Non-volant mammals from the protected areas associated to hydroelectric projects on the eastern slope of the northern Cordillera Central , Colombia

The northern part of the Cordillera Central in Colombia has been recognized as a region of particular relevancy in vertebrates biodiversity. We provide a list of non-volant mammal species in Jaguas and San Carlos, two protected areas around hydroelectric projects on the eastern slope of the Cordillera Central in Antioquia. As part of an ongoing monitoring project, we obtained records from a standardized survey in 2011 and sporadic surveys in 2014–2015 (capture and non-invasive methods), and from the revision of voucher specimens. From 132 records we generated a list of 34 species, 22 species in Jaguas and 27 in San Carlos, belonging to 20 families and seven orders. We record the occurrence of four endemic and four threatened species, including the endemic and Endangered Tamarin, Saguinus leucopus, highlighting the importance of these protected areas for mammal conservation in this highly diverse region.


INTRODUCTION
Power generation in Colombia relies heavily on generation from hydroelectric dams.Currently, 24 active hydroelectric projects and at least five more in construction represent nearly 64% of the generated electricity in the country (Palacios 2013;UPME 2013).Over the last decade, continued biodiversity studies associated with hydroelectric power projects have indirectly become an important and alternative means for obtaining biodiversity data on flora and vertebrate fauna in some regions of the country (e.g., Cardona et al. 2010Cardona et al. , 2011;;Andrade et al. 2013;Cuartas-Calle & Marín 2014;Jiménez-Segura et al. 2014;Pareja-Carmona & Ospina-Pabón 2014;Peña & Quirama 2014).Often, hydroelectric projects are located in understudied areas with expansive natural habitat of high conservation value.Colombia is one of the countries in the Neotropical Region with the greatest number of environmental studies associated with the development of hydroelectric projects.However, about half of these studies remain available only as unpublished reports (Jiménez-Segura et al. 2014).Therefore, the access and use of biological information for management and conservation and by the academic community is limited.
The eastern flank of the northern Cordillera Central (between 06°11′ N and 06°27′ N) holds one of the main hydroelectric power complexes in the country with five operational hydroelectric plants (Palacios 2013).Altogether, this system maintains an important area in a highly fragmented landscape with over 8,000 ha of protected forest covering a wide elevational range (400-1,800 m) and several life zones (Cardona et al. 2011).The northern Cordillera Central is recognized as a region with high biogeographic value because of the confluence of biological elements from different areas (e.g., Chocó, Central America, and inter-Andean valleys), resulting in high levels of richness and endemism of plants and vertebrates (Kattan & Franco 2004;Kattan et al. 2004;Cuervo et al. 2008aCuervo et al. , 2008b;;Idárraga & Callejas 2011).Likewise, during the last decade the discovery of 10 new species, including birds, frogs, snakes and lizards, have come from this region (Cuervo et al. 2001;Passos et al. 2009;Bravo-Valencia & Rivera-Correa 2011;Velasco et al. 2010;Rivera-Correa & Gutierrez-Cárdenas 2012;Rivera-Correa & Faivovich 2013;Rivera-Prieto et al. 2014).
The northern part of the Cordillera Central has been the focus of mammalian studies since the early 1900s (Allen 1916;Patterson 1987;Sánchez-Giraldo & Díaz-Nieto 2015).Recent survey efforts have significantly improved the species lists for several sites, finding new populations of threatened and endemic species from Colombia, and complex taxonomic entities (e.g., Castaño & Corrales 2010;Díaz-N et al. 2011;Sánchez-Giraldo & Díaz-Nieto 2015).Nonetheless, large portions of the region have not yet surveyed, or surveys have been sporadic and scattered; information on mammal diversity is incomplete (Sánchez-Giraldo & Díaz-Nieto 2015).For the area on the eastern slope of the Cordillera Central holding hydroelectric power complex, check lists of mammal species are based mainly on literature reviews, sparse specimen collections, and focus mostly on bats (e.g., Cuartas-Calle & Muñoz-Arango 2003;Navarro et al. 2005).
Over the last decade, as part of a mammal monitoring program, intensive fieldwork has been conducted in the protected areas of two hydroelectric power plants in the northeastern Cordillera Central (ISAGEN S.A. 2007(ISAGEN S.A. , 2008a(ISAGEN S.A. , 2009)).Even though these studies have produced important sources of information, and start to fill the knowledge gap of mammals in the region, they are unpublished.Here, we update the knowledge of the species richness and distribution of the mammal fauna on this region.We provide a taxonomic list for non-volant mammal species in the pro-tected areas of Jaguas and San Carlos hydroelectric power plants.We compile data from previous studies supported by museum specimens and from our own recent surveys.

Study sites
We conducted the study in the protected areas of the Jaguas and San Carlos hydroelectric power plants (ISAGEN S.A.) on the eastern slope of the northern Cordillera Central, Department of Antioquia, Colombia (Figure 1).Areas in both hydroelectric plants are privately protected areas since mid-1980s and recently they have been declared as Regional Forest Reserves (Cardona et al. 2011).The protected area at Jaguas hydroelectric plant (within 06°26′ N, 075°05′ W; 06°21′ N, 074°59′ W) covers ca.50 km 2 and includes the San Lorenzo reservoir (10.2 km 2 ).The area is classified as Premontane Wet Forest (bmh-PM), with an elevation range between 1,100 of on sand banks and watercourses margins.For each record, we collected data of specific locality, geographic coordinates, and photographic material whenever possible.We used specialized field guides for identification of signs (Emmons & Feer 1999;Defler 2003;Aranda 2012).
In addition to field observations, we reviewed the voucher specimens deposited at the Colección Teriológica Universidad de Antioquia, Medellín, Colombia (CTUA).Most of the examined material was collected between 2006 and 2009 during surveys of terrestrial vertebrate fauna in the protected areas of Jaguas and San Carlos hydroelectric plants.We recovered the specific locality information, geographic coordinates and checked the taxonomic identification for all examined specimens.We followed the taxonomic nomenclature by Wilson & Reeder (2005) for those taxonomically stabile species.Additionally, for specific nomenclature, we followed Patton et al. (2015) for rodents, Voss & Jansa (2009) and Rossi et al. (2010) for some marsupials, and Ryland & Mittermeier (2009) and Rylands et al. (2013Rylands et al. ( , 2016) ) for primates (Table 1; Table A1).

RESULTS
We obtained 132 records (52 in Jaguas and 80 in San Carlos) from 49 specific sites; of these, 20 were from newly collected specimens, 56 were direct observations, one was photo-trapped, one was a carcass, 19 were based on footprints, and 35 were museum specimens (Table 1; Appendices 1 and 2).The record from photo-trapping was provided by Faunativa S.A.S. as a result of an occasional survey with camera-traps carried out in Jaguas power plant in 2014.In total from both hydroelectric plants, we recorded the occurrence of 34 species of non-volant mammals belonging to seven orders and 20 families (Table 1; Figures 2, 3).One species, Black Rat [Rattus rattus (Linnaeus, 1758)] is exotic.The greatest number of species recorded belonged to the orders Rodentia and Carnivora, with 14 and eight species respectively.The orders Primates and Didelphimorphia had four species each, followed by Pilosa with two, and Cingulata and Artiodactyla with one species each (Table 1).We recorded most of the species from primary sources: 19 species from capture and museum vouchers, 13 from direct observations, one from photo-trapping [Puma yagouaroundi (É.Geoffroy Saint-Hilaire, 1803)], and one exclusively from carcasses (Dasypus novemcinctus Linnaeus, 1758) (Table 1).
In Jaguas, we found records of 22 species from 20 localities covering an elevational range of 1,000 to 1,400 m, and in the case of San Carlos we recorded 27 species from 29 localities between 600 to 1,150 m (Table 1; Appendix 1).Rodentia and Carnivora had the highest richness at both study areas, with 11 and five species in Jaguas, and 11 and six species (respectively) in San Carlos.Didelphimorphia also reached a high representation with four species in Jaguas (Table 1; Figure 2).Species of Cingulata, Pilosa and Artiodactyla were not recorded in Jaguas.Fifteen spe-1,300 m (above sea level), an annual average temperature between 18-24 °C, and annual rainfall from 2,000-4,000 mm (Holdridge 1964).San Carlos hydroelectric plant (06°16′ N, 074°55′ W; 06°12′ N, 074°49′ W) has a protected area of 30 km 2 , with Punchiná reservoir covering ca.3.3 km 2 (Figure 1).The San Carlos area has an elevational gradient from 400 to 1,100 m and is mostly Tropical West Forest (bh-T), with a zone of warm transition to Premontane Wet Forest (bmh-PM), characterized by annual rainfall of 2,000-4,000 mm and annual average temperature exceeding 24 °C (Holdridge 1964).Vegetation cover in the two protected areas includes different successional states of secondary forest, shrubs and bushes, and small areas used for agricultural and cattle activities (Cardona et al. 2011) (Figure 1).

Data collection
We obtained records of non-volant mammal species in both hydroelectric plants from fieldwork and the revision of voucher specimens.Fieldwork was conducted in two periods: (1) a standardized survey during 2011, and (2) several sporadic surveys between 2014 and 2015.The 2011 survey included the capture of small mammal species (marsupials and rodents) and the collection of data by noninvasive methods, including opportunistic observations and the search of footprints, feces and carcasses.Surveys in 2014 and 2015 only used non-invasive methods.The 2011 survey was conducted in four sampling periods: 1) 26 March-11 April, 2) 8-22 June, 3) 29 September-13 October, and 4) 17 November-1 December in Jaguas; and 1) 14-28 April, 2) 30 June-14 July, 3) 7-23 September, and 4) 6-20 December in San Carlos.The sampling included 12 localities in Jaguas and 16 in San Carlos (Figure 1).The 2014-2015 survey included three occasional sampling periods (May and October of 2014, andMarch 2015) only in San Carlos.
We used large Sherman (H.B.Sherman Traps, Tallahassee, USA) folding live traps (ca.8 × 9 × 23 cm) to capture small species in different vegetation types.Traps were placed in single stations ca. 10 m apart from each another, following a transect arrangement (Pearson & Ruggiero 2003), and baited every morning during the sampling days with a mixture of peanut, rolled oats and vanilla essence.We sampled 47 nights in Jaguas and 52 in San Carlos, representing a total sampling effort of 940 and 1,040 trapnights, respectively.We recorded standard measurements from each captured individual, and collected reference material preserved as fluid and dry specimens (following Hall 1962).All procedures were conducted under permit No. 112-0046 granted by the local environmental authority, Corporación Autónoma Regional CORNARE.The collected material is deposited in the Colección Teriológica Universidad de Antioquia (CTUA), Medellín, Colombia (Appendix 2).
Direct observations of individuals were obtained during opportunistic walks of transects following paths and dirt roads available within each study area.We searched for footprints, feces and carcasses along these transects and cies-two didelphids, three carnivores, two primates and eight rodents-were common to both study areas; and seven and 12 species were recorded only in Jaguas and San Carlos, respectively (Table 1).
Among the 33 native species listed here, four species are endemic to Colombia: the primates Saguinus leucopus (Günther, 1877) and Cebus versicolor Pucheran, 1845, and the rodents Nectomys grandis Thomas, 1897 and Proechimys chrysaeolus (Thomas, 1898) (Figures 2,3).Saguinus leucopus has the smallest distribution among all Saguinus species.Its distribution ranges from the confluence of the Magdalena and Cauca rivers in the north, southward on the Cordillera Central between the eastern bank of the lower Cauca River and the western bank of the middle Magdalena River, to elevation of 1,500 m (Defler 2010).Cebus versicolor populations inhabit the middle Magdalena valley from southern department of Magdalena to department of Tolima (Defler 2010;Rylands et al. 2013).Nectomys grandis is found in the north-central part of the country throughout the basins of the Magdalena and Cauca rivers, between 0 and 2,000 m (Patton et al. 2015).Lastly, the known localities for P. chrysaeolus are found from the Caribbean coast into the lower Cauca and Magdalena valleys, including the departments of Antioquia, Bolívar, Boy-

Species accounts
We list basic information for each recorded species and provide a brief diagnosis for those difficult-to-identify species.tling of the distal portion, gray-based ventral pelage and longer ears (Gardner & Creighton 2008).However, both species show significant geographic variation in some of these characters, becoming extremely similar in some areas of sympatry (Patton et al. 2000).
According to Gardner & Creighton (2008), the most consistent external character useful to distinguished M. demerarae from M. regina is the extent of the long pelage on the base of the tail, which extends beyond 30 mm in M. demerarae and usually cover less than 25 mm in the latter.We assigned all specimens from study area to M. demerarae considering their characteristic morphological pattern of the tail, including a tip white and mottle distally, and long fur extending above 35 mm.Future studies delimiting the variation of M. demerarae in our study area and this region of the Cordillera Central are necessary.Goldman, 1912 Figures 2, 4 In contrast to species of Marmosa (Micoureus), adult members of Marmosa (Marmosa) have brown or reddishbrown dorsal pelage, tail often lacking of white tip, and longer dense fur on the base of tail extending only for 15 mm or less (Creighton & Gardner 2008).Marmosa (Marmosa) isthmica could be confused with M. (Marmosa) robinsoni, a species with similar body size and morphological aspect with which could overlap potentially its range in the inter-Andean valley of the Magdalena River.Specimens examined from the study area have consistently a welldeveloped and distinct postorbital process and absence of palatine fenestrae, which are diagnostic characters of M. isthmica (Rossi et al. 2010).

Material examined: Appendix 2.
Heteromys anomalus has a large, elongated and robust skull, with a narrow, flat and strongly ridged braincase, which contrasts with the shorter and relatively broader skull and the wide and inflated braincase of similar species H. australis (Anderson 1999(Anderson , 2003)).Heteromys anomalus can be distinguished from H. australis by more robust zygomatic arches, masseter-temporal fossae well excavated, and an interorbital region strongly constricted (Anderson 1999(Anderson , 2003)).Specimens from the study area conform to the diagnostic characters described above, and have the typical well excavated masseter-temporal fossae.(Linnaeus, 1758) Mus rattus Linnaeus (1758): 61. -Musser & Carleton (2005):
Handleyomys alfaroi (J.A. Allen, 1891) Figures 3, 4 Material examined: Appendix 2. Weksler (2015) included provisionally alfaroi (member of "alfaroi group") as a member of Handleyomys.Handleyomys alfaroi is morphologically similar and become confused with oryzomyine species Transandinomys talamancae, with which overlap partially its distributional range (Musser et al. 1998).Handleyomys alfaroi differs from T. talamancae by having less body size, shorter length of molar row (range: 3.8-4.2mm), and longer incisive foramina relative to length of skull (see Musser et al. 1998: 165, fig. 72).Cranially, both species differ consistently in the occlusal surface patterns of second upper and lower molars.Second upper molars of H. alfaroi exhibit a medial fossete and shorter paraflexus, and second lower molars have a shorter hypo-flexid and conspicuous fossetid; in contrast, T. talamancae lacks of a medial fossete and fossetid, and exhibits larger paraflexus, and deep hypoflexid (Musser et al. 1998).
Material examined from the study area was previously assigned to T. talamancae; however, it exhibits the diagnostic features of H. alfaroi.It has characteristic occlusal pattern in second molars, and reaches length of molar row below 4.2 mm (3.8-4.0 mm).(Tomes, 1860) Figure 3 Hesperomys caliginosus Tomes ( 1860 Thomas, 1900 Figure 3 Neacomys spinosus tenuipes Thomas (1900) Material examined: Appendix 2. Specimens of this species normally lack a dark mid-dorsal stripe on the dorsal pelage, and cranially are recognized mainly by exhibiting a skull uniformly convex, markedly different from other congeneric species that have frontally flattened skulls (Bonvicino & Weksler 2015).The skull is heavy with upper profile evenly convex throughout, and frontal and parietal regions swollen (Bonvicino & Weksler 2015).Additionally, it has incisive foramina widely opened, with parallel sides, and rounded at both ends; posterior palate with large and deep lateral pits; and palatal margin of the mesopterygoid fossa squared.Specimens examined by us exhibited consistently a skull uniformly convex.(Tomes, 1860) Figures 3, 4 Hesperomys latimanus Tomes (1860): 213. -Tribe (2015): 599.
Sigmodon hirsutus is recognizable from other congeneric species in Colombia by its long nasal bones (which conceal the upper incisors from dorsal view) and narrow, ungrooved and strongly opisthodont upper incisors (Voss 1992(Voss , 2015b)).Likewise, S. hirsutus has a broad interorbital region, long incisive foramina, posterior palatal foramina usually enclosed by the palatine bones, and broad and long palatal bridge without conspicuous longitudinal grooves (Voss 1992(Voss , 2015b)).Specimens examined from study area conform to above diagnostic characters.Thomas, 1899 Tylomys mirae Thomas ( 1899  Material examined: Appendix 2.

Tylomys mirae
Zygodontmys brevicauda is distinguished from Z. brunneus, with which occurs sympatrically in some regions of Magdalena Valley, by differences in molar and cranial characters.Molars of Z. brevicauda are less hypsodont, and upper molars have a simpler occlusal architecture with principal cusps symmetrically disposed in opposite labiallingual pairs, and less oblique mures and murids (overall aspect of orthogonality); upper incisors are more opisthodont (Voss 1991).Zygodontmys brevicauda exhibits also deeper zygomatic notches, and more inflated nasolacrimal capsules (Voss 1991).Additionally, populations of Z. brevicauda in the upper Magdalena Valley have lower measures of length of hind foot (< 28 mm) and length upper molars (< 4.5 mm) (Voss 2015a).Specimens from the study area conform to the occlusal architecture of upper molars and cranial characters, and to the measurements (length of hind foot: 23.3 and 24.3 mm; length upper molars: 3.96-4.13mm) of Z. brevicauda.(Linnaeus, 1766) Figure 3 Mus paca Linnaeus ( 1766 Material examined and records: Appendixes 2 and 3.
According to Patton (1987), P. chrysaeolus is the most distinctive species within trinitatis group, exhibiting consistency in morphological characters associated to incisive foramina and counterfold pattern of the cheek teeth.Specimens of P. chrysaeolus possess an oval to teardrop-shape incisive foramine with weakly posterolateral flanges, which extend onto the anterior palate; counterfold pattern of the all maxillary cheek teeth have consistently three folds (3-3-3-3), and mandibular check teeth varying slightly: mp4 usually with three folds, m1 always with three folds, and m2 and m3 with two or three folds (Patton & Leite 2015).Specimens from the study area exhibit the folds distribution, occlusal architecture of upper and lower toothrows (see Patton 1987: fig. 30), and incisive foramine morphology characteristic of the species.

DISCUSSION
Mammal diversity studies with broad multi-taxa efforts are few in the northern Cordillera Central (e.g., Castaño & Corrales 2010;Escobar-Lasso et al. 2013;Cuartas-Calle & Marín 2014).Available mammal checklists for the region where our study area is located include 36 to 39 non-volant mammal species of eight orders (Cuartas-Calle & Muñoz-Arango 2003;Navarro et al. 2005).Jaguas and San Carlos reach richness values similar to that of the region, with 33 native species and seven orders, even though we did not record 13 species.No species recorded in Jaguas and San Carlos belong to the genera Caluromys, Philander, Chironectes, Cyclopes, Cabassous, Bradypus, Ateles, Mustela, Galictis, Leopardus, Microsciurus, Coendou, and Sylvilagus.In comparison to specific localities on the eastern slope with similar elevational ranges (400-1,200 m) and life zones (bh-T, bp-PM, bh-PM), Jaguas (22 species and five orders) and San Carlos (27 species and seven orders) reached a comparable composition of taxonomic orders and similar or lower values of species richness.Localities in the Río La Miel basin recorded between 21 and 26 species and six and seven orders (ISAGEN S.A. 2008b;Castaño & Corrales 2010), and in the Río Porce basin were recorded 47 species and eight orders (Cuartas-Calle & Marín 2014).Except for the order Lagomorpha, the mammal communities in Jaguas and San Carlos included all orders found in the La Miel and Porce river basins.
Records from 2006-2009 surveys of the terrestrial fauna of Jaguas and San Carlos have been previously published on the digital platform SIB (Sistema de información en Biodiversidad) Colombia (ISAGEN S.A. 2007(ISAGEN S.A. , 2008a(ISAGEN S.A. , 2009)).According to these data, in Jaguas and San Carlos were recorded 36 and 38 species of non-volant mammals distributed in seven orders (Table A1).We found museum vouchers for 19 species (11 species in Jaguas and 13 in San Carlos) collected during 2006-2009 surveys, which included 13 rodents, four marsupials, and large mammals such as Pecari tajacu (Linnaeus, 1758) and Puma concolor (Linnaeus, 1771) (Table 1; Table A1).However, for 13 of the species in the SIB platform, and not recorded in our surveys between 2011 and 2015, no reference material was found (Table A1).We did not include these records due to the unavailability of reference material and the inability to confirm their identifications.Some of these records were incompletely identified or are small rodents and didelphids, whose taxonomic assignment could be doubtful.
Non-volant mammal communities of Jaguas and San Carlos had similar species composition, with 15 species common to both (Table 1).Eight of them are considered common and widespread species (i.e., Didelphis marsupialis, Cerdocyon thous, Notosciurus granatensis, Cuniculus paca and Dasyprocta punctata), while the remaining correspond to exclusively species distributed either along the Cauca and Magdalena inter-Andean valleys and the Caribbean region (i.e., Aotus griseimembra Elliot, 1912 and Zygodontomys brevicauda J.A. Allen & Chapman, 1893), or are endemic to Colombia (i.e., Saguinus leucopus and Nectomys grandis) (Solari et al. 2013) (Table 1).Among the 19 species recorded in only one of the hydroelectric plants (seven in Jaguas and 12 species in San Carlos), 13 also have wide distributional ranges and occur between lowlands and areas above 1,500 (Solari et al. 2013), so they could be present in both study areas.Proechimys chrysaeolus, Tylomys mirae Thomas, 1899, and Sigmodon hirsutus (Burmeister, 1854) found in San Carlos are associated with typical lowlands assemblages (Solari et al. 2013;Sánchez-Giraldo & Díaz-Nieto 2015;Patton et al. 2015).
In addition to be a representative community of nonvolant mammal on the eastern slope of the northern Cordillera Central, with threatened and endemic species, the protected areas in Jaguas and San Carlos hydroelectric power plants become important areas for biodiversity conservation at the regional scale.In the current scenario, in which such areas are located within a highly fragmented landscape, they play an important role as refuges for the mammalian fauna and other vertebrate groups.These are also the most relevant protected areas including low and mid elevation habitats in this part of the Central Andes of Colombia (Vásquez & Serrano 2009).Maintaining these protected areas, as well as those associated to other hydroelectric projects in the region, and improving the connectivity between them will allow the establishment of a network of reserves that would contain large forest extensions in an otherwise highly human-modified ecosystem.
As suggested by this and other studies, the development and maintenance of hydroelectric infrastructure may become an important source of biodiversity data for the region.We strongly advocate for the publication of these results of environmental and monitoring studies associated with hydroelectric projects.In the next few decades the Colombian government expects to increase hydropower development as part of its energy-mining infrastructure program (UPME 2013).This is an important opportunity for biodiversity research that aims to evaluate the responses of the biota to large infrastructure projects, and to design strategies to minimize the associated impacts (Jiménez-Segura et al. 2014).

Figure 1 .
Figure 1.Study area location in Colombia (A) and detail within hydroelectric complex on the eastern slope of the Cordillera Central (B).Map showing in detail the localities (numbers; see Appendix 1) and covers (red: infrastructure and towns; blue: water bodies; dark green: fragmented forest; light green: shrubland) in Jaguas (C) and San Carlos (D) hydroelectric power plants.The transparent layer indicates the Protected Areas in Jaguas and San Carlos respectively.