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Introduction
Paraguay is a landlocked country nested among Argentina, Bolivia, and Brazil in the Southern Cone of South America. While its topography is generally flat, a few hills ranging from 50 m to a maximum of 759 m above sea level are located primarily in the eastern portion of the country (Gorham 1973; Bartrina 2007). Because of its geographic position in the middle of South America, several major biomes of the continent (Cerrado, Chaco, Pantanal, and Atlantic Forest) extend into Paraguay, resulting in a more diverse flora and fauna than expected given the country's relatively small area and shallow topographic relief.
Paraguayan borders are delineated mainly by rivers, including the Paraná, Pilcomayo, and Paraguay. The center of the country lies on the Tropic of Capricorn at the interface between temperate and tropical zones. Paraguay's climate is characterized as tropical continental with six regional climates (Fariña 1973) and follows a continuum from semiarid at the northwestern border, where rainfall averages around 400 mm annually, to semitropical in the southeast, where annual rainfall is around 1,800 mm. Average annual temperatures vary from 25.9 °C in the NW to 21.4 °C in the SE (Fariña 1973). The Paraguay River bisects the country from north to south into eastern and western regions that are distinctive geologically, ecologically, and faunistically (Myers 1982; Hayes 1995; Myers et al. 2002; López-González 2004).
Paraguay was the site of some of the earliest explorations of the Americas (Sainz Ollero et al. 1989), and it has played an important role in the history of South American mammalogy. The work of Félix de Azara (Azara 1801, 1802) supplied descriptions that are the basis of numerous currently recognized taxa, many of which are widely-distributed mammalian species. A total of six currently recognized marsupial (Gardner 2008a), two armadillo (Gardner 2008a), one felid, two canid (Wozencraft 2005), three primate (Groves 2005), two cervid (Grubb 2005), seven bat (López-González 2005; Simmons 2005), and 17 rodent species (Patton et al. 2015) have been described based on Paraguayan specimens.
Despite the long history of mammalogy in Paraguay, the country's mammal assemblage remains among the least studied in South America (Pine 1982; Myers et al. 2002). During the past 20 years, however, research on Paraguayan mammals has intensified (see a recent summary in López-González et al. 2014). A large number of species has been added recently to the Paraguayan fauna, information on species distributions has improved, and the natural history of some species is better known. In this work we provide an updated list of the mammals of Paraguay that reflects recent taxonomic advances and additions to the fauna.
Methods and Materials
Species list. We used the species list of Myers et al. (2002) as the starting point for a revised list of the mammalian fauna of the country. Because there was a delay of several years between the submission of the manuscript of Myers et al. (2002) and the actual publication of the work, papers published between 1997 and 2002 were not cited in that publication; therefore, those publications on species occurrences were included in this account. We used the list of Myers et al. (2002) instead of that of Rumbo (2010) because the latter is based mostly on a previous list by Gamarra de Fox and Martin (1996) with few additions. Similarly, the list by Neris (1998) only included records to 1993. Annotations to the list published here include new species records for the country (NSRC), taxonomic revisions and or nomenclature clarifications (TXNM), updated species distribution east or west of the Rio Paraguay (DIST), and subspecific status of populations when available (SSP).
A species was included in the list only if it could be traced to a published record associated with museum specimens, sequences, photographs, or other types of verifiable vouchers. Verification of literature records by actual examination of specimens (including photographs) is much needed but far beyond the scope of this report; it is our intent to provide a useful platform for such study. Nomenclature and taxonomic arrangement to subfamily level follows Wilson and Reeder (2005) with the following exceptions: for Cetar-tiodactyla we follow Agnarsson and May-Collado (2008) and Vislobokova (2013); for Cingulata, Gibb et al. (2016); and for Primates, Rylands and Mittermeier (2009). Genera and species are arranged in alphabetical order. Domestic or wild introduced species are not considered in the list.
Results
Updated checklist. Our search retrieved 181 native species of mammals (Table 1) that have been reported for Paraguay, representing 10 orders, 34 families, and 116 genera. The order Chiroptera was the most diverse (58 species), followed by Rodentia (56), Carnivora (20) and Didelphimorphia (18; Figure 1). At the family level, Cricetidae had the highest species richness (34), followed by Phyllostomidae (20), Didel-phidae (18), Molossidae (17), Vespertilionidae (16), Dasypo-didae (11), Felidae (8), Mustelidae (5), Echimyidae (5), and Cervidae (5; Figure 2). All other families were represented by four or fewer species. Three species, Ctenomys pilarensis, C. paraguayensis, and C. dorsalis are known only from Paraguay (Bidau 2015). Subspecific names were available for 69 species. We documented 59 taxonomic or nomenclatural changes at the species level since Myers et al. (2002).
Table 1 List of Paraguayan mammals to December 2016. Taxonomic arrangement to subfamily follows Wilson and Reeder (2005), except for Cetartiodactyla we follow Agnarsson and May-Collado (2008) and Vislobokova (2013); for Cingulata, Gibb et al. (2016); and for Primates, Rylands and Mittermeier (2009). Genera and species are arranged in alphabetical order within subfamilies. W, western Paraguay, E, Eastern Paraguay. Remarks on taxonomic and nomenclatural changes (TXNM), distributional changes post Myers et al. (2002) (DIST), and new species records (NSRC) since Myers et al. (2002) are included when applicable. SSP: subspecific epithet and reference of paper where the subspecies is recognized, PY: Paraguay.
Myers et al. (2002) reported 156 species in their account, but we could not confirm the presence of Bradypus varie-gatus, Monodelphis scalops, or Ctenomys boliviensis in Paraguay. M. scalops reported in Myers et al. is a misidentified M. brevicaudis = M. sorex (de la Sancha et al. 2007). Conepa-tus humboldti is now regarded as a synonym of C. chinga, both listed by Myers et al. (2002) as distinct species. The presence of Myotis levis was based on a report that was probably erroneous (Table 1). These changes reduced the list to 151 species. Here we document 30 additional species for the Paraguayan mammalian fauna (Table 1), either as new records or as populations formerly considered as one species but recently split into two, both occurring in Paraguay. Five of the additions are opossums, 10 are bats, 14 are rodents, and 1 is a carnivore. Three additional species, Anoura caudifer (López-González 2005), Dasypus septem-cinctus (Wetzel et al. 2008), and Calomys callidus (Salazar-Bravo 2015) have been reported for Paraguay but no unambiguous records of their presence are available (Griffiths and Gardner 2008; Salazar-Bravo 2015) and therefore they are not included in our list.
Geographic distribution. We document 27 changes that either expand or restrict the distributions of species in eastern and western Paraguay reported by Myers et al. (2002). Of the total 181 species reported (Table 1), 58 (32.0 %) have been found only east of the Río Paraguay, 35 (19.3 %) only west of the river, and 88 (48.6 %) on both sides. Most mammalian Families include more species east of the Rio Paraguay, but one third have more species west of the river (Emballonuri-dae, Molossidae, Dasypodidae, Sciuridae, Caviidae, Tayas-suidae, Camelidae, Callitrichidae, Aotidae, and Pitheciidae), although the difference in numbers between East and West assemblages is small (one or two species) within each of these families.
Discussion
Species richness. The first documentation of the Paraguayan mammal fauna dates to the earliest natural history explorations of South America in the 16th century (reviewed by López-González et al. 2014), yet the Paraguayan fauna is still one of the most poorly understood in South America. In recent years, however, investigations focusing on the biology of Paraguayan mammals have accelerated. The 151 species reported by Myers et al. (2002); sent to publication in 1997) increased to 167 in the list by Neris (1998), and to 181 in this account, an increase of 19.9 % from Myers et al. (2002) in less than 20 years. Species have been added due to new findings in the field, review of museum material, taxonomic revisions, and phylogenetic analyses (e. g, López-González et al. 1998; Willig et al. 2000; Voss et al. 2005, 2009; López-González 2005; Weksler and Bonvincino 2005; de la Sancha et al. 2007; D'Elía et al. 2008a, 2008b; Percequillo et al. 2008; de la Sancha et al. 2009; Voss et al. 2009; Stevens et al. 2010; de la Sancha et al. 2011 ; Bornholdt et al. 2013; de la Sancha 2014; González-Ittig et al. 2014; Moratelli and Wilson 2013; Owen et al. 2014; de la Sancha and D'Elía 2015; Moratelli et al. 2015; Timm et al. 2015; Pardiñas et al. 2016). The number of nomenclatural and taxonomic changes observed reflects an improving understanding of the diversity and phylogenetic relationships of the South American mammalian fauna in general, and the Paraguayan assemblage in particular. This body of work is improving our understanding of distributions at a finer scale for many species, particularly of small mammals, but less has been done on mid-size and large species. Continued field work, museum-based research, DNA barcoding, and raptor pellet examinations (i. e, Torres et al. 2014) likely will reveal the presence of undescribed species in the country as well as species currently known from adjacent areas of neighboring countries.
Probable species. Myers et al. (2002) reported the occurrence of Bradypus variegatus in Paraguay. Although it has been recorded from Misiones, Argentina (Gardner 2008b), and there are unconfirmed reports for Paraguay (Bertoni 1939), we are not aware of unequivocal evidence of its presence, although the species may occur, or may have occurred, in Paraguay. Anoura caudifer was included in the Paraguayan fauna by López-González (2005) based on a report by Pod-tiaguin (1944), but Griffiths and Gardner (2008) questioned this report, and no specimen of A. caudifer is available to confirm its presence in Paraguay. Salazar-Bravo (2015) reported Calomys callidus for Paraguay; although it is likely to occur in the humid Chaco following a distribution similar to that of several marsupials (de la Sancha and D'Elía 2015), we found no published evidence of its occurrence in Paraguay. Ctenomys boliviensis was included in Myers et al. (2002), but the only available records for the species are from the area around Santa Cruz, Bolivia (Bidau 2015).
Leopardus guttulus was reported by Johnson et al. (1999) and Trigo et al. (2008) to occur in the Paraguayan Chaco. However, a closer examination of their specimen lists raises doubts about the distribution of this species. Figure 1 in Johnson et al. (1999) includes a locality in the Chaco. In their list of examined material (Appendix 1) these authors report a sample (LTI 37) from Iguazu Paraguay, referring to the source of the sample as "Itaipu Paraguay." They also list a sample (LTI 38) from "Curuguaty, W. Paraguay," referring the source of the sample to"Itaipu Paraguay"as well. Iguazu is not in Paraguay and Curuguaty is not in Western Paraguay, making it impossible to determine where their samples came from. In their Figure 1A, Trigo et al. (2008) suggest the species is only found in Eastern Paraguay, but in their Figure 1B they report a site in the Paraguayan Chaco. Furthermore, in their Supporting Material, they state that the geographic origin of their sample is the Paraguayan Chaco. Because of these apparently conflicting reports, we list L. guttulus only for Eastern Paraguay but recognize that its distribution is poorly known and may eventually be shown to include Chacoan sites.
Dasypus septemcinctus has been reported to occur in Paraguay (Wetzel et al. 2008) but no specimen records were presented by those authors. We were unable to find other published records of this species and thus do not include it in Table 1.
Current knowledge of major mammalian groups
Didelphimorphia. Recent works have incorporated both morphological and genetic evidence to improve our understanding of the distribution and systematics of Paraguayan marsupials (Voss et al. 2005; de la Sancha et al. 2007; Teta et al. 2009; Voss et al. 2009; de la Sancha et al. 2012; Smith et al. 2012; Martínez-Lanfranco et al. 2014; Smith and Owen 2015; de la Sancha and D'Elia 2015). Five species of marsupials have been reported for Paraguay for the first time since 2005. Nonetheless, major gaps remain in our understanding of the natural history and ecology of Paraguayan marsupials.
Cingulata. Much of our understanding of the armadillo species present in Paraguay is based on the works of Wetzel (1980, 1985). Only one study has incorporated molecular data from Paraguayan populations (Frutos and Van Den Bussche 2002), and few investigations have addressed geographic distribution or conservation, a pressing concern given that armadillos are hunted for food (Smith et al. 2011; Weiler and Núnez 2012). Ecology, phylogenetics, conservation, and management themes provide valuable research opportunities for this group in Paraguay.
Pilosa. To our knowledge, no publication has focused exclusively on Paraguayan anteaters, even though they are common throughout the country. Research on distribution, ecology and natural history is urgently needed because of the extensive habitat conversion and loss currently occurring in Paraguay.
Primates. The taxonomy of Neotropical primates has changed considerably in the past few years, reflecting current research efforts focusing on the group across the South American continent. Although Paraguayan specimens have been used in regional studies including morphology (Aristide et al. 2014), genetics (Matayoshi et al. 1986; Mudry et al. 1987; Pargament and Slavutsky 1987; Martinez et al. 2004; Mudry et al. 2007; Casado et al. 2010), phylogenetics and phylogeography (Hoyos et al. 2016), ecology (Boyle 2014) and zoonosis (Diaz et al. 2007), little research has been done on this group within Paraguay; the few works available focus on rare or uncommon species such as Mico melanurus (Stallings and Mittermeier 1983), Aotus azarae (Campos et al. 2004), and on the more common Alouatta caraya (Giordano and Ballard 2010). Conservation status of primates in Paraguay was assessed by Stallings (1985) and Rumiz and Stallings (1989) and has not been revised since. Given the current rate of habitat loss, this charismatic fauna should be the focus of ecological and conservation studies.
Lagomorpha. Information on Paraguayan lagomorphs is scarce. The taxonomy of the Paraguayan populations is still unclear at best given that Sylvilagus brasiliensis is probably a species complex (Bonvicino et al. 2015) and is in need of revision. We found no literature focused on the biology of S. brasiliensis in Paraguay even though it is a common species throughout the country.
Chiroptera. Bats, with a total of 58 species, are the most species-rich order in Paraguay. López-Gonzalez (2005) summarized knowledge before 2000 of Paraguayan Chiroptera, listing 54 species based on specimens collected and deposited in collections. Since then, Myotis levis (Stevens et al. 2010), M. midastactus and Myotis "simus-like" (Moratelli et al. 2015), Saccopteryx leptura, and Gardnerycteris crenulatum (Owen et al. 2014) have been added to Paraguay's fauna, while Anoura caudifer has been removed from the list (see above). The inventory of bats is likely to grow as further field and revisionary research is conducted.
Recent non-taxonomic bat research in Paraguay has focused mainly on community ecology (Stevens et al. 2004; Gorresen et al. 2005; Presley 2007; Stevens et al. 2007; Presley et al. 2009; Presley 2012; Stevens and Amarilla-Stevens 2012), on relationships of bats with their ectobionts (Durette-Dusset and Vaucher 1999; Dick and Gettinger 2005; Graciolli et al. 2006; Heddergott 2008; Presley and Willig 2008), ecological biogeography (López-González 2004; Stevens et al. 2007), and conservation issues (Andelman and Willig 2002; Gorresen and Willig 2004). Little has been done on the natural history and ecology of individual species or Paraguayan populations with few exceptions (Stevens 2001; McCulloch and Stevens 2011 ; McCulloch et al. 2013; Stevens et al. 2016).
Carnivora. Paraguay is home to 20 species of carnivores, all occurring on both sides of the Rio Paraguay with the possible exceptions of Leopardus guttulus (see above) and Galictis vittata (see details Table 1). A finer scale analysis is needed to ascertain the specific habitats or bioregions that these organisms occupy. Additionally, their ecology and natural history in Paraguay has not been explored, and a number of taxonomic and nomenclatural issues have yet to be resolved. Considering that many medium and large-sized carnivores are highly charismatic it is surprising to find so little research has been done on them.
Most studies on felids have focused primarily on jaguars and pumas (Taber et al. 1997; de Angelo et al. 2011a, 2011b; Giordano et al. 2014). Studies of other cats include only a few notes on medium sized species (Zuercher et al. 2001). For canids, there are few taxon-specific publications. Descriptive and conservation-related work is available for Chrysocyon brachyurus (Meritt 1973; Queirolo et al. 2011 ; Cartes et al. 2015). Ironically the most elusive canid in Paraguay, Speothos venaticus, is the best studied (Zuercher and Villalba 2002; Zuercher et al. 2003,2005). Nonetheless, basic taxonomic, ecological, and distributional issues are yet to be resolved for Paraguayan populations of the bush dog. Beyond lists or locality records, studies of mustelids, mephitids, and procyonids are essentially non-existent. Carnivores in general represent a major knowledge gap in Paraguay and offer scientists a great opportunity for study.
Cetartiodactyla. Most of the nine species that occur in Paraguay are found on both sides of the Rio Paraguay, with the exception of Parachoerus wagneri and Lama guanicoe, both restricted to Western Paraguay, and Mazama nana, which is restricted to Eastern Paraguay. Until 1975, Parachoerus wagneri was known only from the fossil record; the discovery of this "living fossil" (Wetzel et al. 1975) precipitated a massive effort to document the biology of this species (Wetzel et al. 1975; Mayer and Brandt 1982; Benirschke et al. 1985; Mayer and Wetzel 1986; Byrd et al. 1988; Benirschke et al. 1989a, 1989b; Taber 1990; Handen and Benirschke 1991; Taber 1991; Brooks 1992; Taber 1993; Handen et al. 1994; Taber et al. 1993, 1994; Yahnke et al. 1997; Toone and Wallace 2002; Toone et al. 2003; Sutherland-Smith et al. 2004; Meritt 2010). Studies of other ungulates in Paraguay, however, have lagged far behind, and those species are known primarily from lists or reports of sightings. Of the five species of Paraguayan deer, only Mazama gouazoubira has been studied ecologically (Stallings 1984, 1986) whereas the guanaco (Lama guanicoae) is only known from a few sightings (Villalba and Bonacic 2006). Even the taxonomy of populations of common, medium-sized species like Mazama americana is uncertain in Paraguay. The name M. americana currently applies to populations of northern South America (Groves and Grubb 2011). The names M. rufa and M. jucunda are available for the Paraguayan populations (Groves and Grubb 2011), but no decision as to which applies is possible without revision of the pertinent materials. Here, we have opted to be conservative and kept the name Mazama sp. for Paraguayan populations of this species until such revision is available.
Perissodactyla. The few publications concerning Paraguayan tapirs deal with their use by indigenous people (Hill et al. 1997; Hill and Padwe 2000; Hill et al. 2003) and the effects that habitat changes are having on this species (Brooks et al. 1997). Many habitats in Paraguay have changed considerably since the late 1990s and therefore, this report is likely outdated. Paraguay is a potential contact zone for T. terrestris terrestris and T. t. spegazzinii; however, to date only T. t. terrestris is confirmed for the country (Groves and Grubb 2011). The possible occurrence of T. t. spegazzinii is currently an open research opportunity with taxonomic and population genetic implications.
Rodentia. Rodents are the most diverse order of mammals in the world (Carleton and Musser 2005). They comprise close to 50 % of the mammal species in Central and South America (Patton et al. 2015), yet in Paraguay they appear to be somewhat less diverse than bats. We suggest that the apparent under-representation of rodents (or over-representation of bats) in the Paraguayan fauna is an artifact of inadequate sampling and lack of taxonomic study. Remarkably, since 2005 a new Family (Sciuridae), three genera (Sciurus, Bibimys, Juliomys) and 13 species of rodents (Table 1) have been reported for Paraguay for the first time. Many rodent groups continue to receive scant attention from sys-tematists, and future taxonomic revisions are likely to result in the proportion of rodents in the Paraguayan fauna more closely reflecting proportions in faunas elsewhere.
A better understanding of the rodent fauna of Paraguay is critical. Rodents and other small mammals play important ecological roles, including seed predators, consumers of insects including possible crop pests, and as prey base for a large community of mammalian, avian and reptilian predators. They are valuable in ecological studies, including those concerning anthropogenic disturbance such as landscape and climate change (de la Sancha 2014; de la Sancha et al. 2014). Rodents are also important hosts for human pathogens, including hantaviruses, which are known from Paraguay (Yahnke et al. 2001; Chu et al. 2003,2006; Goodin et al. 2006; Padula et al. 2007; Chu et al. 2009; Goodin et al. 2009). Studies dealing with population dynamics of rodents in Paraguay have been severely handicapped by lack of field identification tools; reliable keys and much more basic work are still needed in Paraguay.
Our review of publications in the preparation of Table 1 revealed the following major trends:
Most publications are still fundamentally descriptive works, mostly taxonomic and distributional. Chiroptera, Didelphimorphia, and Rodentia are the most-studied taxa, but research efforts even within these groups have focused on a few species and mostly on distributional, taxonomic, and systematic issues. Other aspects of the Paraguayan mammalian fauna are very poorly studied.
The basic taxonomy of many medium-sized and large mammal species is poorly understood at best. Few Paraguayan specimens of most medium-sized and large species are available, and because many of these animals are threatened or endangered, further collection of samples is expected to be limited. However, as new sampling methods are devised and processing costs decrease with the application of new molecular techniques, non-lethal sampling is becoming more effective and affordable. Also, developments in tracking technology and camera trapping make possible new kinds of studies of natural history and distribution. Many opportunities for work on larger mammals exist, and this kind of research is urgently needed.
Our inventory of Paraguayan mammals is likely incomplete, as is our knowledge of species distributional limits within Paraguay. Particularly for rodents, no comprehensive review is available, and field identifications are problematic. Considerable collections already exist in several museums across the world, but critical study of many of these specimens, further collection of selected species, and surveys of critical areas remain to be done. DNA barcoding will play a role, but the usefulness of this technique rests on the association of tissue samples with properly identified, well curated, and accessible vouchers.
Very few studies at the population, community or metacommunity levels are available. Conservation assessment and management strategies exist only for a handful of species or for restricted protected areas. Conservation-oriented research is urgent given the accelerated rate of environmental modification currently affecting Paraguay.
Paraguay is located in the heart of South America and at the intersection of several major South American ecore-gions. Yet, for many biological groups, Paraguay represents a knowledge gap between Brazil, Argentina, and Bolivia. Further local and regional research will narrow this gap, thus providing better understanding of large-scale biogeo-graphical and evolutionary processes. For instance, there is still much to understand about the role of the Rio Paraguay as a dispersal filter or barrier between major biomes, not only within Paraguay but at a larger scale.
Improved understanding of the Paraguayan fauna is vital to understand the impacts of anthropogenic changes.
We conclude that the current status of knowledge on Paraguayan mammals is incomplete and offers a fertile ground for young scientists, offering many valuable and interesting taxonomic, biogeographic, and ecologic questions yet to be resolved.
