con- History of Paraguayan Primatology siderably less than neighboring Bolivia and Brazil, but the same as Argentina. All Paraguayan monkeys are catego- The first reports of Paraguayan primates were by San- rized as Least Concern on the IUCN Red List and are listed chez Labrador (1770) who observed the “dumb and ugly” in CITES Appendix II (Saldívar et al. 2017; Cartes et al. Carayáa (Alouatta caraya) and the “small” Caí (Sapajus 2018), although global conservation reassessments of most cay). Azara (1802) then provided detailed natural history species are well overdue. information and descriptions for three species: Carayá and The distribution, specimen record and bibliographical Caý as before, and the Miriquiná (Aotus azarae), with a history of the Paraguayan primates have yet to be prop- fourth species, the Tití (Callithrix jacchus) specifically erly clarified. We here review the specimens, literature excluded from the Paraguayan fauna. The same three spe- and reliable recent field records with a view to consolidat- cies were also described by Rengger (1830). The remain- ing the available data on the distribution and status of the ing two species were documented in the 20th Century.
1 Smith et al.
Figure 1. Map showing the political departments of Paraguay and the number of species of primates recorded in each. Departments as follows: Chaco region – Alto Paraguay (APY), Boquerón (BOQ), Presidente Hayes (PHA); Oriental region – Amambay (AMA), Alto Paraná (APA), Caaguazú (CAA), Canindeyú (CAN), Caazapá (CAZ), Central (CEN), Concepción (CON), Cordillera (COR), Guairá (GUA), Itapúa (ITA), Misiones (MIS), Ñeembucú (ÑEE), Paraguarí (PAR), San Pedro (SPE).
Callicebus pallescens Thomas, 1907, was newly described Mudry and Slavutsky 1987; Schneider et al. 1988; Sam- from Paraguayan specimens and the first record of the black- paio et al. 1991; Martinez et al. 2004; Casado et al. 2010), tailed marmoset Mico melanurus was documented by Stall- and an ethnographical focus (Hill et al. 1999, 2003; Cartes ings and Mittermeier (1983). 2007; Centrón et al. 2007), besides general reviews based Paraguayan primates were largely ignored by research- on previously published data (Rumiz and Stallings 1989; ers until the work of Jody Stallings in the 1980s (Stallings Gamarra de Fox and Martin 1996; Villalba and Yanosky 1983, 1984, 1985; Stallings et al. 1989). He provided the 2000; Esquivel 2001; Fariña and Hostettler 2003; Yahnke et first modern assessment of primate distributions in the coun- al. 2003; Vinke and Vinke 2008; Horton 2008; 2010; Porter try, and in the 1980s and 1990s Patricia Wright compared et al. 2013; Velázquez and Ramírez Pinto 2014). Lacking the behavior of Paraguayan and Peruvian night monkeys are longer-term field studies of wild populations, but a nota- (Wright 1983, 1989, 1994). Beyond this point, Paraguayan ble exception is the behavioral studies on wild Sapajus cay primate publications have consisted largely of occasional and urban Alouatta caraya led by Rebecca Smith (Smith and natural history notes (Clark 1983; Roguin 1986; Brooks et al. Briggs 2015; Smith 2017a, 2017b; Smith and Payne 2017; 1993; Brooks 1996; Ávila 2004, 2015; Campos et al. 2004; Smith et al. 2018; Kane and Smith 2020; Smith et al. 2020; Giordano and Ballard 2010; Cabral et al. 2017), papers with Wellian and Smith in press; Duffy et al. in press), which a biomedical focus (Rosner et al. 1984, 1988; Moreno and have contributed to the global knowledge of these species. Rosner 1999; Samudio et al. 1999; Diaz et al. 2007; Acosta The national conservation status of Paraguayan primates et al. 2016), a genetic focus (Mayatoshi et al. 1986, 1987; was recently reviewed by Cartes et al. (2017, 2018).
2 Paraguayan primatology
Materials and Methods The synonymy deals only with Paraguayan literature or literature citing Paraguayan specimens and is not intended to Specimens of primates from the major zoological col- be a complete list of synonyms for the species. lections in Paraguay were reviewed during 2017 to 2019. Local names: Local common names published in the Identifications were confirmed by inspection of the speci- Paraguayan literature are provided. We tried to reference mens, and locality data was collated from museum data- the earliest published usage for each name. bases and specimen labels. Specimens at national park Comments: Noteworthy or confusing themes in the Par- collections are also included, though these collections are aguayan literature. uncatalogued, unregistered and specimens are not labelled. There then follows a “hierarchical reliability” approach Data for these specimens were obtained, when possible by to the Paraguayan distribution of each species. This approach personal communication with the collectors and curators. is taken so as to not unduly bias understanding by depending The location of specimens in foreign museums was gleaned solely on the limited specimen record. The hierarchies are, from the literature and from Vert Net (which returned 164 in order of documented reliability: (1) examined specimen; results for “Paraguay Primates”). Specimens considered (2) specimen not examined; (3) record from published litera- to represent significant geographical range extensions were ture; (4) published photographic record; and (5) reliable field reviewed with the assistance of museum curators when fea- observation by one of the authors or knowledgeable local sible. Those that did not present noteworthy distributions observer. Records are presented with the political depart- were assumed to be correct and not examined. Maps were ment in bold capitals, followed by the details of the record made using Simplemappr (https://www.simplemappr.net/). (in alphabetical order). (Records from the capital Asunción Collection acronyms for museums housing Para- are included in Central department for geographic reasons, guayan primate specimens are as follows: AMNH Ameri- though officially it has an autonomous position.) For speci- can Museum of Natural History, New York; BMNH Brit- men records this involves the specimen number followed by ish Museum of Natural History, London; BZM Berliner the locality. These records are also mapped distinguishing Zoologisches Museums, Berlin; CBMI Colección Biológica the hierarchical categories so that readers may interpret their Museo de Itaipú, Hernandarias, Paraguay; CLO Macau- reliability for themselves. Published photographic records lay Library. Macaulay Library Audio and Video Collec- (category 4) and reliable field observations (category 5) tion; CONN University of Connecticut Museum of Natu- include only localities that are not covered by any one of the ral History, Storrs, CT; CZPLT Colección Zoológica Para previous three categories. La Tierra, Pilar, Paraguay; DEL Delaware Natural History The criteria for inclusion of literature records was that Museum, Wilmington, DE; MACN Museo Argentino de it was published in Paraguay or specifically deals with Para- Ciencia Naturales “Bernardino Rivadavia, Buenos Aires, guay or in the case of international publications that it makes Argentina; MCNM Museo de Ciencias Naturales de Madrid, specific reference to Paraguayan specimens or primary Spain; MLP Museo de La Plata, Argentina; MHNG Musee records. We omit a recent reference (Sequera et al. 2019) d´histoire Naturelle de Geneve, Switzerland; MNHNP dealing with primate epizootics in Paraguay as it is not Museo Nacional de Historia Natural del Paraguay, San entirely an original work, merely an adaptation of an exist- Lorenzo, Paraguay; PRC Pro Cosara museum based at the ing Brazilian manual, as stated by the editors. Every effort headquarters of the NGO Pro Cosara, Estancia Nueva Gam- was made to be thorough in this regard, though undoubtedly bach, Alto Verá, Paraguay; RBINS Royal Belgian Institute some references will have been missed. of Natural Sciences, Brussels, Belgium; SMNS Staatliches A statement on the ecological affinities of each species Museum für Naturkunde Stuttgart, Stuttgart, Germany; TTU in Paraguay is provided based on the ecoregions defined in Museum of Texas Tech University, Lubbock, TX; UMMZ Guyra Paraguay (2005) and Mereles (2013) (Fig. 2). These University of Michigan Museum of Zoology, Ann Arbor, can be broadly defined as follows: Atlantic Forest (subtropi- MI; USNM National Museum of Natural History, Smithso- cal humid forests of eastern Paraguay); Cerrado (central nian Institute, Washington, DC. South American tropical bush savanna of northern eastern Species accounts begin with the current common name, Paraguay); Dry Chaco (low, arid thorn forest and scrub of the scientific name and author, which are presented for each western Occidental region); Humid Chaco (palm savanna species in bold type following Mittermeier et al. (2013) and marshlands of the Paraguay River Basin; Pantanal (gal- and Rowe and Myers (2016). The original described name, lery forests and swamps of the north-eastern Chaco); Cer- author and type locality follow. There then follows a refer- rados del Chaco (an area of Cerrado in the northern Chaco enced list of the synonyms used in the Paraguayan literature contiguous with the Chiquitania of Bolivia) and Mesopota- with a (hopefully self-explanatory) single word descriptor mian Grasslands (flooded grasslands of the southern Orien- of the subject of the publication, as follows: behavior, bio- tal region). geography, conservation, diet, distribution, ecology, epide- miology, genetics, guide, habitat, list, mention, morphom- etry, parasitology, pharmacology, report, specimen/s, ssp. description, taxonomy, tracks, type description and use.
3 Smith et al.
Figure 2. Map showing geographical coverage of all the localities cited in this paper on a base map of the regional ecoregions: Dark Green (Dry Chaco and Cerrados del Chaco); Light Green (Humid Chaco); Orange (Cerrado); Bright Green (Atlantic Forest).
Results Callithrix argentata melanura: Stallings and Mittermeier (1983: ecology, distribution); following Hershkovitz (1977; Data for five species of primates in five families are pro- taxonomy, distribution) vided. One additional species is introduced/feral and four Callithrix melanura: Brooks (1996: ecology) other species are considered to be erroneously cited and are Callithrix argentata: Stallings (1984, 1985: ecology); Stall- thus rejected. Distributions for each of the confirmed spe- ings et al. (1989: ecology); Gamarra de Fox and Martin cies are mapped (Figs. 3–7) and levels of hierarchy are dis- (1996: distribution, specimens); Dirección de Parques tinguished from each other in the map keys allowing future Nacionales y Vida Silvestre (1998: conservation) researchers to make their own decisions on the reliability Callitrix [sic] argentata: Morales (2007: mention) of the records consistent with the demands of their own Mico melanurus: Almeida-Noronha et al. (2008: distribu- research. tion); Cabral et al. (2017: distribution); de la Sancha et al. (2017: checklist); attributed to Mico Lesson, 1840, follow- CALLITRICHIDAE: Marmosets and Tamarins (Fig. 3) ing Rylands et al. (2000) (see also Groves 2004) Mico argentata: Rumbo (2010: biogeography) Black-tailed Marmoset Mico melanurus (É. Geoffroy Local names: GUARANÍ: Cai poshy (Stallings 1985); Saint-Hilaire, 1812) Ka’i eléctrico (Dirección de Parques Nacionales y Vida Jacchus melanurus É. Geoffroy Saint-Hilaire, 1812: Rec. Silvestre 1998); Ka'i pochy (Cartes 2004); Ca’i eléctrico Observ. Zool. 1: 361. Type locality: “Brazil”, restricted to (Morales 2007); SPANISH: Mono eléctrico (Dirección “Cuyubá, Matto Grosso” by Allen (1916). de Parques Nacionales y Vida Silvestre 1998); Titi de cola negra (Cartes et al. 2017).
4 Paraguayan primatology
Figure 3. Distribution of Mico melanurus (northern Paraguay) and Callithrix jacchus.
Comments: The first citation for Paraguay is Stallings Dulce (MNHNP 503); Estancia Punto Alto (19º41’23”S, and Mittermeier (1983), who also provided some ecologi- 58º42’22”W) (MNHNP 3358). cal observations. The common name provided by Stallings Specimens not examined: ALTO PARAGUAY: 3 km E (1985) Cai poshy is probably intended to be Ka’i pochy, of Agua Dulce, PN Defensores del Chaco (NMNH 555657); roughly “angry monkey”. A specimen (NMNH 3353) col- 48 km E of Agua Dulce on Linea 1 (UMMZ 158045). lected by Captain Page during 1852 on the “Paraguay River” Literature references: ALTO PARAGUAY: 20 km W lacks precise locality data and may not have been collected of Mbarigui (19°47ʹ38.95ʺS, 58°48ʹ07.73ʺW) (Cabral et al. in Paraguay. During October 1852, Page received permis- 2017); 30 km E of Aguadulce (Stallings and Mittermeier sion from the Paraguayan president Carlos Antonio López 1983); 48 km E of Aguadulce, 1.9 km S of Linea 1 (Stall- to explore the Upper Paraguay River as far as the limits of ings and Mittermeier 1983); 48 km east of Aguadulce, 14 Paraguayan territory, and reached Bahía Negra (the north- km S of Linea 1 (Stallings and Mittermeier 1983); Chovo- ern limit) on 25 November of the same year. In defiance reca (Cartes et al. 2017). of the presidential instructions, however, he continued into Brazilian territory and anchored off Corumbá, state of Mato Common Marmoset Callithrix jacchus (Linnaeus, 1758) Grosso do Sul, Brazil, on 1 December (Smith and Bartlett 2009). The specimen could thus have been taken in Brazil- Comments: A group of approximately 10 individuals ian or Bolivian territory. lives as a feral troop in the grounds of the Hotel del Lago, Geographical distribution: Mico melanurus is restricted San Bernardino, department of Cordillera, with some addi- to the northeastern part of the Chaco region, where it inhab- tional individuals reported free at nearby Altos and Atyrá, in its tall subhumid forests (Stallings 1985; Cabral et al. 2017) the same department. The San Bernardino troop was intro- in a transitional area between the Cerrados del Chaco, Dry duced by the owners of the hotel and is fed by them, but is Chaco and Pantanal ecoregions (Mereles et al. 2013; Cabral free-living. The species also appears on a stamp printed in et al. 2017). This species is considered Vulnerable in Para- Paraguay in 1985 as part of the “Nature Protection – Ani- guay (Cartes et al. 2017, 2018). mals of Paraguay” issue. We are aware of reports dating Specimens examined: ALTO PARAGUAY: 2 km E back several decades, and this species, native to Northeast of Agua Dulce (MNHNP 505; Cabral et al. 2017); 54 km Brazil, is feral/introduced in Paraguay. E of Agua Dulce (MNHNP 502, 504); 65 km SE of Agua
5 Smith et al.
Figure 4. Distribution of Sapajus cay in Paraguay.
CEBIDAE: Capuchins and Squirrel Monkeys (Fig. 4) tracks); Esquivel (2001: guide); Cartes (2003: list); Fariña and Hostettler (2003: distribution); Hill et al. (2003: use); Hooded Capuchin Sapajus cay (Illiger, 1815) Cartes (2007: use); Morales (2007: list); Horton (2008: men- Callithrix Cay Illiger, 1815: Abd. K. pr. Akad. Wiss. p.107. tion); Vera de Bilbao (2009: epidemiology); Itaipú Binacio- Type locality “left bank of the Río Paraguay, Paraguay.” nal (2010: guide); Rumbo (2010: biogeography) Cebus azarae: Rengger (1830: ecology, type description); Cebus apella paraguayanus: Roguin (1986: distribution); Burmeister (1869: mention); Elliot (1913: taxonomy) Matayoshi et al. (1986: genetics); Matayoshi et al. (1987: Cebus fatuellus: Bertoni (1914: list) genetics); Mudry de Pargament and Slavutsky (1987: genet- Cebus libidinosus: Bertoni (1914: list); Bertoni (1939: list); ics); Schneider et al. (1988: genetics); Sampaio et al. (1991: Ávila (2004: morphometry, taxonomy) genetics); Szapkievich et al. (1998: genetics); Martinez et Cebus fatuellus azarae: Bertoni (1939: list) al. (2004: genetics) Cebus apella azarae: Pusch (1941: description) Cebus appella [sic] paraguayanus: Sampaio et al. (1991: Cebus apella morrulus: Pusch (1941: p.207, ssp. descrip- genetics) tion, type locality “Santa Barbara, Central Paraguay”) Cebus libidinosus paraguayanus: Ávila (2004: morphom- Cebus apella chacoensis: Pusch (1941: p.208, ssp. descrip- etry, taxonomy); Arístide et al. (2014: morphometry, tion, type locality “Chaco Paraguayo”) taxonomy) Cebus apella: Servicio Forestal Nacional (1982: guide); Cebus sp.: Roig et al. (2009: epidemiology) Travi et al. (1982: parasitology); Stallings and Mittermeier Cebus (Sapajus) cay: Casado et al. (2010: genetics) (1983: mention); Clark (1983: report); Stallings (1984, 1985: Cebus paraguayanus: Soria (1959: anatomy); Masi Pallarés ecology); Stallings et al. (1989: mention); Matayoshi et al. (2011: ecology) (1986: genetics); Matayoshi et al. (1987: genetics); Ferro Cebus (apella) cay: Centrón et al. (2013: use) et al. (1988: pharmacology); Rosner et al. (1988: parasitol- Cebus nigritus: Velázquez and Ramírez Pinto (2014: guide) ogy); Rosner et al. (1988: parasitology); Ferro et al. (1990: Sapajus cay: Ávila (2015: morphometry, taxonomy); Smith pharmacology); Jara Yörg et al. (1990: pharmacology); and Briggs (2015: demography); Acosta et al. (2016: para- Brooks et al. (1993: distribution); Brooks (1996: ecology); sitology); Cabral et al. (2017: mention); de la Sancha et al. Gamarra de Fox and Martin (1996: distribution, specimens); (2017: checklist); Smith (2017a, 2017b: behavior); Smith Lowen et al. (1996: distribution); Hill et al. (1997: use); and Payne (2017: pharmacology); Smith et al. (2018: behav- Dirección de Parques Nacionales y Vida Silvestre (1998: ior); Smith et al. (2020: behavior) conservation); Szapkievich et al. (1998: genetics); Yahnke et Local names: ACHÉ: Pua’á (Villalba and Yanosky al. (1998: distribution); Samudio et al. (1999: parasitology); 2000); Pua’a (Esquivel 2001); Fuakumba (Centrón et Hill and Padwe (2000: use); Villalba and Yanosky (2000: al. 2013); Puaa (Centrón et al. 2013); GUARANÍ: Caí
6 Paraguayan primatology
(Sanchez-Labrador 1770); Caimiri (Azara 1801); Caý noted, however, that the character was variable and “not of (Azara 1801); Caygüazú (Azara 1801); Mihi (Rengger great value.” Both of these in fact refer to this same species. 1830); Kaaí (Bertoni 1914); Cai comun (Stallings 1985); Pusch (1941) described two subspecies from Paraguay Ka’i Paraguay (Villalba and Yanosky 2000); Ka’i (Cartes (neither of which is currently considered valid), which he 2003); Ca’i Paraguay (Morales 2007); SPANISH: Capu- recognized in addition to the form azarae Rengger, 1830, chino (Servicio Forestal Nacional 1982); Mono capuchino and all of which he treated under the species name Cebus marrón (Esquivel 2001); Mono capuchino (Morales 2007); apella. One of these was a supposed Chaco subspecies Capuchino marrón (Horton 2008); Mono caí (Velázquez and chacoensis, but no precise locality was provided. Stallings Ramírez Pinto 2014); Mono capuchino de Azara (Cartes et (1985) surmised that it may have been based on a pet. al. 2017). The local indigenous name Cay (and variations) The species is the second most hunted and third most means “resident of the forests” (Rengger 1830). important mammal species by biomass in the diet of the Comments: The nomenclatural history of this form is Aché indigenous tribe of the Mbaracayú Reserve, Canindeyú extremely complex. The “robust capuchin” genus Sapa- department (Hill et al. 1997, 2003). It is used in local medi- jus Kerr, 1792, was long considered to be part of the genus cine to treat coughs, pain, anthrax and skin afflictions, and to Cebus Erxleben, 1777, but they form two distinct, mono- increase intelligence (Cartes 2007). phyletic clades (Lynch Alfaro et al. 2012a; Martins Jr. et al. Sapajus cay has long been used in the region as a 2018). Elliot (1913) split the capuchins into two groups: species for biomedical (mainly physiology and parasitol- those with “heads without tufts on males” and those with ogy) research in laboratories. A compilation of previous “heads with tufts or ridges on males”. Hershkovitz (1949, works made on the subject with Paraguayan specimens or 1955) agreed with this separation but argued that Cebus by Paraguayan researchers was edited by Moreno Azorero apella should be classed as a member of the tufted group. and Rosner (1989) but it unfortunately failed to properly Hill (1960) reduced the 12 recognized species of tufted cite the original works or to mention authors. These works capuchin to one, Cebus apella, with 16 subspecies. Groves were identified by cross-referencing with a list of literature (2001) recognized four species (C. apella, C. libidinosus, included at the end of the book and only the original sources C. nigritus and C. xanthosternos) with 13 subspecies. The are cited here. A similar case occurs with Rosner and Kawa- tufted (Sapajus Kerr, 1792) and untufted (Cebus Erxleben, bata (1990) who edited a monograph on Chagas’ disease in 1777) capuchins were classified as separate subgenera by Paraguay, including both unpublished and previously pub- Silva Jr. (2001) and as separate genera by Lynch Alfaro et al. lished works, many of them concerning Paraguayan Sapajus. (2012b) based on their morphologies. Genetic studies have Geographical distribution: Distributed mainly in east- since confirmed that Sapajus and Cebus diverged around ern Paraguay where it is associated with the Atlantic Forest the late Miocene epoch, possibly as a result of the establish- and Cerrado eco-regions. It occurs in gallery forest, Cer- ment of the Amazon River (Hoorn et al. 2010; Halsam 2012; radón, and Atlantic Forest and can tolerate considerable Lynch Alfaro et al. 2012a; Martins Jr. et al. 2014). habitat modification provided it is not hunted (Smith and The correct name applicable to the species has also been Briggs 2015; Smith 2017a, 2017b; Smith and Payne 2017). much debated (Elliot 1913; Cabrera 1917, 1939, 1957; Hill It extends marginally into the northern Chaco in the Cer- 1960; Torres 1983; Mantecon et al. 1984; Brown and Rumiz rados del Chaco ecoregion, although the status of the spe- 1985; Mudry 1990; Zunino and Mudry 1993; Ponsà et al. cies there requires confirmation, and may also extend very 1995; Groves 2001; Silva Jr. 2001; Martínez et al. 2002, marginally into gallery forest in the extreme southeast of 2004; Ávila 2004; Casado et al. 2010; Rylands et al. 2012; the department of Ñeembucú (Álvaro Vera pers. comm.). Aristide et al. 2014). And numerous subspecies and species The distribution maps provided by Stallings (1985) and the have been described on the basis of Paraguayan type mate- IUCN Red List show a wide distribution throughout Ñeem- rial (Rengger 1830; Pusch 1941). bucú, which is is not supported by the data, and indeed the The first citation for Paraguay is the Caý of Azara (1801: swamps of the Humid Chaco ecoregion possibly act as a bar- No.62 Tome 2: 182–194), who described it as “more scarce” rier to its distribution. than Alouatta caraya and provided a detailed description The population in the Jardín Botánico of the capital and biological data. He noted the use of two common names city Asunción is of uncertain origin. In 2017, staff mem- Caygüazú (“big monkey”) and Caimiri (“little monkey”) bers at the Asunción Zoological Gardens informed author which he attributed to differing ages. The species was then Rebecca Smith that they had being releasing their surplus subsequently given the name Callithrix cay by Illiger (1815) animals and difficult individuals (surrendered pets) into based on Azara’s description. Unaware of this, Rengger the forested area there, making it impossible to determine (1830) later described Cebus azarae based partly on the whether the species occurs there naturally or if the entire same description and provided additional biological details population is of captive origin. The zoo has also released from his own observations. surplus primates in unspecified localities on the west bank of Bertoni (1914, 1939) listed two species in this genus for the Paraguay River close to Asunción (where the species is Paraguay stating that C. libidinosus had a “longer tail” than not known to occur naturally), and the status of these popu- C. fatuellus and 23 as opposed to 22 “free vertebrae.” He lations is unknown. At least one, extremely dark individual
7 Smith et al.
resembling (from photos) the black-horned capuchin Sapa- 124696); SAN PEDRO: Puerto Ybapobo (FMNH 26651, jus nigritus was released west of the Paraguay River during 26652); Santa Barbara Central-Paraguay (BZM 44290; type one of these campaigns. of Cebus apella morrulus Pusch, 1941). Two specimens (AMNH 139998, 139999) collected by Literature references: ALTO PARANÁ: Estancia San Pedro Willim on 10 April 1941 with the vague locality of Antonio (Brooks et al. 1993); Parque Nacional Ñacunday “Boquerón, Paraguay” are considered unlikely to have been (Stallings 1985); Reserva Nacional Kuri’y (Stallings 1985); collected in the department of Boquerón, and probably came AMAMBAY: Parque Nacional Cerro Corá (Stallings 1985); from elsewhere. Willim did collect in the Chaco along the CAAGUAZÚ: Estancia Kaa’gua Rory (Lowen et al. 1996); Pilcomayo during late April and early May 1941, but these Santa Catalina (Matayoshi et al. 1986; Matayoshi et al. 1987; specimens are two weeks earlier than the earliest speci- Schneider et al. 1988; Sampaio et al. 1991; Casado et al. mens of other species with Pilcomayo collection data. We, 2010); CAAGUAZÚ/CANINDEYÚ: Estancia La Golon- therefore, consider the provenance of these specimens to be drina II (Brooks et al. 1993); CAAZAPÁ: Parque Nacional doubtful. Caaguazú (Stallings 1985); Reserva Ecológica Caaguazú The populations at Rancho Laguna Blanca, San Pedro (Lowen et al. 1996); Reserva Natural Tapytá (Velázquez department (2013–2017), and Estancia Nueva Gambach, and Ramírez Pinto 2014); CANINDEYÚ: Reserva Bosque Itapúa department (2017 to present) are being extensively Mbaracayú (Brooks et al. 1993; Hill et al. 1997; 2003); studied by Rebecca Smith and students of the Para La Tierra Reserva Natural Privada Itabó (Brooks et al. 1993; Lowen Centro IDEAL research center (
8 Paraguayan primatology
Figure 5. Distribution of Aotus azarae in Paraguay.
Aotus azarae: Allen (1916: specimen); Hershkovitz (1983: Binacional 2010); Mono nocturno de Azara (Cartes et al. taxonomy, distribution); Stallings (1984, 1985: ecology); 2017); Mono de noche (Weiler et al. 2019). Stallings et al. (1989: ecology); Brooks (1996: biology); Comments: The first citation for Paraguay is the- Mir Cartes (2003: list); Itaipú Binacional (2010: guide); Masi iquiná of Azara (1801: No. 63 Tome 2: 195–199). He states Pallarés (2011: ecology); Cabral et al. (2017: mention); de that the species is absent from the Oriental region and con- la Sancha et al. (2017: checklist); Sánchez et al. (2019: eth- fined to the Chaco and provides a detailed description. This nology); Weiler et al. (2019: field guide). was echoed by Bertoni (1939) who stated that the species Aotus trivirgatus: Wright (1983: behavior); Whitaker and occurs in the Paraguay River basin and that he had never Abrell (1987: parasitology). found it in the forests of Alto Paraná. Although Stallings Aotus trivirgatus azarae: Cabrera (1959: mention); Wetzel (1985) mentions rumors of the species east of the Paraguay and Lovett (1974; specimens); Roguin (1986: distribution) River by indigenous groups there are still no records in the Aotus sp.: Stallings and Mittermeier (1983: mention) Oriental Region to this day (although a feral population of Aotus azarai: Gamarra de Fox and Martin (1996: distribu- released individuals is present in the Jardín Botánico de tion, specimens); Dirección de Parques Nacionales y Vida Asunción). Given what we know about the habitat require- Silvestre (1998: conservation); Yahnke et al. (1998: dis- ments of this species, its natural occurrence over most of the tribution); Villalba and Yanosky (2000: tracks); Ziegler et Oriental region seems improbable. However, local reports al. (2002: distribution); Campos et al. (2004: distribution); (residents of Pilar to RS pers. comm.) from the department Morales (2007: list); Vinke and Vinke (2008: guide); Rumbo of Ñeembucú, an area of humid Chaco on the eastern banks (2010: biogeography). of the Paraguaya River similar to the habitat in the depart- Local names: AYOREO: Ñame caate (Sánchez et al. ment of Presidente Hayes, where the species is known to 2019); GUARANÍ: Miriquiná (Azara 1801); Mirikina occur, may have substance and are worthy of investigation. (Rengger 1830); Mirikiná (Bertoni 1914); Cai pyhare (Stall- Forbes (1896) ignored Azara, providing a geographi- ings 1985); Mbirikina (Stallings 1985); Ka’i pyhare (Vil- cally confused distribution that the species occurs on the lalba and Yanosky 2000); Mbirikiná (Villalba and Yanosky “right bank of the River Paraguay, in the north-east of the 2000); Ca’i mirikiná (Morales 2003); Mirikiña (Masi Pal- Argentine Republic, but not in Paraguay proper” (p.170). larés 2011); LENGUA-MASCOY: Kyilineat (Stallings Elliott (1913) used the name Aotus miriquouina (É. Geof- 1985); MANJUI: Laynakit (Stallings 1985); SPANISH: froy, 1812) which was also based on Azara’s description for Mono nocturno (Cartes 2007); Mono de la noche (Itaipú the species, borrowing part of Forbes (1896) distribution
9 Smith et al.
in restricting the type locality to “right bank of the River locality (MNHNP 1113); Parque Nacional Teniente Enciso, Paraguay, north-eastern part of the Argentine Republic.” Picada Boliviana 3 km N of administration (MNHNP 498). (p.11). Until that moment the priority of the name Aotus Specimens not examined: “Paraguay” (RBINS 448617, miriquouina (É. Geoffroy, 1812) over Aotus azarae was still 448618); ALTO PARAGUAY: 50 km WNW of Madrejón, assumed, as the publication date of Humboldt’s Recueil d’ Misión Nuevo Tribu (UMMZ 124692, 124693, 125577); Observations de Zoologie et d’Anatomie was thought to be Puerto Casado, 7 km SW of Laguna General Díaz (FMNH 1815. 54331, 54332); BOQUERÓN: 15 km S of PN Tte Enciso, Use of the masculine form of the species name Aotus 4.5 km E of Transchaco (UF 20657); Orloff (FMNH 63864); azarai was promoted as an emendation to A. azarae Hum- 50 km WSW of Madrejón (AMNH 248393); PRESI- boldt, 1811 by several authors (Groves 1989, 2001; Aquino DENTE HAYES: 30 km W of Puerto Casado on the rail et al. 1990; Gozalo and Montoya 1990) supposedly to road (FMNH 54333); 80 km W of Puerto Pinasco (USNM comply with Article 31 of the Code of Zoological Nomen- 236351); Central Chaco, 100 km N of Concepción (BMNH clature (Garbino and Costa 2015). However, when rec- 1894.3.6.3, 1894.3.6.4); Estancia Apendice km 293 Ruta ognized as a Latin name, Azara (of Félix de Azara) gives Transchaco (MHNG 1689.064); Left bank of Río Verde, 3 azarae and should not be emended (Brandon-Jones et al. km N of line camp Juan de Salazar (DEL, CONN 16609, 2007; Dubois 2007). Wetzel and Lovett 1974); Río Negro (AMNH 36508, 36509, The species is reported to be diurnal in the Argentine 36510). Chaco (Fernández-Duque and Ekert 2006) or to be most Literature references: ALTO PARAGUAY: Cerro active at dawn and dusk (Fernández-Duque et al. 2010), but León (Campos et al. 2004); Estación Biológica Tres Gigan- is apparently active by day and by night in the Paraguayan tes (González et al. 2019); Estancia San José (Brooks 1996); Chaco (Wetzel and Lovett 1974; Wright 1983). Seasonal “surroundings of 20º19'S 60º18'W” (Ziegler et al. 2002); nocturnal activity seems unlikely as animals were observed BOQUERÓN: Neuwestland (Ziegler et al. 2002); “outside feeding close to midnight at Cerro León during mid-winter of Neuland” (Campos et al. 2004); Teniente Ochoa (Wetzel (11 August 2015) and emerging from tree roosts shortly after and Lovett 1974); PRESIDENTE HAYES: Río Pilcomayo, sunset during late spring (12 October 2017), while a troop at mouth of Río Negro, about 100 miles west of Asunción 2 km north of Cruce Los Pioneros, Presidente Hayes, was (Kerr 1891; Allen 1916); Parque Nacional Tinfunque (Stall- active mid-morning on 22 September 2014 (Paul Smith). In ings 1985). the Argentine Chaco nocturnal activity is associated with the Photographic records: ALTO PARAGUAY: Picada lunar cycle, with activity inhibited by a lack of moonlight Chovoreca (CLO-ML 195379); BOQUERÓN: Fortín (Fernández-Duque et al. 2010). Patria (José Luís Cartes); PRESIDENTE HAYES: Estan- In the Paraguayan Humid Chaco, they appear to ran- cia La Golondrina (CLO-ML 90200, 90201, 90202, 90203, domly select sleeping locations rather than reusing specific 90204, 90205, 90206). sleeping sites, hold home ranges about half the size of those Reliable observations: BOQUERÓN: Estancia in Peru (5 ha), and maintain a shorter daily path length Iparoma (PS); PRESIDENTE HAYES: 2km north of Cruce (Wright 1994). Night monkeys in Paraguay are omnivo- Los Pioneros (PS). rous but eat significantly more leaves in winter and insects and flowers in spring (Wright 1994). Individuals at Estancia PITHECIIDAE: Titis, Sakis and Uacaris (Fig. 6) Iparoma were seen to eat flowers of the Samu’u tree (Ceiba chodatii, Malvaceae). White-coated Titi Monkey Plecturocebus pallescens Geographical distribution: Apparently restricted to the (Thomas, 1907) Paraguayan Chaco in the departments of Boquerón, Alto Callicebus pallescens Thomas, 1907: Ann. Mag. Nat. Paraguay and Presidente Hayes, where it is widespread in the Hist., ser. 7, 20: 161. “Chaco of Paraguay: 30 miles N of ecoregions of Dry and Humid Chaco, Cerrados del Chaco Concepción.” and Pantanal. It has been observed in forested hedgerows Callicebus pallescens: Thomas (1907: description); Elliot in heavily-modified agricultural environments in the central (1912: taxonomy); Cartes (2003: list); Horton (2010: men- Chaco, suggesting a tolerance for habitat modification. tion); Rumbo (2010: biogeography); Porter et al. (2013: Specimens examined: ALTO PARAGUAY: 1 km W of conservation); Cartes (2015: ecology); Boyle (2016: conser- Madrejón Parque Nacional Defensores del Chaco (MNHNP vation); Cabral et al. (2017: mention) 492); 3 km E of Agua Dulce administration Parque Nacional Callithrix sciurea: Bertoni (1914: list, see hypothetical sp.) Defensores del Chaco (MNHNP 491); 18 km W of Agua Callicebus moloch: Stallings and Mittermeier (1983: men- Dulce (MNHNP 490); 35 km E of Agua Dulce on Linea 1 tion); Stallings (1984, 1985: ecology); Stallings et al. (1989: (MNHNP 497); 54 km E of Agua Dulce 14 km S of Linea ecology); Hugot et al. (1994: parasitology); Brooks (1996: Vieja (MNHNP 500, 501); Linea 16, 12 km S of Linea 1 ecology) Parque Nacional Defensores del Chaco (MNHNP 496); Callicebus moloch donacophilus: Roguin (1986: Parque Nacional Defensores del Chaco 3 km E of admi- distribution) nistration on Linea Z (MNHNP 499); BOQUERÓN: No
10 Paraguayan primatology
Figure 6. Distribution of Plecturocebus pallescens in Paraguay.
Callicebus donacophilus pallescens: Hershkovitz (1990: perhaps seasonal). The species seems to be associated with taxonomy, distribution) Pantanal, Cerrados del Chaco and more humid areas within Callicebus donacophilus: Gamarra de Fox and Martin (1996: the Dry Chaco region (especially along water courses, even distribution, specimens); Dirección de Parques Nacionales when these run dry), but may be able to expand its range y Vida Silvestre (1998: conservation); Yahnke et al. (1998: further into the Dry Chaco during particularly wet years. distribution); Morales (2007: list) Indeed, the Guaraní name Kai yguá means “water monkey,” Plecturocebus pallescens Byrne et al. (2016: taxonomy); de potentially in reference to this association. This species is la Sancha et al. (2017: checklist); Sánchez et al. (2019: eth- considered Near Threatened in Paraguay (Cartes et al. 2017, nology); Weiler et al. (2019: field guide). 2018). Local names: AYOREO: Ñame po (Sánchez et al. The type locality “Chaco, 30 km N of Concepción” 2019); GUARANÍ: Kaaí-mirí (Bertoni 1914); Cai ygau (BMNH 1894.3.6.1) implies that it was collected west of the (Stallings 1985); Ka’i y’gua (Dirección de Parques Nacio- Paraguay River. It is tentatively listed as in the department nales y Vida Silvestre 1998); Ka’i ygáu, Kai yguá (Cartes of Presidente Hayes here (based on the known distribution 2003); Ca’i ygáu (Morales 2007); Kaí Ygáu (Cartes 2015); of the species), but it should be noted that, taken literally, the Ka’i mirĩ (Weiler et al. 2019); LENGUA-MASCOY: Yam- locality would be the only report of the species from east of kyilineat (Stallings 1985); MANJUI: Lawite (Stallings the Paraguay River. 1985); SPANISH: Tití (Azara 1801); Mono titi (Dirección Specimens examined: ALTO PARAGUAY: 10 km de Parques Nacionales y Vida Silvestre 1998); Sahui (Cartes from Colonia Tribu Nueva Bahía Negra (MNHNP 1877); 2003); Mono tití blanco, Titi chaqueño (Cartes 2015); Tití 13 km E of Agua Dulce Linea 1 (MNHNP 494); 15 km W del Chaco (Sánchez et al. 2019). of Bahía Negra (MNHNP 817); 18 km W of Agua Dulce Comments: Byrne et al. (2016) established the genus Linea 1 (MNHNP 493); 36 km E of Agua Dulce Linea 1 Plecturocebus but retained the species in the donacophilus (MNHNP 495); Estancia Guyra Toro km 55 Ruta to Bahía group following the traditional arrangement of previous Negra (19°48.331'S, 58º37.243'W) (MNHNP 3359); PRES- authors (Hershkovitz 1990; Kobayashi 1995; Van Roos- IDENTE HAYES: 1 km E of Parador Cainn Río Verde malen et al. 2002; Groves 2001, 2005). (MNHNP 1876); Close to Río Verde (MNHNP 816). Geographical distribution: All modern records are Specimens not examined: ALTO PARAGUAY: Cerro from the Chaco departments of Alto Paraguay (where it León, 50 km WNW of Madrejón (UMMZ 125576; Brooks appears to be widespread and common) and Boquerón and 1996); Parque Nacional Defensores del Chaco (MNHG Presidente Hayes (where occurrence is more marginal and 1636.030; Hugot et al. 1994; Porter et al. 2013); 30 km
11 Smith et al.
Figure 7. Distribution of Alouatta caraya in Paraguay.
W of Puerto Casado along the rail road (FMNH 54334); Alloutta caraya: Hill et al. (1999: use); Díaz et al. (2007: BOQUERÓN: 19 km WSW of Trans Chaco road km588 epidemiology) (UMMZ 161802); PRESIDENTE HAYES: Chaco, 30 Alouatta caraya: Krieg (1928: behavior, ecology); Stallings miles north of Concepción (BMNH 1894.3.6.1, type speci- and Mittermeier (1983: mention); Stallings (1984, 1985: men); Chaco opposite San Salvador (BMNH 1894.3.6.2); ecology); Mudry de Pargament and Slavutsky (1987: men- 80 km W of Puerto Pinasco (USNM 236352); Fort Wheeler tion); Stallings et al. (1989: mention); Brooks et al. (1993: (AMNH 42208, 42209, 42211, 42212, 42213, 42214). distribution); Brooks (1996: ecology); Gamarra de Fox and Literature records: ALTO PARAGUAY: Cerro Chovo- Martin (1996: distribution, specimens); Lowen et al. (1996: reca (Porter et al. 2013); Estación Biológica Tres Gigantes distribution); Dirección de Parques Nacionales y Vida Sil- (González et al. 2019); Estancia San José (Brooks 1996); vestre (1998: conservation); Szapkievich et al. (1998: Finca Tobich, near Bahía Negra (Cartes 2015); Fortín genetics); Yahnke et al. (1998: distribution); Hill and Padwe Patria Lodge (Porter et al. 2013); Parque Nacional Río (2000: use); Villalba and Yanosky (2000: tracks); Esquivel Negro (Porter et al. 2013); BOQUERÓN: Parque Nacional (2001: guide); Cartes (2003: list); Fariña and Hostettler Teniente Enciso (Yahnke et al. 1998). (2003: distribution); Asunce et al. (2007: genetics); Díaz et Photographic records: ALTO PARAGUAY: Picada al. (2007: epidemiology); Morales (2007: list); Roig et al. Chovoreca (CLO ML 195381); S side of Cerro León (CLO (2009: epidemiology); Giordano and Ballard (2010: distri- ML 144158). bution); Horton (2010: mention); Rumbo (2010: biogeog- raphy); Masi Pallarés (2011: ecology); Centrón et al. (2013: ATELIDAE: Howlers, Spider and Woolly Monkeys and use); Cabral et al. (2017: mention); de la Sancha et al. (2017: Muriquis (Fig. 7) checklist); Kowalewski et al. (2017: parasitology); Sánchez et al. (2019: ethnology). Paraguayan Howler Monkey Alouatta caraya (Hum- Local names: ACHÉ: Krajá (Villalba and Yanosky boldt, 1812) 2000); Kraja (Esquivel 2001); Karaja (Centrón et al. Simia Caraya Humboldt, 1812: Rec. Obs. Zool. Anat. 2013); AYOREO: Ojojo (Sánchez et al. 2019); GUAR- Comp., p.355. Type locality “Paraguay”. ANÍ: Carayáa (Sánchez-Labrador 1770); Carayá (Azara Mycetes caraya: Rengger (1830: biology); Kerr (1891: 1801); Karadyá, Pohû (Bertoni 1914); Guarí, Karayá (Ber- distribution) toni 1939); Caraya (Stallings 1985); Karaja (Villalba and Mycetes carayá: Burmeister (1869: mention) Yanosky 2000); GUAYCURU: Aychega (Sanchez Labrador Mycetes auratus: Burmeister (1869: mention) 1770); LENGUA-MASCOY: Yitsenei Kyelowai (Stallings Alouata nigra: Bertoni (1914, 1939: distribution) 1985); MBYA: Pohu (Villalba and Yanosky 2000); SPAN- ISH: Mono aullador (Esquivel 2001); Mono aullador negro
12 Paraguayan primatology
(Morales 2007); Mono carayá (Velázquez and Ramírez Pinto Melgarejo, Isla Yacyretá, (MNHNP 1115, 1116); Isla Tala- 2014); Mono aullador negro y dorado (Cartes et al. 2017); vera (MNHNP 1101); Isla Vaí, Isla Yacyretá (MNHNP Macaco (in Ñeembucú region). 1112); Schulz property “Área para Parque Nacional” San Comments: The first citation for Paraguay is the Carayá Rafael (PRC 003); MISIONES: Bosque Mbaepú, Estancia of Azara (1801: No.61 Tome 2: 169–182), meaning “chief Santa Ana (MNHNP 1105); “on the main road to Encar- of the forest”. He provided a detailed description and bio- nación” (MNHNP 1114); Reserva Yabebyry, Estancia Santa logical data, later complemented by Rengger (1830). Bur- Ana (MNHNP 1163); ÑEEMBUCÚ: Estancia Santa Ana meister (1869) mentioned a specimen “very probably” from (CZPLT 950); Pilar (CZPLT 482, 483, 498. 491, 492, 509, Paraguay under the name Mycetes auratus Gray, 1845, 951); PARAGUARÍ: Banks of the Tebicuary River, oppo- from “Orinoco”, adding that it is probably a synonym of the site Hotel Centu-Cue (26º23.942’S, 57º02.756W) (MNHNP “Carayá de Azara”. 3360). A semi-habituated troop is resident in the town plaza Specimens not examined: “Paraguay” BMNH at Santa María de la Fe, department of Misiones, and the 1930.7.31.6; ALTO PARANÁ: Hernandarias, Vivero species is commonly encountered in urban parks of Ayolas, Forestal de Itaipú (CBMI 90, 103); Tatí Yupí (CBMI 91); Misiones and in the urban area of Pilar, department of CAAGUAZÚ: Río Guyraunguá near Estancia Primera Ñeembucú, which has a substantial population of over 100 (MCZ 28095, 28096, 28654, 28655, 28656, 28713); MIS- individuals (Para La Tierra, unpubl. data). The latter popu- IONES: 2.7 km N of San Antonio by road (UMMZ 124689, lation is being extensively studied by Rebecca Smith and 124690); 37 km SW of San Ignacio by road (UMMZ students at the Para La Tierra Centro IDEAL research centre 146506); 40 km S of San Ignacio (AMNH 234785, 234786); (www.paralatierra.org), based in Pilar (Pinkowski and Smith ÑEEMBUCÚ: Tacuaras (UMMZ 124691); SAN PEDRO: 2018; Alesci et al. 2018; Kane and Smith 2019; McBride Puerto Ybapobo (FMNH 26650, 26653). and Smith 2019; Kane and Smith 2020; Wellian and Smith Literature references: ALTO PARAGUAY: Estación in press; Duffy et al. in press). Biológica Tres Gigantes (González et al. 2019); Puerto A series of specimens (USNM 3354, 3355, 3357, 3359, Casado (Soria 1959); Río Negro (Horton 2010); ALTO 4619) collected during the mid-19th Century by Captain T. PARANÁ: Parque Nacional Ñacunday (Stallings 1985); Page on or near the Río Paraguay lack precise data. They are Reserva Nacional Kuri’y (Stallings 1985); BOQUERÓN: omitted here because of the possibility they were collected in “130 km S of Chaco Defensores National Park (21°41.176'S, Argentina. Similarly, a BMNH specimen no.1911.10.27.5, 60°09.234'W)” (Giordano and Ballard 2010); CAAGUAZÚ/ reportedly from Tayru, Paraguay, is accompanied by approx- CANINDEYÚ: Estancia La Golondrina II (Brooks et al. imate coordinates (c. 27º00'W, 58º33'S) that place it margin- 1993); CAAZAPÁ: Estancia La Golondrina (= Reserva ally into Argentina close to the mouth of the Río Bermejo. Ypeti) (Brooks et al. 1993); Parque Nacional Caaguazú (Stall- We are unable to find reference to a Paraguayan locality with ings 1985); Reserva Natural Tapytá (Velázquez and Ramírez that name, so it is not included below. Pinto 2014); CANINDEYÚ: Estancia Itabó (Brooks et al. The species forms only a minor part of the diet of the 1993); Reserva Mbaracayú (Brooks et al. 2013, Lowen et Aché indigenous of Canindeyú department (Hill et al. 1999; al. 1996); Reserva de Patrimonio Aché de Kuetuvy (Centrón Centrón et al. 2013). Researchers from Para La Tierra have et al. 2013); CENTRAL: Asunción (Asunce et al. 2007); been informed that howler monkeys are not uncommonly CORDILLERA: Reserva Natural Privada Sombrero hunted for food both in and around the city of Pilar in the (Lowen et al. 1996); ITAPÚA: Isla Yacyretá (Brooks et al. department of Ñeembucú, where it is very common (Alesci 1993; Szapkievich et al. 1998; Asunce et al. 2007; Díaz et et al. 2018, submitted). al. 2007); Monumento Nacional Bosque de Arary (Lowen Geographical distribution: Widespread across the coun- et al. 1996); MISIONES: Ayolas (Szapkievich et al. 1998); try. It is absent only from the most arid areas of the Dry ÑEEMBUCÚ: “S of Pilar” (Brooks 1996); PARAGUARÍ: Chaco, but is prone to wandering and may extend its distri- Parque Nacional Ybycuí (Stallings 1985); PRESIDENTE bution west during wet years. Especially common in gallery HAYES: Banks of the Pilcomayo within 100 miles of forest and palm savannas in the Paraguay River watershed. Asunción (Kerr 1891); Río Negro affluent of the Pilcomayo It is sympatric with Aotus azarae and Plecturocebus palles- (Allen 1916); Riacho Negro at 58ºW, 25.5ºS (Krieg 1928); cens in the Humid Chaco and Pantanal, Mico melanurus in Estancia La Golondrina (Stallings 1985); Parque Nacional the Pantanal and Sapajus cay in the Atlantic Forest and Cer- Tinfunque (Stallings 1985); Montelindo (Brooks 1996); rado zone (though it is much less frequently encountered SAN PEDRO: S bank of Río Ypané near Belén (Sanchez in those habitats). We were unable to find any published Labrador 1770). records from the departments of Concepción, Amambay Photographic records: ALTO PARAGUAY: Estancia and Guairá, but the species undoubtedly occurs in all three, Cerrito, 21°26’46”S.57°55’W, 25 km N of Carmelo Peralta albeit at low densities in the Cerrado region. (SDR); ITAPÚA: Reserva Chopi Sayju (Roberto Derna); Specimens examined: ALTO PARAGUAY: 54 km E ÑEEMBUCÚ: Cerrito (CLO ML 195463). of Agua Dulce (MNHNP 489); ITAPÚA: Estancia Bogado, Reliable observations: ALTO PARAGUAY: Fuerte Isla Yacyretá (MNHNP 1107, 1108, 1109); Estancia Olimpo (PS); ITAPÚA: Estancia Nueva Gambach (PS,
13 Smith et al.
RS); MISIONES: Santa María de la Fe (PS, RS, SDR); Listed by Forbes (1896) as Callithrix castaneiventris PARAGUARÍ: Base Farmer, Caapucú (Roberto Derna); Gray, 1866 (considered a junior synonym of Callicebus SAN PEDRO: Rancho Laguna Blanca (RS). caligatus by Groves [2001]), perhaps following Gray (1870) who apparently associated the name with Azara’s Miriquiná. Species Cited Erroneously This species is well out of range and cited in error.
Black-horned Capuchin Sapajus nigritus (Spix, 1823) Atlantic Titi Callicebus personatus (É. Geoffroy in Velázquez and Ramírez Pinto (2014) used the scientific Humboldt, 1812) name Cebus nigritus for the species inhabiting the Reserva Listed for the “Chaco now occupied by the Paraguay- Natural Tapytá, department of Caazapá, but this is a mis- ans” by Burmeister (1869), under the name “Callitrix per- application of the nomenclature and refers to Sapajus cay. sonata Illig. Pr. Wied” [sic]. Although the authorship indi- Bertoni (1914, 1939) listed that species as “Kaaí hû” Cebus cated by Burmeister was wrong, the name is associated with vellerosus I. Geoffroy Saint-Hilaire, 1851, for Misiones, what now is considered Callicebus personatus, endemic to Argentina stating clearly that the species occurs from Santa eastern Brazil. The intended species is presumably the only Ana to Ihguasú “but does not cross to Paraguay.” Titi in Paraguay, the at the time undescribed Plecturocebus Various other species of capuchin monkey have been pallescens. listed as occurring in Paraguay in the older literature (for example, Cebus xanthocephalus Spix, 1823, in Gray 1870, Common Squirrel Monkey Saimiri sciureus and Black- considered a synonym of nigritus by Groves [2001]), but all capped Squirrel Monkey Saimiri boliviensis of these are attributable to confusion over the correct appli- Bertoni (1914, 1939) listed “Callithrix sciurea L. - cation of the nomenclature. Cabrera (1912) notes a speci- Kaaí-mirí Paraguay?,” citing a specimen “obtained from the men in the Museo de Ciencias Naturales de Madrid (MCNM Indians of the Paraguay River” and adding that “it seems to 1465) identified as Cebus cirrifer É. Geoffroy St. Hilaire in be the same species as that which inhabits the yerba planta- Humboldt, 1812, with the collection locality “Paraguay”. tions of the northern interior of the country.” The common The specimen was bought from a Parisian dealer who con- name Kaaí-mirí translates roughly as “little monkey.” This sidered the specimen to be Cebus azarae Rengger, 1830, and name and spelling was also mentioned by Illiger (1815). Cabrera (1912) believed that the locality was assigned by Callithrix sciureus (Linnaeus, 1758) has been applied the dealer based on the “erroneous identification.” Groves in the older literature to squirrel monkeys of the genus Sai- (2001) believed that Cebus cirrifer is a senior synonym of miri Voigt, 1831 – a name which has its root in Tupi mean- Cebus cucullatus Spix, 1823 that Groves placed as a subspe- ing “little monkey” (sai-mirim or çai-mbirín), with sai (çai) cies of C. nigritus Goldfuss, 1809. Silva Jr. (2001) believed meaning monkey and mirim (mbirín) meaning “small” that cucullatus was a junior synonym of C. nigritus, but (Simpson 1941). However, no Saimiri has ever been doc- molecular genetic studies by Lynch Alfaro et al. (2012a) umented to occur in Paraguay. The black-capped squirrel have shown that cucullatus (which perhaps should be named monkey S. boliviensis (d’Orbigny, 1834, cf. Groves 2001) cirrifer) is a distinct species. We have been unable to exam- of northern and eastern Bolivia is the species which comes ine this specimen but assume that if it really came from Par- geographically closest to Paraguay, but it is distributed well aguay then it would refer to Sapajus cay. to the north (Wallace et al. 2010). Probably on the basis of A single subadult individual of Sapajus nigritus was Bertoni´s works, Cabrera and Yepes (1940) include Paraguay photographed at Salto de Monday, Hernandarias, depart- in the distribution of Saimiri sciureus, but they expressed ment of Alto Paraná during October 2019 and shared by the doubt as to the validity of the identification. Later, Cabrera Club de Observadores de la Naturaleza - Paraguay (CON- (1957) gave the distribution of Saimiri sciureus boliviensis PY). It is unknown whether this individual was a member as “All eastern Bolivia, reaching to the south to Paraguay” of a complete family group, but its unnaturally habituated but with no additional comment regarding its supposed pres- behavior indicated that it may have been a released pet. It ence in Paraguay. has been suggested that it may have crossed the river from Callithrix sciureus (Schott, 1861) has also been used the Iguassu National Park in Brazil during a drought that as a synonym of the cotton-top tamarin Saguinus oedipus caused the river level to drop dramatically, but this seems (Linnaeus, 1758), a species that is distributed in Panama unlikely. and Colombia. This represents the only usage of this name associated with the family Callitrichidae as it is currently Black-headed Night Monkey Aotus nigriceps Dollman, understood. The name has never been applied as such to the 1909 only callitrichid that does occur in Paraguay, the black-tailed Mapped for Paraguay by Petter and Desbordes (2013) marmoset Mico melanurus (Humboldt, 1812) – the “littlest who apparently erroneously included the distributions of A. monkey” in Paraguay. Bertoni’s use of the common name azarae and A. infulatus under this species. Kaaí mirí is however consistent with the local name still in use for white-coated titi Plecturocebus pallescens today and Chestnut-bellied Titi Callicebus caligatus (Wagner, 1842) it would seem probable that this is the species intended.
14 Paraguayan primatology
Bertoni (1914, 1939) omits the name Callicebus palles- in press) use of the vertical strata and terrestrial behavior cens Thomas, 1907, from his Catálogo, even though the type (Henderson and Smith in prep.) and gastrointestinal parasite locality is “Chaco, 30 miles north of Concepción” and it is communities (Kane and Smith 2020), as well as the attitudes today still a common primate in the northern Paraguayan of local people towards the urban monkeys (Alesci et al. Chaco. Callicebus was included in Callithrix until Thomas 2018; submitted). Results from the PLT primate projects (1903) clarified its usage, but the use of the genus Chryso- are disseminated through several avenues at a national and thrix Kaup, 1835 for the squirrel monkeys Saimiri Voigt, international level, with presentations by students at various 1831, was already widespread well before this time (Palmer national and major international conferences, and multiple 1897). Bertoni’s usage seems certain to be a misapplication papers published, in press and in preparation in international of the nomenclature. Masí Pallares (2011), perhaps on the peer-reviewed journals. basis of this, stated erroneously that Saimiri sciureus “is the PLT primatology research runs in tandem with an inten- species found in the Chaco.” sive community engagement and education program. In 2018 PLT initiated the first annual Paraguayan Field Methods Discussion in Primatology course, in which international students learn participatory field methods as well as factors of relevance to This paper is a first attempt to critically quantify the primatology and conservation in Paraguay. The PLT primate available data on the distribution of Paraguayan primates team works to engage and educate the Paraguayan commu- by highlighting gaps in our knowledge, clarifying misun- nity in primate conservation through a series of different derstandings and distinguishing between different types of programs including: environmental education focusing on records so that they may be assessed separately according primate ecology and conservation in 22 rural and indige- to their level of documentation. The current representation nous schools surrounding “Área para Parque Nacional” San of Paraguayan primates in museum collections is far from Rafael; forest guard training courses in primatological field adequate and the age of many of the specimens provides techniques and in delivering participatory environmental only limited or extremely outdated information on distribu- education; and, working with national zoos, a national cam- tion and status in a country with a rapidly changing land- paign against the primate pet trade, which culminated in the scape. Accurate specimen collection data is sadly lacking publication of an illustrated children’s book (“No Soy Mas- for a large number of specimens, and collection has been cota”) (Smith and Sarvary 2017). The PLT Primate Project largely biased towards the Chaco, with most of the Oriental aims to fill the gaps in our current knowledge of Paraguayan region poorly represented in collections. primates and to train national and international primatolo- Since the work of Jody Stallings in the Paraguayan gists in important techniques to encourage greater support Chaco in the 1980s, Paraguayan primatology has been of habitat conservation in Paraguay, using Sapajus cay and largely dormant, but it has recently seen a rebirth, and qual- Alouatta caraya as flagship species. ity publications based on extensive, long-term field observa- In November 2019, the first Paraguayan primate society tions are now at last being published again, with the focus on was formed during a round table meeting at the Primer Con- the two species occurring in the Oriental region—Alouatta greso Paraguayo de Zoología. It was named Ka’i Paraguay caraya and Sapajus cay. and currently has 13 members. For the last eight years Fundación Para La Tierra (PLT) has been running Paraguay’s first-ever long-term prima- Acknowledgments tological projects: The PLT Capuchin Project and the PLT Urban Howler Monkey Project. The PLT Capuchin Project The authors are grateful to the locally-based research began in January 2013 at Rancho Laguna Blanca, San Pedro NGO Para La Tierra (www.paralatierra.org) for promoting and moved to Estancia Nueva Gambach, Itapúa in May 2017. field work with primates, offering courses in primatology, This project studies the ecological requirements of the Para- intern opportunities for students, encouraging the presenta- guayan hooded capuchin in the Upper Paraná Atlantic Forest tion of results at international congresses and helping bring and aims to determine its adaptability to anthropogenic hab- primate education to rural Paraguayan classrooms. Isabel itat disturbance. The PLT Urban Howler Monkey Project Gamarra de Fox (Museo Nacional de Historia Natural del that began in May 2017 is based in Pilar, Ñeembucú. This Paraguay) and Brogan Pett (Colección Zoológica Para La project focuses on the unusual population of urban-dwelling Tierra) provided assistance in the review of primate speci- howler monkeys in the city of Pilar. Both projects invite the mens. We thank Hugo Cabral, José Luis Cartes, Hugo del participation of national and international students in carry- Castillo, Roberto Derna, Luis Doldan, Juan Klavins, Oscar ing out research on the behavior and ecology of these mon- Rodríguez and Álvaro Vera for sharing their observations. keys. Studies so far have, for example, examined the effects Pedro, Christine and Hans Hostettler (Estancia Nueva Gam- of the urban environment on activity budgets (Pinkowski bach; Hostettler S.A.) and Malvina Duarte (Laguna Blanca) and Smith 2018; Overbeck et al. in consideration), diet, are thanked for their support and encouragement of ongo- social interactions, and home range (McBride and Smith ing primate studies on their properties, and the support of 2019; Duffy et al. in press.), risk awareness (Wellian et al. the conservation organization Pro Cosara is also recognised.
15 Smith et al.
The authors would also like to give special mention to the Boyle, S. A. 2016. Pitheciids in fragmented habitats: land work of Jody Stallings, who provided the basis for the cur- cover change and its implications for conservation. Am. rent studies. All authors are assisted by, and grateful to, the J. Primatol. 78: 534–549. Pronii program of CONACyT Paraguay. Rebecca Smith Brandon-Jones, D., J. W. Duckworth, P. D. Jenkins, A. B. receives assistance from the National Geographic Society Rylands and E. E. Sarmiento. 2007. The genitive of (Grant Number: NGS-299-18C), the Elphinstone Scholar- species group scientific names formed from personal ship (University of Aberdeen), International Primatologi- names. Zootaxa 1541: 41–48. cal Society (Lawrence Jacobsen Education Development Brooks, D. M. 1996. Some observations on primates in Par- Award) and the Primate Society of Great Britain (Cyril aguay. Neotrop. Primates 4: 15–19. Rosen Award). Brooks, T. M., L. Bartrina, S. H. M. Butchart, R. P. Clay, E. Z. Esquivel, N. I. Etcheverry, J. C. Lowen and J. Literature Cited Vincent. 1993. Bird surveys and conservation in the Paraguayan Atlantic Forest. BirdLife Int. Study Rep. 57: Acosta, N., J. Miret, E. López and A. Schinini. 2016. First 1–145. report of Sapajus cay naturally infected by Trypano- Brown A. D. and D. I. Rumiz. 1986. Distribución y con- soma cruzi in San Pedro Department, Paraguay. Brazil. servación de los primates en Bolivia. Estado actual de J. Vet. Parasitol. 25: 327–332. su conocimiento. In: A Primatologia no Brasil – 2, M. Alesci, M., R. L. Smith, J. D. Ayala Santacruz and A. Cam- Thiago de Mello (ed). pp.335–363. Sociedade Brasileira perio Ciani. 2018. Howler monkeys (Alouatta caraya), de Primatologia, Brasilia, Brazil. human interactions in the urban city of Pilar: conflict Burmeister, H. von. 1869. Catálogo de los mamíferos argen- or coexistence? Presentation at the XXVIIth Congress tinos con las especies exóticas que se conservan en of the International Primatological Society, Nairobi, el Museo Público de Buenos Aires. An. Mus. Público Kenya, 19–25 August 2018. Buenos Aires 1(6): 446–470. Allen, J. A. 1916. Mammals collected on the Roosevelt Bra- Byrne, H., A. B. Rylands, J. C. Carneiro, J. W. Lynch Alfaro, zilian expedition, with field notes by Leo E. Miller.Bull. F. Bertuol, M. N. F. da Silva, M. Messias, C. P. Groves, Am. Mus. Nat. Hist. 35: 559–610. R. A. Mittermeier, I. Farias, T. Hrbek, H. Schneider, I. Almeida-Noronha, M. de, W. R. Spironello and D. Campista Sampaio, and J. P. Boubli. 2016. Phylogenetic relation- Ferreira. 2008. New occurrence records for Mico mel- ships of the New World titi monkeys (Callicebus): first anurus (Primates, Callitrichidae). Neotrop. Primates appraisal of taxonomy based on molecular evidence. 15: 26–28. Front. Zool. 13: 1–25. Aquino, R., P. Puertas and F. Encarnacíon. 1990. Supple- Cabral, H., L. Romero, D. Bueno, A. Yanosky and D. M. mental notes on population parameters of northeastern Brooks. 2017. A new locality in Paraguay for the black- Peruvian night monkeys, genus Aotus (Cebidae). Am. J. tailed marmoset, Mico melanurus (Geoffroy Saint- Primatol. 21: 215–221. Hilaire, 1812) (Primates, Callitrichidae). Check List 13: Arístide, L., I. M. Soto, M. D. Mudry and M. Nieves. 2014. 2142. Intra and interspecific variation in cranial morphology Cabrera, A. 1912. Catálogo metódico de las colecciones de on the southernmost distributed Cebus (Platyrrhini, Pri- mamíferos del Museo de Ciencias Naturales de Madrid. mates) species. J. Mammal. Evol. 21:349–355. Trab. Mus. Cienc. Nat. 7: 1–147. Ascunce, M. S., E. Hasson, C. J. Mulligan and M. D. Mudry. Cabrera, A. 1917. Notas sobre el género Cebus. Revta. Real 2007. Mitochondrial sequence diversity of the southern- Acad. Cienc. Exact. Fis. Nat. Madrid 16(5): 1–24. most extant New World monkey, Alouatta caraya. Mol. Cabrera, A. 1939. Los monos de la Argentina. Physis 16: Phylogenet. Evol. 43: 202–215. 3–39. Ávila, I. 2004. Morphological variation between two Cabrera, A. 1957. Catálogo de los mamíferos de América subspecies of Cebus libidinosus (Primates: Cebidae). del Sur 1 (Metatheria-Unguiculata-Carnivora). Revta. Bol. Mus. Nac. Hist. Nat. Paraguay 15: 1–8. Mus. Argent. Cienc. Nat. “Bernardino Rivadavia” 4 Ávila, I. 2015. Estudio de morfometría de cráneo de dos (1): 1–307. diferentes poblaciones de Sapajus (Primates: Plathyr- Campos, J. M., I. Benítez and D. Merritt. 2004. On the rini), con notas sobre la taxonomía del género. Bol. occurrence of the owl monkey Aotus azarai in Cerro Mus. Nac. Hist. Nat. Paraguay 19: 50–57. León, Chaco, Paraguay. Neotrop. Primates 12: 55–56. Azara, F. de. 1801. Essais sur l´Histoire Naturelle des Qua- Cartes, J. L. 2004. Importancia de la conservación de los drupèdes de la Province du Paraguay. Tome 2. Charles humedales para los mamíferos. In: Los Humeda- Pougens, Paris, France. les de Paraguay, D. A. Salas-Dueñas, F. Mereles and Azara, F. de. 1802. Apuntamientos para la Historia Natural A. Yanosky (eds.), pp.141–165. Comité Nacional de de los Quadrúpedos del Paragüay y Río de la Plata. Humedales, Asunción, Paraguay. Imprenta de la Viuda de Ibarra, Madrid, Spain. Cartes, J. L. 2007. Patrones de uso de los mamíferos del Paraguay. Importancia sociocultural y económica. In:
16 Paraguayan primatology
Biodiversidad del Paraguay: Una Aproximación a sus Elliott, D. G. 1913. A review of the Primates Volume 2. Realidades, D.A. Salas-Dueñas and J. F. Facetti (eds.), Anthropoidea Aotus to Lasiopyga. Am. Mus. Nat. Hist. pp.133–149. Fundación Moises Bertoni, USAID, GEF/ Monogr. 2: 1–383. BM, Asunción, Paraguay. Erxleben, J. C. P. 1777. Systema Regni Animalis per Classes, Cartes, J. L. 2015. Notas sobre poblaciones de ka’i ygáu Ordines, Genera, Species, Varietates cum Synonymia (Callicebus pallescens Thomas, 1907) en la Finca et Historia Animalium. Classis 1 Mammalia. Impensis Tobich, Bahía Negra. Paraquaria Nat. 3: 6–11. Weygandianis, Lipisiae. Cartes, J. L., H. del Castillo, M. Kowalewski, J. J. Thomp- Esquivel, E. 2001. Mamíferos de la Reserva Natural del son and M. Velilla. 2017. Primates: Los monos. In: Bosque Mbaracayú. Fundación Moises Bertoni, Asun- Libro Rojo de Mamíferos del Paraguay, S. Saldívar, ción, Paraguay. V. Rojas and D. Giménez (eds.), pp.55–60. Asociación Fariña, R. and T. Hostettler. 2003. Vertebrados de la Reserva Paraguaya de Mastozoología y Secretaría del Ambiente. Natural del Bosque Mbaracayú Checklist. Fundación Asunción, Paraguay. Moises Bertoni, Asunción, Paraguay. Cartes, J. L., M. Velilla, N. González-Brítez and J. J. Ferro, E., A. Schinini, M. Maldonado, J. Rosner and G. S. Thompson. 2018. Estado de conservación de los prima- Hirschmann. 1988. Eugenia uniflora leaf extract and tes en Paraguay. In: La Primatología en Latinoamérica lipid metabolism in Cebus apella monkeys. J. Ethno- 2. Tomo 2, B. Urbani, M. Kosalewski, R. G. T. Cunha, pharmacol. 24: 321–325. S. de la Torre and L. Cortés-Ortiz (eds.), pp.583–596. Ferro, E. A., G. Velázquez de Saldívar, A. Rodríguez Sán- Ediciones IVIC, Caracas, Venezuela. chez, M. I. Monzón de Calabró, C. Rebollo and R. Casado, F., C. R. Bonvicino, C. Nagle, B. Comas, T. D. Henning. 1990 Producción de conjugados para inmu- Manzur, M. M. Lahoz and H. N. Seuánez. 2010. Mito- nofluorescencia indirecta y serodiagnóstico en humanos chondrial divergence between 2 populations of the y monos (Cebus apella). In: Enfermedad de Chagas Hooded Capuchin, Cebus (Sapajus) cay (Platyrrhini, en el Paraguay. J. M. Rosner and M. Kawabata (eds.), Primates). J. Hered. 101: 261–269. pp.265–271. EFACIM-JICA, Asunción. Centrón, S., R. Zárate, A. Chivugui, M. Achipurangui, E. Forbes, H. O. 1896. A Hand-book to the Primates Volume 1. Mayeregger and J. L. Cartes. 2013. Patrones de uso de Edward Lloyd, London, UK. la fauna en la Reserva de Patrimonio Aché de Kuetuvy, Gamarra de Fox, I. and A. J. Martin. 1996. Mastozoología. Canindeyú. Paraquaria Nat. 1(1): 25–31. Lista de Mamíferos del Paraguay. In: Colecciones de Clark, P. T. 1983. Observations on Cebus apella in National Flora y Fauna del Museo Nacional de Historia Natu- Park Ybycuí in Paraguay. Report. Servicio Forestal ral del Paraguay, O. Romero Martínez (ed.), pp.469– Nacional, Ministerio de Agricultura y Ganaderia, Asun- 573. Museo Nacional de Historia Natural del Paraguay. ción, Paraguay. Ministerio de Agricultura y Ganadería. San Lorenzo, de la Sancha, N. U., C. López-González, G. D’Elia, P. Myers, Paraguay. L. Valdez and M. L. Ortiz. 2017. An annotated checklist Garbino, G. S. T. and H. C. Costa. 2015. Some nomen- of the mammals of Paraguay. Therya 8: 241–260. clatural notes regarding authorship and dates of New Díaz, L. A., M. del P. Díaz, W. R. Almirón and M. S. Conti- World monkeys (Primates: Platyrrhini). Sherbornia giani. 2007. Infection by UNA virus (Alphavirus; Toga- 2(3): 21–27. viridae) and risk factor analysis in black howler mon- Geoffroy St. Hilaire, É. 1812. Tableau des quadrumanes ou keys (Alouatta caraya) from Paraguay and Argentina. des animaux composant le premiere ordre de la classe de Trans. Roy. Soc. Trop. Med. Hyg. 101: 1039–1041. Mammifères. Ann. Mus d’Hist. Nat. Paris 19: 85–122. Dirección de Parques Nacionales y Vida Silvestre. 1998. Geoffroy St. Hilaire, I. and H. M. D. de Blainville. 1834. Fauna Amenazada del Paraguay. Ministerio de Agri- Rapport sur les résultats scientifiques du voyage de M. cultura y Ganaderia/Fundación Moises Bertoni, Asun- Alcide D’Orbigny dans l’Amérique du sud, pendant les ción, Paraguay. années 1826, 1827, 1828, 1829, 1830, 1831, 1832 et Dollman, G. 1909. Six new species of Aotus. Ann. Mag. Nat. 1833. Nouv. Ann. Mus. d’Hist. Nat. Paris 3: 84–115. Hist., ser. 8, 4: 199–204. Giordano, A. J. and W. B. Ballard. 2010. Noteworthy record Dubois, A. 2007. Genitives of species and subspecies nomina of a black howler monkey (Alouatta caraya) from the derived from personal names should not be emended. central Dry Chaco of Paraguay. Neotrop. Primates 17: Zootaxa 1550: 49–68. 74–75. Duffy, X., J. Wellian, and R. L. Smith. 2021. Home range González, A. R., C. Benítez R., M. Ferreira, N. Cantero, A. sizes and use of core areas of Paraguayan Alouatta Arias, L. Matosso and V. Rojas Bonzi. 2019. Mamíferos caraya living in an urban environment. In press. medianos y grandes de la Reserva Pantanal Paraguayo: Elliot, D. G. 1912. A review of the Primates. Volume 1. Estación Los Tres Gigantes, Alto Paraguay, Paraguay. Lemuroidea Daubentonia to Indris. Anthropoidea Paraquaria Nat. 7(1): 8–18. Seniocebus to Saimiri. Am. Mus. Nat. Hist. Monogr. 2: 1–315.
17 Smith et al.
Gozalo, A. and E. Montoya. 1990. Mortality causes of owl through time: Andean uplift, climate change, landscape monkeys (Aotus nancymae and Aotus vociferans) in evolution, and biodiversity. Science 330: 927–931. captivity. J. Med. Primatol. 19: 69–72. Horton, E. Y. 2008. Salvemos San Rafael / Saving San Gray, J. E. 1870. Catalogue of Monkeys, Lemurs and Fruit- Rafael. Guyra Paraguay, Asunción, Paraguay. eating Bats of the Collection of the British Museum. Horton, E. Y. 2010. Gran Pantanal Paraguay. Guyra Para- British Museum of Natural History, London, UK. guay, Asunción, Paraguay. Groves, C. P. 1989. A Theory of Human and Primate Evolu- Humboldt, F. H. A. 1812. Recueil d’Observations de Zoo- tion. Clarendon Press, Oxford, UK. logie et d’Anatomie Comparée, Faites dans l’Océan Groves, C. P. 2001. Primate Taxonomy. Smithsonian Institu- Atlantique, dans l’Intérieur du Nouveau Continent et tion Press, Washington, DC. dans la Mer du Sud Pendant les Années 1799, 1800, Groves, C. P. 2004. The what, why and how of primate tax- 1801, 1802 et 1803. Volume 1. F. Schoell and G. Dufour, onomy. Int. J. Primatol. 25: 1105–1126. Paris, France. Groves, C. P. 2005. Order Primates. In: Mammal Species Hugot, J. P., S. Morand and R. Guerrero. 1994. Trypanoxy- of the World: a Taxonomic and Geographic Reference, uris croizati n.sp. and T. callicebi Hugot and Vaucher, Volume 1, D. E. Wilson and D. M. Reeder (eds), pp.111– 1985 (Nematoda: Oxyuridae), two vicariant forms para- 184. Johns Hopkins University Press, Baltimore, MD. sitic in Callicebus spp. (Primatia, Cebidae). Syst. Para- Guyra Paraguay 2005. Atlas de las Aves del Paraguay. sitol. 27: 35–43. Guyra Paraguay, Asunción, Paraguay. Illiger, J. K. W. 1815. Ueberblick der Säugthiere nach Ihrer Halsam, M. 2012. Towards a prehistory of primates. Antiq- Vertheilung Über die Welttheile. Abh. Königl. Akad. uity 86: 299–315. Wiss. Berlin 1804–1811: 39–159. Hershkovitz, P. 1949. Mammals of northern Colombia. Pre- Itaipú Binacional. 2010. Animales del Zoológico de Itaipú. liminary report no. 4: Monkeys (Primates), with taxo- Dirección de Educación Ambiental, Itaipú, Hernandar- nomic revisions of some forms. Proc. U.S. Natl. Mus. ias, Paraguay. 98: 323–427. Kane, J. and R. L. Smith. 2020. Bertiella spp. Infection of Hershkovitz, P. 1955. Notes on the American monkeys of Alouatta caraya (Humbolt, 1812) in urban and natural the genus Cebus. J. Mammal. 36: 449–452. environments in Ñeembucú, southwest Paraguay. Am. J. Hershkovitz, P. 1977. Living New World Monkeys (Platyr- Primatol. 82(9): e23166. rhini) with an Introduction to Primates, Vol. 1. The Chi- Kaup, J. J. 1835. Chrysothrix. In: Das Thierreich, ein- cago University Press, Chicago. getheilt nach dem Bau der Thiere als Grundlage ihrer Hershkovitz, P. 1990. Titis, New World monkeys of the Naturgeschichte und der vergleichenden Anatomie von genus Callicebus (Cebidae, Platyrrhini): a preliminary den Hern Ritter von Cuvier. Erster Band. Säugethiere taxonomic review. Fieldiana Zool. n.s. 55: 1–109. und Vögel, G. Cuvier (ed.), p.50–52. J. G. Cotta’schen Hershkovitz, P. 1983. Two new species of night monkeys, Buchandlung, Stuttgart und Tübingen, Germany. genus Aotus (Cebidae, Platyrrhini): a preliminary report Kerr, J. G. 1891. Extracts from the letters of Mr J. Graham on Aotus taxonomy. Am. J. Primatol. 4: 209–243. Kerr, naturalist to the Pilcomayo expedition. Ibis 6(3): Hill, K. and J. Padwe. 2000. The sustainability of Aché hunt- 260–272. ing in the Mbaracayú Reserve, Paraguay. In: Hunting Kerr, R. 1792. The Animal Kingdom or Zoological System of for Sustainability in Tropical Forests, J. G. Robinson the Celebrated Sir Charles Linnaeus; Being a Transla- and E. L. Bennett (eds.), pp.79–105. Columbia Univer- tion of that Part of the Systema Naturae, as Lately Pub- sity Press, New York. lished, with Great Improvements by Professor Gmelin Hill, K., J. Padwe, C. Bejyvagi, A. Bepurangi, F. Jakugi, R. of Goettingen, Together with Numerous Additions Tykuarangi and T. Tykuarangi. 1999. Impact of hunting from More Recent Zoological Writers, and Illustrated on large vertebrates in the Mbaracayu Reserve, Para- with Copper Plates.Class 1 Mammalia: Containing a guay. Conserv. Biol. 11: 1339–1353. Complete Systematic Description, Arrangement, and Hill, K., G. McMillan and R. Fariña. 2003. Hunting-related Nomenclature, of all the Known Species and Varieties changes in game encounter rates from 1994 to 2001 in of the Mammalia or Animals which give Suck to their the Mbaracayu Reserve, Paraguay. Conserv. Biol. 17: Young. Strahan and Cadell, London, UK. 1312–1323. Kobayashi, S. 1995. A phylogenetic study of titi monkeys, Hill, W. C. O. 1960. Primates: Comparative Anatomy and genus Callicebus, based on cranial measurements: I. Taxonomy. IV Cebidae, Part A. Edinburgh University Phyletic groups of Callicebus. Primates 36: 101–20. Press, Edinburgh. Kowalewski, M. M., J. Torres, C. Milozzi and T. R. Gil- Hoorn, C. F., H. Wesselingh, M. Ter Steege, A. Bermudes, lespie. 2017. Bertiella sp. infection patterns in black- J. Mora, I. Sevink, A. Sanmartin, C. Sanchez-Meseguer, and-gold howler monkeys across their distribution. In: J. Anderson, C. Figueiredo, D. Jaramillo, F. Riff, T. Primatology in Argentina, M. M. Kowalewksi and L. Stadler, T. Särkinen and A. Antonelli. 2010. Amazonia I. Oklander (eds.), pp. 219–233. SAREM, Mendoza, Argentina.
18 Paraguayan primatology
Krieg, H. 1928. Tagebuch-Aufzeichnungen auf der Deut- Presentation at the Primer Congreso Zoología Para- schen Chaco-Expedition. 9. Schwarze brüllaffen. Z. guaya. Asunción, Paraguay, 25-29 November 2019. Säugetierkd. 2: 119–132. Mereles, F. 2013. Acerca de las extensiones de Cerrados y Linnaeus, C. 1758. Systema Naturae per Regna Tria Natu- Cerradones en el Paraguay. Paraquaria Nat. 1: 35–38. rae, Secundum Clases, Ordines, Genera et Species Mereles, F., J. L. Cartes, R. P. Clay, P. Cacciali, C. Paradeda, Redacta Tabulisque Aeneis Illustrata. Editio decima. O. Rodas and A. Yanosky. 2013. Análisis cualitativo Laurentii Salvii, Holmiae. para la definición de las ecorregiones de Paraguay occi- Lowen, J. C., L. Bartina, R. P. Clay, and J. A. Tobias. 1996. dental. Paraquaria Nat. 1(2): 12–20. Biological Surveys and Conservation Priorities in East- Mittermeier, R. A., A. B. Rylands and D. E. Wilson. 2013. ern Paraguay. CBS Conservation Publications, Cam- Handbook of the Mammals of the World. Volume 3. Pri- bridge, UK. mates. Lynx Edicions, Barcelona. Lynch Alfaro, J. W., J. P. Boubli, L. E. Olson, A. Di Fiore, Morales, M. A. 2007. Diversidad de mamíferos en Paraguay. B. Wilson, G. A., Gutiérrez-Espeleta, K. L. Chiou, M. In: Biodiversidad del Paraguay: Una Aproximación a Schulte, S. Neitzel, V. Ross, D. Schwochow, M. T. sus Realidades, D. A. Salas-Dueñas and J. F. Facetti T. Nguyen, I. Farias, C. H. Janson and M. E. Alfaro. (eds.), pp.133–149. Fundación Moises Bertoni, USAID, 2012a. Explosive Pleistocene range expansion leads to GEF/BM, Asunción, Paraguay. widespread Amazonian sympatry between robust and Moreno Azorero, R. and J. M. Rosner. 1989. Cebus sp. (Kai gracile capuchin monkeys. J. Biogeog. 39: 272–288. Paraguay) un modelo experimental para investigación Lynch Alfaro, J. W., Silva Jr., J. S. and Rylands, A. B. 2012b. biomédica. Mem. Inst. Investig. Cienc. Salud 9: 1–120. How different are robust and gracile capuchin mon- Mudry de Pargament, M. and I. Slavutsky. 1987. Banding keys? An argument for the use of Sapajus and Cebus. patterns of the chromosomes of Cebus apella: com- Am. J. Primatol. 74: 273–286. parative studies between specimens from Paraguay and Mantecon, M. A., M. D. Mudry and A. D. Brown. 1984. Argentina. Primates 28: 111–117. Cebus apella de Argentina, distribución geográfica, Mudry, M. D. 1990. Cytogenetic variability within and fenotipo y cariotipo. Rev. Mus. Argent. Cienc. Nat. across population of Cebus apella in Argentina. Folia “Bernardino Rivadavia” 13(41): 399–408. Primatol. 54 (3–4): 206–216. Martínez, R. A., A. Giudice, V. B. Szapkievich, M. Ascunce, Nagle, C. A., J. H. Daneri, S. Quiroga, F. Gómez-Argaña M. Nieves, G. Zunino and M. D. Mudry. 2002. Param- and J. M. Rosner. 1979. The plasma pattern of ovarian eters modeling speciogenic processes in Cebus apella steroids during the menstrual cycle in capuchin monkey (Primates: Platyrrhini) from Argentina. Mastozool. Neo- (Cebus apella). Biol. Reprod. 21: 979–983. trop. 9: 171–186. Palmer, T. S. 1897. Notes on the nomenclature of four genera Martínez, R. A., E. Torres, M. Nieves, V. Szapkievich, S. of tropical American mammals. Proc. Biol. Soc. Wash. Rodríguez, A. Schinini, M. Ascurra and M. D. Mudry. 11: 173–174. 2004. Genetic variability in two captive colonies of Petter, J. J. and F. Desbordes. 2013. Primates of the World. Cebus apella paraguayanus (Primates: Platyrrhini) Princeton University Press, Princeton, NJ. from eastern Paraguay. Caryologia 57: 332–336. Pinkowski, D. and R. L. Smith. 2018. Activity budgets of Martins-Junior, A. M. C., J. Carneiro, I. Sampaio, S. F. Fer- urban dwelling Paraguayan Howler Monkeys in Pilar, rari and H. Schneider. 2018. Phylogenetic relationships Paraguay. Poster presentation at the XXVIIth Congress among Capuchin (Cebidae, Platyrrhini) lineages: An of the International Primatological Society, Nairobi, old event of sympatry explains the current distribution Kenya, 19–25 August 2018. of Cebus and Sapajus. Genet. Mol. Biol. 41: 699–712. Ponsà, M., M. García, A. Borell, F. Garcia, J. Egozcue, M. Masi Pallarés, R. 2011. Vertebrados del Paraguay. Descrip- A. Gorostiaga, A. Delprat and M. D. Mudry. 1995. Het- ciones y Hábitos con las Denominaciones en Guaraní. erochromatin and cytogenetic polymorphisms in Cebus Herederos Rafael Masi Pallarés, Asunción, Paraguay. apella (Cebidae, Platyrrhini). Am. J. Primatol. 37: Matayohsi, T., E. Howlin, N. Nasazzi, C. Nagle, E. Gadow 325–331. and H. N. Seuánez. 1986. Chromosome studies of Cebus Porter, L, J. Chism, T. R. Defler, L. Marsh, J. Martinez, H. apella: the standard karyotype of Cebus apella para- Matthews, W. McBride, D. G. Tirira, M. Velilla and guayanus, Fischer, 1829. Am. J. Primatol. 10: 185–193. R. Wallace. 2013. Pitheciid conservation in Ecuador, Matayoshi, T., H. N. Seuánez, N. Nasazzi, C. Nagle, J. L. Colombia, Peru, Bolivia and Paraguay. In: Evolutionary Armada, L. Freitas, G. Alves, C. M. Barroso and E. Biology and Conservation of Titis, Sakis and Uacaris, Howlin. 1987. Heterochromatic variation in Cebus L. M. Veiga, A. A. Barnett, S. F. Ferrari and M. A. Nor- apella (Cebidae, Platyrrhini) of different geographic conk (eds.), pp.320–330. Cambridge University Press, regions. Cytogenet. Cell Genet. 44: 158–162. Cambridge, UK. McBride, J.H. and R. L. Smith. 2019. Monos Aulladores Pusch, B von. 1941. Die Arten der Gattung Cebus. Z. Säuge- (Alouatta caraya) urbanos y su socioecología única. tierkd. 16:183–237.
19 Smith et al.
Rengger, J. R. 1830. Naturgeschichte der Saeugethiere von Kowalewski, J. López, V. Martínez, N. Mujica, N. Neris, Paraguay. Schweighauserschen Buchhandlung, Basel, M. L. Ortiz, F. Ramírez, S. D. Ríos, M. Ruíz Díaz, J. Switzerland. Sánchez, P. Smith, R. Stevens, P. Teta, J. J. Thompson, Roguin, L. de 1986. Les mammifères du Paraguay dans les J. Torres, M. Velázquez, M. Velilla, L. Villalba and A. collections du Museúm de Genève. Rev. Suisse Zool. 93: Weiler. 2017. Los mamíferos amenazados del Paraguay. 1009–1022. In: Libro Rojo de Mamíferos del Paraguay, S. Saldívar, Roig, C., J. Miret, A. Rojas, Y. Guillén, L. Aria, L. Men- V. Rojas and D. Giménez (eds.), pp.27–33. Asociación doza, M. E. Acosta, T. Meza, L. Sosa, G. Echagüe, V. Paraguaya de Mastozoología y Secretaría del Ambiente, V. Müller, N. Vera de Bilbao, A. Schinini, J. H. Rodas Asunción, Paraguay. and V. H. Aquino. 2009. Estudio de Fiebre Amarilla en Sampaio, M. I. C., C. M. L. Barroso, B. T. F. da Silva, H. primates en áreas de brote de los departamentos de San Seuánez, T. Matayoshi, E. Howlin, N. Nassazi, C. Nagle Pedro y Central del Paraguay Study of Yellow Fever in and H. Schneider. 1991. Genetic variability in Cebus primates in outbreaks areas of the departments of San appella [sic] paraguayanus: biochemical analysis of Pedro and Central in Paraguay. Mem. Inst. Investig. seven loci and variation in Glyoxalase I (E.C.4.4.1.5). Cienc. Salud 7: 40–45. Primates 32: 105–109. Rosner, J. M., J. Bellassai, A. Schinini, T. Rovira, A. Rojas Samudio, M., S. Montenegro-James, E. Kasamatsu, M. de Arias, E. A. Ferro, E. Ferreira, G. Velázquez, M. I. Cabral, A. Schinini, A. Rojas de Arias and M. A. James. Monzón, M. Maldonado, R. Galeano and M. A. Fresco. 1999. Local and systemic cytokine expression during 1989. Cardiomyopathy in C. apella monkeys experi- experimental chronic Trypanosoma cruzi infection in a mentally infected with Trypanosoma cruzi. Trop. Med. Cebus monkey model. Parasite Immunol. 21: 451–460. Parasitol. 40: 24–31. Sánchez, P., A. Bonzi and S. D. Ríos 2019. Patrimonio Rosner, J. M., A. Schinini, A. Rojas de Arias and A. Chiola. Natural y Cultural Ayoreo Totobiegosode: Notas de 1984. Effects on growth and development of experimen- Etnozoología y Etnopaisaje. Gente, Ambiente y Ter- tal T. cruzi infection in the monkey C. apella. IDRCS ritorio, Organización Payipie Ichadie Totobiegosode. Med. Sci. 12: 101. OPIT/GAT, Asunción. Rosner, J. M., A. Schinini, T. Rovira, A. Rojas de Arias, G. Sánchez Labrador, J. 1770. [1910]. El Paraguay Católico. Velazquez, M. I. Monzon and M. Maldonado. 1988. Homenaje de la Universidad Nacional de La Plata al Acute chagas disease in non-human primates. 1. Chro- XVII Congreso Internacional de los Americanistas en nology of clinical events, clinical chemistry. ECG, radi- su reunión de Buenos Aires, en mayo 16 a 21 de 1910. ology, parasitemia and inmunological parameters in the Buenos Aires, Argentina. Cebus apella monkey. Trop. Med. Parasitol. 39: 51–55. Schneider, H., M. I. C. Sampaio, C. M. L. Barroso, B. T. E. Rosner, J. M. and M. Kawabata (eds.). 1990. Enfermedad Silva, R. Warzbort, T. Matayoshi, E. Howlin, N. Nas- de Chagas en el Paraguay. Mem. Inst. Investig. Cienc. sazi, C. Nagle, and H. Seuánez. 1988. Genetic varia- Salud 15: 1–484. bility in a natural population of Cebus apella para- Rumiz, D. and J. Stallings. 1989. Estado de la primatologia guayanus (Cebidae, Primates). Revta. Brasil. Genet. 11: en Paraguay. Bol. Primatol. 1: 37–42. 89–96. Rowe, N. and M. Myers. 2016. All the World’s Primates. Servicio Forestal Nacional. 1982. Guía de Algunos Verte- Pogonias Press, Charlestown, RI. brados del Parque Nacional Ybycuí. Ministerio de Agri- Rumbo, M. 2010. Análisis biogeográfico de los mamíferos cultura y Ganaderia, Asunción, Paraguay. de Paraguay. Boletín del Mus. Nac. Hist. Nat. Paraguay Sequera, G., H. Rodríguez and M. Torales Ruotti (eds.). 16: 18–29. 2019. Guía de Vigilancia de Epizootias en Primates Rylands, A. B., R. A. Mittermeier and E. Rodríguez Luna. No Humanos con Sospecha de Fiebre Amarilla. Minis- 1995. A species list for the New World Primates (Plat- terio de Salud Pública y Bienestar Social, Asunción, yrrhini): distribution by country, endemism, and con- Paraguay. servation status according to the Mace-Lande system. Silva. Jr., J. S. 2001: Especiação nos macacos-prego e caia- Neotrop. Primates 3(suppl.): 113–160. raras, gênero Cebus Erxleben, 1777 (Primates, Cebi- Rylands, A. B., H. Schneider, A. Langguth, R. A. Mitter- dae). Doctoral thesis, Universidade Federal do Rio de meier, C. P. Groves and E. Rodríguez-Luna. 2000. An Janeiro, Rio de Janeiro. assessment of the diversity of New World primates. Simpson, G. G. 1941. Vernacular names of South American Neotrop. Primates 8(2):61–93. mammals. J. Mammal. 22(1): 1-17. Rylands, A. B., R. A. Mittermeier and J. e S. Silva Jr. 2012. Smith, G. A. and L. Bartlett. 2009. “A most unprovoked, Neotropical primates: taxonomy and recently described unwarrantable, and dastardly attack”: James Buchanan, species and subspecies. Int. Zoo Yearb. 46:11–24. Paraguay, and the Water Witch incident of 1855. The Saldívar, S., V. Rojas, D. Giménez, A. M. Abba, R. Ayala, Northern Mariner 19: 269–290. R. Barreto., J. L. Cartes, H. del Castillo, E. Cuéllar, N. Smith, R. 2017a. An observation of an unusual human- U. de la Sancha, I. Gamarra de Fox, A. J. Giordano, M. directed threat display by Sapajus cay Illiger, 1815
20 Paraguayan primatology
(Cebidae: Primates) in a fragment of Upper Paraná Thomas, O. 1907. On Neotropical mammals of the genera Atlantic Forest, eastern Paraguay. Mammal. Notes 4: Callicebus, Reithrodontomys, Ctenomys, Dasypus, and 5–6. Marmosa. Ann. Mag. Nat. Hist., ser. 7, 20: 161–168. Smith, R. 2017b. Preliminary observations of complex Torres, C. 1983. An Ecological Study of the Primates of object manipulation in a wild population of Sapajus cay Southeastern Brazil, with a Reappraisal of Cebus apella Illiger, 1815 (Primates: Cebidae) in a fragment of Upper Races. Ph.D. thesis, University of Edinburgh, Edin- Paraná Atlantic Forest, Rancho Laguna Blanca, eastern burgh, Scotland. Paraguay. Acta Ethol. 20: 75–80. Travi, B. L., O. J. Colillas, F. L. Segura and A. Schudel. Smith, R. and E. Briggs. 2015. Using camera traps to deter- 1982. Monos neotropicales: evaluación de su infección mine group demography in a Paraguayan population of natural por protozoarios y virus de importancia epide- Sapajus cay. Neotrop. Primates 22: 81–88. miológica. Veterinaria-Corrientes 7(4/5): 123–156. Smith, R. and C. J. Payne. 2017. Consumption of the bark of Van Roosmalen, M. G. M., T. van Roosmalen and R. A. Mit- Albizia niopoides (Mimosaceae) by Sapajus cay Illiger, termeier. 2002. A taxonomic review of the titi monkeys, 1815 (Cebidae: Primates) in the Atlantic Forest frag- genus Callicebus Thomas, 1903, with the description of ment of Rancho Laguna Blanca in eastern Paraguay. two new species, Callicebus bernhardi and Callicebus Mammal. Notes 4: 7–9. stephennashi, from Brazilian Amazonia. Neotrop. Pri- Smith, R. and J. G. Sarvary. 2017. ¡No soy mascota! (I am mates 10(Suppl.): 1–52. not a pet!). Fundación Para La Tierra, Paraguay. Velázquez, M. and F. Ramírez Pinto. 2014. Guía de los Smith, R., S. E. Hayes, P. Smith and J. Dickens. 2018. Sleep- Mamíferos de la Reserva Natural Tapytá. Fundación ing site preferences in Sapajus cay Illiger 1815 (Pri- Moises Bertoni, Asunción, Paraguay. mates: Cebidae) in an Atlantic Forest fragment, Rancho Vera de Bilbao, N. 2009. Investigaciones sobre la enferme- Laguna Blanca, eastern Paraguay. Primates 59: 79–88. dad de Chagas en el Departamento de Medicina Tro- Smith, R. L., E. Briggs and P. Smith. 2020. Unusual behav- pical del Instituto de Investigaciones en Ciencias de la ioural responses of the South American coati Nasua Salud. Aňo 1982–2009. A 100 años del Descubrimiento nasua (Carnivora: Procyonidae) to hooded capuchins de la Enfermedad de Chagas. Mem. Inst. Investig. Cienc. Sapajus cay (Primates: Cebidae) in the Paraguayan Salud 7: 65–69. Upper Paraná Atlantic Forest? Neotrop. Primates. Villalba, R. and A. Yanosky. 2000. Guía de Huellas y Seña- 26(3): 23–29. les: Fauna Paraguaya. Fundación Moises Bertoni, Soria, M. F. 1959. Otros casos de intrusión del vómer en el Asunción, Paraguay. género Cebus. Com. Mus. Argent. Cienc. Nat. “Bernar- Vinke, T. and S. Vinke. 2008. El Maravilloso Chaco Par- dino Rivadavia” 3: 131–144. aguayo. Imágenes e Informaciones sobre su Flora y Spix, J. B. von. 1823. Simiarum et Vespertilionum Brasi- Fauna. Dauvi-Verlag, Bergheim, Germany. liensum Species Novae: Ou Histoire Naturelle des Espe- Voigt, F. S. 1831. Der Saimiri. In: Das Thierreich, einge- cies Nouvelles de Singes et Chauves-souris Observées theilt nach dem Bau der Thiere als Grundlage ihrer et Recueilles Pendant le Voyage dans L´interieur de Naturgeschichte und der vergleichenden Anatomie von Bresil. Typis Francisi Serephici Hübschmanni, Monaco. den Hern Ritter von Cuvier. Erster Band. Säugethiere Stallings, J. and R. A. Mittermeier 1983. The black-tailed und Vögel, G. Cuvier (ed.), p.132. J. G. Cotta’schen marmoset Callithrix argentata melanura recorded from Buchandlung, Stuttgart und Tübingen, Germany. Paraguay. Am. J. Primatol. 4: 159–163. Wallace, R. B., H. Gómez, Z. R. Porcel and D. I. Rumiz. Stallings, J. R. 1984. Status and Conservation of Paraguayan 2010. Distribución, Ecología y Conservación de los Primates. M. A. Thesis, University of Florida, Gaines- Mamíferos Medianos y Grandes de Bolivia. Fundación ville, USA. Simón I. Patiño, Santa Cruz, Bolivia. Stallings, J. 1985. Distribution and status of Primates in Par- Wagner, J. A. 1842. Diagnosen neuer Arten brasilischer Säu- aguay. Primate Conserv. (6): 51–58. gethiere. Arch. Naturgeschichte 8: 356–362. Stallings, J. R., L. West, W. Hahn and I. M. Gamarra. 1989. Weiler, A., K. Núñez, S. Peris, F. Silla, K. Airaldi, G. Gon- Primates and their relation to habitat in the Paraguayan zález de Weston, F. Cubilla, P. Salinas, B. Zaldivar, E. Chaco. In: Advances in Neotropical Mammalogy, J. F. Valiente, K. Chavez, Y. Ramos and D. Tabilo. 2019. Eisenberg and K. H. Redford (eds.), pp.425–442. Sand- Guía para la Identificación de Mamíferos Medianos y hill Crane Press, Gainesville, FL. Grandes del Chaco Seco. Facultad de Ciencias Exac- Szapkievich, V. B., C. I. Comas, G. E. Zunino and M. D. tas y Naturales, Universidad Nacional de Asunción, San Mudry. 1998. Análisis de variabilidad proteica en Alou- Lorenzo, Paraguay. atta caraya y Cebus apella (Primates: Platyrrhini). Wellian, J. and R. L Smith. 2021. Risk awareness of black- Mastozool. Neotrop. 5: 53–59. &-gold howler monkeys (Alouatta caraya) living in Thomas, O. 1903. Notes on South American monkeys, bats, an urban environment in Pilar, Ñeembucú, south-west carnivores and rodents, with descriptions of new spe- Paraguay. In press. cies. Ann. Mag. Nat. Hist., ser. 7, 12: 455–464.
21 Smith et al.
Whitaker, J. O. and D. B. Abrell. 1987. Notes on some ecto- parasites from mammals of Paraguay. Entomol. News 98: 198–204. Wetzel, R. M. and J. W. Lovett. 1974. A collection of mam- mals from the Chaco of Paraguay. Univ. Connecticut Occas. Pap. Biol. Sci. 2(13): 203–216. Wright, P. C. 1983. Day-active night monkeys (Aotus trivir- gatus) in the Chaco of Paraguay. Am. J. Phys. Anthropol. 60: 272. Wright, P. C. 1989. The nocturnal primate niche in the New World. J. Hum. Evol. 18: 635–658. Wright, P. C. 1994. The behavior and ecology of the owl monkey. In: Aotus: The Owl Monkey, J. F. Baer, R. E. Weller and I. Kakoma (eds.), pp.97–112. Academic Press, San Diego, CA. Yahnke C. J., I. G. Fox and F. Colman. 1998. Mamma- lian species richness in Paraguay: the effectiveness of national parks in preserving biodiversity. Biol. Conserv. 84: 263–268. Ziegler, T., J. Unger, A. Feiler and E. Lehr. 2002. The first Gran Chaco Expedition of the Museum für Tierkunde Dresden: records of amphibians, reptiles and mammals from the Dry Chaco of Paraguay (Amphibia, Reptilia, Mammalia). Faun. Abh. Mus. Tierkd. Dresden 23: 219–238. Zunino, G. E. and M. D. Mudry. 1993. Estudio morfológico y cardiológico de las subespecies de Cebus apella del la Argentina. Bol. Primatol. Latinoam. 4(1): 9–13.
Authors’ addresses: Paul Smith, FAUNA Paraguay, Encarnación, Itapúa, Para- guay; Rebecca L. Smith, Para La Tierra, Centro IDEAL, Mariscal Estigarribia 321 c/ Tte. Capurro, Pilar, Departa- mento Ñeembucú, Paraguay; and Sergio D. Rios, Museo Nacional de Historia Natural del Paraguay, Sucursal 1 Campus., Central XI, San Lorenzo, Paraguay.
Corresponding author: Paul Smith e-mail:
Received for publication: 21 May 2020 Revised: 20 January 2021
22