Herpetology Notes, volume 10: 685-696 (2017) (published online on 28 November 2017)

Protected areas assessment for the conservation of threatened amphibians in the Cordillera Oriental of Colombia

Mónica M. Albornoz-Espinel1, Carlos H. Cáceres-Martínez1,2 and Aldemar A. Acevedo-Rincón1,3,*

Abstract. The global decline of amphibians is one of the greatest challenges in Conservation Biology. In this study we assessed the level of protection in Protected Areas (PAs) in the Cordillera Oriental of Colombia for 52 species of threatened amphibians. We also determined the changes in vegetation coverage, both inside and outside the PAs. Our data collection was made between February 2015 and June 2017, when we gathered information from databases, biological collections, and the literature. Geographical records were georeferenced and overlaid on the layers of 190 PAs and on the layers of land coverage of the Cordillera Oriental. Our results confirm the limited level of protection for amphibians provided by PAs, whereby only 33 species represented in 160 out of 509 geographical records showed a report within PAs. At the same time, drastic changes were evident in vegetation coverage, which for most localities where records of vegetation were made 10–30 years ago was reduced to mosaics of fragmented forests, crops, and grasslands. This study demonstrates the need to establish priority actions and efficiently generate geographical areas of protection, in terms of coverage of the distribution of threatened amphibians in the Eastern region of Colombia.

Keywords: Amphibians, Andean region, conservation, protected areas, threats

Introduction (10%), Dendrobatidae (10%), and Centrolenidae (9%), and the country is classified second in South South America harbours more than 2300 of the more American species richness after Brazil (Rivera-Correa, than 6500 known amphibian species (IUCN, 2016). 2012; Acosta-Galvis, 2017). Colombia comprises 13 However, around 600 species are listed under some type ecoregions and six biomes (Sánchez-Cuervo et al., 2012) of national or international threat category, and more that offer suitable habitats for amphibians, and these than 700 remain in the data deficient category (IUCN, offer a variety of climatic and orographic characteristics 2016). It is well established that amphibians are one of that doubtlessly facilitated the establishment of the the most threatened groups of vertebrates globally (e.g., observed diversity (e.g., Ruiz-Carranza et al., 1996). On Stuart et al., 2004; Stuart, 2012). the flipside, Colombia has one of the highest numbers Colombia is ranked as a megadiverse country for of threatened amphibians in the world, with 277 species amphibians, and it is home to 812 species in 14 listed according to national and international criteria families. The highest representation is from the families (Rueda-Almonacid et al., 2004; IUCN, 2016). Known Craugastoridae (31%), Hylidae (15%), Bufonidae genera for which species are declining in this country include Pristimantis, Dendrobates, Colostethus, Centrolene, and Atelopus (Rueda-Almonacid, 1999; 1 Grupo de Investigación en Ecología y Biogeografía, IUCN, 2016), of which most are distributed in the Universidad de Pamplona, Barrio El Buque, Km 1, Vía a Andean region, probably due to intrinsic and extrinsic Bucaramanga, Pamplona, Colombia factors that act synergistically (Cooper et al., 2008). 2 Grupo de Investigación en Ecología y Conservación de Fauna Since the late 1980s, the sudden disappearance of Silvestre, Universidad Nacional de Colombia, Sede Medellín, many amphibian populations at several sites in America, Calle 59A No. 63-20, Medellín, Colombia Europe, and Australia has been documented (Stuart et 3 Programa de Doctorado en Ciencias Biológicas, Laboratorio al., 2004), suggesting that the current extinction rate de Biología Evolutiva, Pontificia Universidad Católica de Chile, Avenida Libertador Bernardo O’Higgins 340, of amphibians is 105 times the estimated historical Santiago, Chile rate for the class (McCallum, 2007). These declines, in * Corresponding author e-mail: [email protected] population densities as well as in diversity, continue to 686 Mónica M. Albornoz-Espinel et al. accelerate, affecting amphibians occupying deforested of Amphibians of Colombia (Rueda-Almonacid et al., and intervening spaces but also those occupying pristine 2004), both inside and outside the PAs. In parallel, and remote sectors within the country’s system of we assessed the conservation status of amphibians Protected Areas (PAs; Gardner, 2001; Rueda-Almonacid using information on changes in land coverage where et al., 2004; Nori et al., 2015). Factors that contribute to occurrences of threatened amphibian species have been the decrease of amphibians include pollution, climate registered. change and the resulting emerging diseases, and destruction and fragmentation of habitat that create Materials and Methods isolated patches of forest. Habitat isolation has a negative Study site.—The study was carried out in the Cordillera impact on biotic components, affecting dispersion Oriental of Colombia, including the inter-Andean valley patterns and gene flow of amphibians (Gardner, 2001; of the Magdalena River (Fig. 1). This region is one of the Rueda-Almonacid et al., 2004; Cushman, 2006). three main branches into which the Andean Cordillera in PAs are natural regions of ecological importance that Colombia is divided. The region extends in a southwest- safeguard biodiversity (Dudley, 2008) over roughly 13% to-northeast direction from the Colombian Massif in of the Earth’s habitable area (Bertzky et al., 2012). The Cauca to the Serranía de Perijá in La Guajira (Morales rate of PA expansion has varied in different regions of et al., 2007). Different life zones are represented within the world, with North and South America representing this ecoregion, including premontane humid forest, the fastest-growing regions (Zimmerer et al., 2004). montane forest, rainforest, and premontane dry forest, This fast rate of expansion is the result of government with foothills supporting forests in the south that are support, placing emphasis on PA expansion strategies connected to the humid forests of the northwestern (Naughton-Treves et al., 2005; Le Saout et al., 2013; Amazonas (Fund, 2014). Nori et al., 2015). However, gaps in the efficiency at protecting biodiversity are evident in some regions, Data collection.—A list of threatened amphibian particularly for certain organismal groups (Rodrigues species in the Cordillera Oriental was assembled and et al., 2004; Venter et al., 2014; Butchart et al., 2015; species were categorized as Vulnerable, Endangered, Nori et al., 2015), including amphibians. Amphibians or Critically Endangered according to IUCN criteria are considered the group with the most gaps in terms of and the Red Book of Amphibians of Colombia (Rueda- protection, which is demonstrated by the high number Almonacid et al., 2004). Once species were identified, a of species that occur in the various threat categories search of their occurrences was conducted by reviewing (Rodrigues et al., 2004; IUCN, 2016). scientific publications, original descriptions, online The PA system of Colombia covers 9.98% of the databases (IUCN, SiB-Colombia, Amphibian Species national territory, and is distributed across 59 National of the World, HerpNET, GBIF, ICN online collection Natural Parks and more than 700 other protected areas at the Universidad Nacional de Colombia), and an on- (Parques Nacionales de Colombia, 2017). However, site review of the biological collection of amphibians the scope of protection provided by these PAs remains at the Insituto de Ciencias Naturales at the Universidad limited, considering that the areas with high species Nacional de Colombia and the biological Collection richness do not generally coincide with areas that may José Celestino Mutis at the University of Pamplona. At have a high number of threatened or endemic species the same time, we included the time interval between and which are not spatially protected under any special the oldest record, taken from the original descriptions, management area (Forero-Medina and Joppa, 2010). and the most recent record, obtained from scientific The Cordillera Oriental is considered one of the publications and a review of national and international areas lacking information about threatened amphibian databases. species, yet it is the region with most of the endemic Each amphibian record was verified by checking species (Bernal and Lynch, 2008). Only nine National against the original description and examination of Natural Parks exist in this region as of this writing, museum specimen, and each geographic record was and this small number severely limits the level of georeferenced using ArcGIS 10.1 (ESRI, 2011), protection given to several species of amphibians. Our producing a buffer of 500 m around each record to study in the Cordillera Oriental aims to determine the represent a possible margin of error for the locality. percentage of amphibian species found there that are We then developed a database of amphibian species listed as threatened by the International Union for the to determine the historical distribution of each species. Conservation of Nature (IUCN) and in the Red Book This database was later supplemented with information Protected areas assessment for the conservation of amphibians in Colombia 687

Figure 1. Map of northwestern Colombia, with geographical records of threatened amphibians in the Cordillera Oriental indicated by coloured circles. Several of the blue protected areas are clearly visible, attesting to their ineffectiveness for amphibian conservation. Interactive map in: http://rpubs.com/bioaldemar/amphibians_Colombia

on the conservation status of each species, type of grassland, crop, and urban area. These categories were vegetation, and year of the last sighting. established using the spatial layers of land cover from The layers associated with PAs in the database were 2005–2009 (scale 1:100,000) (IDEAM, 2010). obtained from the Parques Nacionales de Colombia Analysis.—For the historical record of each assessed (2017). One hundred and ninety PAs corresponding amphibian species, we overlapped layers of land to the Cordillera Oriental and some of the Orinoquía cover and PAs using ArcGIS 10.1 (ESRI, 2011). This and Amazonia of Colombia were selected. These PAs technique produced spatial relationships from which included National Natural Parks (NNP = 16; Parques we determined the frequency of geographical records Nacionales Naturales de Colombia), Fauna and Flora available for each species inside and outside the PAs. Sanctuaries (SFF = 3; Santuarios de Flora y Fauna), Historical records and reports of year of last sighting Regional Natural Parks (RNP = 18; Parques Naturales for each species of amphibian were evaluated, and the Regionales), National Protective Forest Reserves (NPFR descriptions of the original habitats were compared with = 32; Reservas Forestales Protectoras Nacionales), recent layers on land cover. Regional Protective Forest Reserves (RPFR = 40; Reservas Forestales Protectoras Regionales), Regional Results Districts of Integrated Management (IMRD = 22; Distritos Regionales de Manejo Integrado), Civil Society Numbers of amphibian species and PAs.—Fifty-two Natural Reserves (RNSC = 58; Reservas Naturales de la species of threatened amphibians in all endangered Sociedad Civil), and Unique Natural Areas (ANU = 1; categories were analysed from 509 geographical records Area Natural Única). compiled for the entire Cordillera Oriental (Fig. 1). Of Land cover was classified as páramo, mature forest, the 190 selected PAs, amphibians were only recorded secondary forest, fragmented forest, riverine forest, in 25 PAs, specifically nine National Natural Parks, one 688 Mónica M. Albornoz-Espinel et al.

Table 1. Amphibian species in protected areas (PAs) in the Cordillera Oriental of Colombia. Table 1. Amphibian species in protected areas (PAs) in the Cordillera Oriental of Colombia. PA1 / IUCN Category2 Date established Species Records 1 as PA Atelopus lozanoi 3 Atelopus mandingues 2 Atelopus muisca 8 NNP Chingaza / II 1977 Pristimantis affinis 2 Pristimantis carranguerorum 1 Pristimantis elegans 8 Pristimantis frater 1

Bolitoglossa lozanoi 4 Hyloscirtus denticulentus 1 Pristimantis bacchus 4 NNP Serranía de Los Yariguíes / II 2005 Pristimantis bicolor 6 Pristimantis merostictus 3 Rulyrana adiazeta 2

Allobates juanii 1 NNP Tamá / II 1977 Pristimantis frater 2

Tachiramantis douglasi 1

NNP Pisba / II 1977 Atelopus marinkellei 1

Pristimantis elegans 2 NNP Sumapaz / II 1997 Pristimantis frater 1

NNP Serranía del Perijá / II 2016 Hyloscirtus piceigularis 2

NNP Cordillera de los Picachos / II 1977 Atelopus petriruizi 1

NNP El Cocuy / II 1977 Pristimantis carranguerorum 1

NNP Alto Fragua Indi Wasi 2002 Hypodactylus dolops 1

Atelopus mittermeieri 2 Atelopus monohernandezi 2 Centrolene buckleyi 1 Hyloscirtus piceigularis 1 SFF Guanentá Alto Río Fonce / IV 1993 Pristimantis bacchus 2 Pristimantis elegans 1 Pristimantis jorgevelosai 1 Pristimantis merostictus 3 Hyalinobatrachium ibama 1 Centrolene buckleyi 1 Hyloscirtus piceigularis 1 RNP El Rasgon / II 2009 Pristimantis bicolor 3 Pristimantis jorgevelosai 2 Pristimantis merostictus 6 Tachiramantis douglasi 3

Hyloscirtus lynchi 2 Pristimantis bicolor 1 RNP Cerro La Judía / II 2009 Pristimantis jorgevelosai 2 Tachiramantis douglasi 2

Atelopus lozanoi 1 RNP Siscunsí-Ocetá / II 2009 Atelopus marinkellei 5

RNP Santurbán / II 2013 Tachiramantis douglasi 2

RNP Serranía de las Quinchas / II 2008 Centrolene petrophilum 1

Centrolene buckleyi 2 FRPN Bosque Oriental de Bogotá / VI 1976 Hyloxalus edwardsi 1 Pristimantis elegans 4

Atelopus lozanoi 1 FRPN Ríos Blanco y Negro / VI 1990 Atelopus muisca 1

FRPN Quebrada Honda / VI 1945 Allobates juanii 1

Centrolene buckleyi 2 FRPR Páramo Guargua y Laguna Verde / VI 2009 Pristimantis elegans 1

FRPR Colombia / VI 2008 Atelopus mandingues 1

FRPR Cuchilla de Peñas Blancas / VI 1983 Hyloxalus vergeli 1

Andinobates virolinensis 5 Atelopus mittermeieri 3 Atelopus monohernandezi 3 Hyalinobatrachium ibama 1 Hyloscirtus denticulentus 1 Hyloscirtus lynchi 1 RDIM Páramos Guantiva-La Rusia / VI 2011 Hyloscirtus piceigularis 1 Pristimantis acutirostris 3 Pristimantis bacchus 3 Pristimantis bicolor 6 Hyalinobatrachium ibama 1 Hyloscirtus piceigularis 1 RNP El Rasgon / II 2009 Pristimantis bicolor 3 Pristimantis jorgevelosai 2 Pristimantis merostictus 6 Tachiramantis douglasi 3

Hyloscirtus lynchi 2 Pristimantis bicolor 1 RNP Cerro La Judía / II 2009 Pristimantis jorgevelosai 2 Tachiramantis douglasi 2

Atelopus lozanoi 1 RNP Siscunsí-Ocetá / II 2009 Atelopus marinkellei 5 Protected areas RNPassessment Santurbán / forII the conservation of amphibians2013 in ColombiaTachiramantis douglasi 2 689 RNP Serranía de las Quinchas / II 2008 Centrolene petrophilum 1

Table 1. Continued. Centrolene buckleyi 2 FRPN Bosque Oriental de Bogotá / VI 1976 Table 1. Amphibian species in protected areas (PAs) in the Cordillera OrientalHyloxalus of Colombia. edwardsi 1 1 2 PA / IUCN Category Date established PristimantisSpecies elegans Records4 1 as PA Atelopus lozanoi 13 FRPN Ríos Blanco y Negro / VI 1990 Atelopus mandinguesmuisca 12 Atelopus muisca 8 FRPN Quebrada Honda / VI 1945 Allobates juanii 1 NNP Chingaza / II 1977 Pristimantis affinis 2 PristimantisCentrolene buckleyi carranguerorum 21 FRPR Páramo Guargua y Laguna Verde / VI 2009 Pristimantis elegans 18 Pristimantis frater 1 FRPR Colombia / VI 2008 Atelopus mandingues 1 Bolitoglossa lozanoi 4 FRPR Cuchilla de Peñas Blancas / VI 1983 Hyloxalus vergeli 1 Hyloscirtus denticulentus 1 PristimantisAndinobates bacchusvirolinensis 54 NNP Serranía de Los Yariguíes / II 2005 PristimantisAtelopus mittermeieri bicolor 36 PristimantisAtelopus monohernandezi merostictus 3 RulyranaHyalinobatrachium adiazeta ibama 12 Hyloscirtus denticulentus 1 Allobates juanii 1 NNP Tamá / II 1977 Hyloscirtus lynchi 1 RDIM Páramos Guantiva-La Rusia / VI 2011 Pristimantis frater 2 Hyloscirtus piceigularis 1 Tachiramantis douglasi 1 Pristimantis acutirostris 3

NNP Pisba / II 1977 AtelopusPristimantis marinkellei bacchuselegans 31 Pristimantis bicolormerostictus 63 Pristimantis elegans 2 NNP Sumapaz / II 1997 Pristimantis renjiforum 3 Pristimantis frater 1 Rulyrana adiazeta 1

NNP Serranía del Perijá / II 2016 HyloscirtusStrabomantis piceigularis ingeri 2

NNPRDIM Cordillera Rio Subachoque de los Picachos y Pantano / II de Arcey / VI 1977 1997 AtelopusPristimantis petriruizi elegans 12

NNPRDIM El Salto Cocuy de /Tequendama II y Cerro Manjui / VI 1977 1999 PristimantisBolitoglossa carranguerorumcapitana 1

NNPRNCS Alto El Horadero Fragua Indi de WasiSan Alejo / VI 20022008 HypodactylusHyloxalus edwardsi dolops 1 1 Protected area categories: National Natural Parks (NNP), Fauna and Flora Sanctuaries (SFF), Regional Natural Parks (RNP), National Protective Forest Reserves (NPFR), Atelopus Regional mittermeieri Protective Forest Reserves2 2 (RPFR), Regional Districts of Integrated Management (IMRD), CivilAtelopus Society monohernandezi Natural Reserves (RNSC),2 3 and Unique Natural Areas (ANU). Centrolene buckleyi 1 4 2 Protected Area Categories IUCN: II = National Park, IV = Habitat/Species Management Area, VI = Protected area with sustainable use of natural resources. Hyloscirtus piceigularis 1 5 SFF Guanentá Alto Río Fonce / IV 1993 6 Pristimantis bacchus 2

7 Pristimantis elegans 1 8 9 Pristimantis jorgevelosai 1 Pristimantis merostictus 3

Sanctuary of Fauna and Flora, five Regional Natural SpeciesCentrolene records buckleyi inside and outside1 of PAs.—Evaluation Parks, three National Protective Forest Reserves, three of the geographical distribution of the amphibian Regional Protective Forest Reserves, three Regional species showed that 33 species (63%) represented by Integrated Management Districts, and one Civil Society 160 geographical records (31%) were reported at least Natural Reserves (Table 1). once in a protected area (Fig. 2A, PAs). However, just In relation to the date of creation of the protected 19 species (36%) were reported in at least one National areas, the majority of national parks in the Cordillera Natural Park (Table 1). In contrast, all evaluated species Oriental were created in the 1970s, sheltering more than were recorded outside PAs (353 geographical records; 20 species of which some (e.g., Atelopus marinkellei, 69%; Fig. 2A, OPAs). Concerning the threat categories, Pristimantis affinis, P. elegans, P. frater) were nine Critically Endangered species (17%) are found described before the of the PA was established (Table within protected areas and 14 (27%) outside, 11 1). However, some NNPs, including the Serranía de Los Endangered species (21%) within and 16 (31%) outside, Yariguíes and the Serranía del Perijá, were created after and 12 Vulnerable (21%) within and 22 (42%) outside 2000, and the NNP Sumapaz in the 1990s. These now (Fig. 2B). harbor eight threatened species, mainly in the NNP Los Of the PAs with the largest area (10,000–60,000 ha), Yariguíes (Table 1). SFF Guanentá Alto Río Fonce holds the largest number 690 Mónica M. Albornoz-Espinel et al.

Figure 2. Bar graphs displaying geographical records for the Cordillera Oriental of Colombia. (A) Records from inside Protected Areas (PAs) and outside of these areas (OPAs). (B) Records according to Red List Categories. Abbreviations include CR = critically endangered, EN = endangered, and VU = vulnerable. (C) Records according to disturbed areas. (D) Records according to natural areas.

of species (n = 8), followed by the NNP Chingaza (n = habitat that has now been transformed from pristine 7) and the NNP Serranía de los Yariguíes (n = 6) (Table forest to areas with mosaics of fragmented forests, 1). In comparison, the largest number of geographical crops, or pastures (Table 2), as evidenced by the high records of amphibians was concentrated in small natural number of records that currently overlap areas of crops reserves and protection zones (< 10,000 ha), such as the (22%) and grasslands (19%), representing by more Páramo Guantiva - La Rusia (n = 15 species) (Table 1). than 70% of the species (Table 2, Fig. 3). Nevertheless, within the PAs most records (11%) fall in areas that still Land cover and geographical records of amphibians.— retain mature forests (Table 2, Fig. 3). For areas outside the PAs 44 species (85%) with 213 records (42%) were recorded in areas that currently have Discussion some degree of disturbance of the vegetation (crops, forest fragmentation) (Table 2, Fig. 2C, OPAs). Among Our findings confirm the limited level of conservation areas within PAs, 18 species (35%) have 41 records that most species of amphibians have in the Cordillera (8%) in areas modified by human activity (Table 2, Fig. Oriental of Colombia. We show that these species are 2C, PAs). not well represented regarding their distribution in PAs, Whereas 46 species (88%) represented by 141 with just 25 of the 190 PAs in the Cordillera Oriental geographical records (28%) were outside of any PA harbouring threatened amphibians. All assessed species (Fig. 2D, OPAs), the areas from which these records were recorded at least once outside PAs, with 37% derive currently have an acceptable vegetation cover. A of species without any PA protection at all (Table 2). total of 116 geographical records (23%), corresponding However, 63% of species have limited presence in to 29 species, were within a PA with vegetation cover some areas with environmental protection (Table (Table 2, Fig. 2D, PAs). 2). For example, seven species of more threatened Collected reports and original descriptions of each genera, such as Atelopus, are represented within a PA. examined species show that species originally occupied However, three species in this genus (A. minutulus, A. Protected areas assessment for the conservation of amphibians in Colombia 691

Table 2. Geographical records of amphibian species and land cover in the Cordillera Oriental of Colombia.

Table 2. Geographical records of amphibian species and land cover in the Cordillera Oriental of Colombia. Species Red List Year of Original Land cover Records in Source for when last seen5 1 3 ͳͲ Status 2 habitat 4 PAs description last seen (2005–2009) Allobates juanii CR 1994 2011 MF-SF FF-SF-C-G-U 2 MCNUP-H ranoides EN 1918 2011 MF SF-G-C none ANDES-A Andinobates virolinensis EN 1992 2006 MF-SF MF-SF-RF-G-C 5 MHN-UIS-A Atelopus lozanoi CR 2001 1993 P G-S-P 5 ICN mandingues CR 2001 1994 P-MF MF-FF-C 3 ICN marinkellei CR 1970 1996 MF-P-RF P-S-G-C-U 6 IAvH minutulus CR 1988 1984 MF MF-C none ICN mittermeieri EN 2006 2007 MF MF-G 5 MPUJ monohernandezi CR 2002 1995 MF MF-G-C 5 MHN-UIS-A muisca CR 1991 1996 MF-P MF-FF-S-P 9 IUCN pedimarmoratus CR 1963 1990 MF FF-G none IAvH petriruizi CR 1999 1998 MF-RF MF 1 IUCN subornatus CR 1899 1999 MF-SF MF-S-C-P none IUCN Bolitoglossa capitana CR 1963 2005 MF-SF SF-G-S-C 1 Chaves-Portilla et al., 2006 lozanoi VU 2001 2014 MF FF-C-G-U 4 MHN-UIS-A pandi EN 1963 2011 RF SF-C none Del Río-García et al., 2014 Centrolene buckleyi VU 1882 2014 P-SF MF-RF-S-G-C 6 IAvH daidaleum VU 1991 2010 MF-RF MF-SF-S-C none MCN-UP geckoideum VU 1872 2007 MF-RF MF-G none M. Rada, pers. comm. petrophilum EN 1991 1983 MF-SF-RF MF-G-C 1 ICN Colomascirtus lindae VU 1978 1999 MF-SF MF-SF-G-C none ICN Cryptobatrachus fuhrmanni VU 1914 2012 MF-SF G-C none MHUA Dendropsophus stingi VU 1994 2006 S-G MF none IAvH Hyalinobatrachium esmeralda EN 1998 2011 MF-SF-RF MF-SF-FF-G-C none ANDES-A ibama VU 1998 2005 RF MF-FF-P-G-C 2 MPUJ Hyla nicefori CR 1970 1945 MF FF none MLS Hyloscirtus denticulentus EN 1972 2011 MF-SF-RF MF-S-G-C 2 MHN-UIS-A lynchi EN 1991 2000 MF-RF MF-P-G 3 MHN-UIS-A piceigularis EN 1982 1987 MF-RF MF-SF-S-G-C 5 MLS torrenticola VU 1978 1990 MF-SF-RF MF-SF-G-C none ICN Hyloxalus edwardsi CR 1982 1996 RF FF-P-C 1 ICN ruizi CR 1982 1990 MF SF-S-C none ICN vergeli VU 1940 2005 MF-RF FF-G-C 1 MLS Hypodactylus dolops VU 1980 1990 MF-RF MF-G 2 ICN Pristimantis acutirostris EN 1984 2016 MF SF-MF-G-C 3 IAvH affinis VU 1899 2014 SF-P MF-FF-C-S 2 IAvH bacchus EN 1984 2015 MF-SF-P MF-SF-RF-C-G-P 9 Chinchilla-Lemus and Meneses-Pelayo, 2016 bicolor VU 1983 2007 MF-SF-RF MF-SF-G-C 16 MHN-UIS-A carranguerorum VU 1994 2016 MF-SF-RF MF-FF-SF-RF-C-G 2 Anganoy-Criollo and Ramírez, 2017 elegans VU 1863 2015 P-MF MF-P-C-S 19 IAvH frater VU 1899 2015 MF-SF MF-FF-SF-C-G-U 4 MCN-UP hernandezi EN 1983 1990 MF MF-C none ICN jorgevelosai EN 1994 2004 MF MF-C 5 MHN-UIS-A merostictus EN 1984 2004 MF MF-FF-C-G 15 MHN-UIS-A mnionaetes EN 1998 2015 MF SF-G none IAvH petersi VU 1991 2004 MF MF-G-C none ICN pugnax VU 1973 1990 MF-RF MF none ICN renjiforum EN 2000 2014 MF MF-C 3 IAvH Rulyrana adiazeta VU 1991 2011 MF-SF-RF MF-G-S-C 3 MHN-UIS-A Strabomantis cornutus VU 1871 1990 MF MF none IUCN ingeri VU 1961 2014 MF MF-SF-G-C 2 Meneses-Pelayo et al., 2017 Tachiramantis douglasi VU 1996 2015 MF-SF MF-SF-FF-C-G-S 8 MCN-UP 1 CR = Critically Endangered, EN = Endangered, VU = Vulnerable according to IUCN and the Libro Rojo de Anfibios de Colombia (Rueda-Almonacid et al., 2004). 2 The years were obtained from scientific publications and through a review of national and international databases. ͳͳ 3 ͳʹ The type locality, according to the original description. 4 G = Grassland, S = Shrub, P = Paramo, FF = Fragmented forest, MF = Mature forest, SF = Secundary forest, RF = Riparian forest, C = Crops, U = Urban area. ͳ͵ 5 ͳͶ MCNUP-H = Museo de Ciencias Naturales – Universidad de Pamplona, Colombia. ANDES-A = Museo de Historia Natural, Colección de Anfibios – ͳͷ Universidad de Los Andes, Colombia. MHN-UIS-A = Museo de Historia Natural, Colección Herpetológica (Anfibios) – Universidad Industrial de Santander, ͳ͸ Colombia (Ramírez, 2016). ICN = Instituto de Ciencias Naturales – Universidad Nacional, Colombia (Raz et al., 2016). IAvH = Instituto de Investigación de ͳ͹ Recursos Biológicos Alexander von Humboldt, Colombia. MPUJ = Museo de Historia Natural – Pontificia Universidad Javeriana, Colombia (Hoyos and ͳͺ Forero, 2016). IUCN = International Union for Conservation of Nature. MHUA = Museo de Herpetología – Universidad de Antioquia, Colombia (Daza, 2016). ͳͻ MLS = Museo de La Salle, Colombia (Espitia, 2016). ʹͲ ʹͳ ʹʹ ʹ͵ ʹͶ ʹͷ elegans VU 1863 2015 P-MF MF-P-C-S 19 IAvH frater VU 1899 2015 MF-SF MF-FF-SF-C-G-U 4 MCN-UP hernandezi EN 1983 1990 MF MF-C none ICN jorgevelosai EN 1994 2004 MF MF-C Mónica5 M. Albornoz-EspinelMHN-UIS-A et al. 692 merostictus EN 1984 2004 MF MF-FF-C-G 15 MHN-UIS-A mnionaetes EN 1998 2015 MF SF-G none IAvH Table 2. Continued.petersi VU 1991 2004 MF MF-G-C none ICN pugnax VU 1973 1990 MF-RF MF none ICN Tablerenjiforum 2. Geographical recordsEN of amphibian 2000 species and land 2014 cover in the CordilleraMF Oriental of Colombia.MF-C 3 IAvH Species Red List Year of Original Land cover Records in Source for when last seen5 Rulyrana 1 3 ͳͲ Status 2 habitat 4 PAs adiazeta VU description 1991 last 2011 seen MF-SF-RF (2005–2009) MF-G-S-C 3 MHN-UIS-A StrabomantisAllobates cornutusjuanii VUCR 18711994 19902011 MF-SFMF FF-SF-C-G-UMF none2 MCNUP-HIUCN ingeriranoides VUEN 19611918 20112014 MF MF-SF-G-CSF-G-C none2 Meneses-PelayoANDES-A et al., 2017 TachiramantisAndinobates douglasivirolinensis VUEN 19921996 20062015 MF-SF MF-SF-FF-C-G-S MF-SF-RF-G-C 58 MMHN-UIS-ACN-UP 1 AtelopusCR = Critically Endangered, EN = Endangered, VU = Vulnerable according to IUCN and the Libro Rojo de Anfibios de Colombia (Rueda-Almonacid et al., 2004).lozanoi CR 2001 1993 P G-S-P 5 ICN 2 The years were obtained from scientific publications and through a review of national and international databases. ͳͳ 3 mandingues CR 2001 1994 P-MF MF-FF-C 3 ICN ͳʹ The type locality, according to the original description. 4 G marinkellei= Grassland, S = Shrub,CR P = Paramo, FF 1970 = Fragmented 1996 forest, MF = Mature MF-P-RF forest, SF = Secundary P-S-G-C-U forest, RF = Riparian6 forest, C = Crops, IAvHU = Urban area. ͳ͵ 5 ͳͶ MCNUP-Hminutulus = Museo deCR Ciencias Naturales 1988 – Universidad 1984 de Pamplona,MF Colombia. ANDES-AMF-C = Museo de Historianone Natural, ColecciónICN de Anfibios – ͳͷ Universidadmittermeieri de Los Andes,EN Colombia. 2006MHN-UIS-A = 2007Museo de HistoriaM Natural,F Colección HerpetológicaMF-G (Anfibios)5 – Universidad IndustrialMPUJ de Santander, Colombia (Ramírez, 2016). ICN = Instituto de Ciencias Naturales – Universidad Nacional, Colombia (Raz et al., 2016). IAvH = Instituto de Investigación de ͳ͸ monohernandezi CR 2002 1995 MF MF-G-C 5 MHN-UIS-A ͳ͹ Recursos Biológicos Alexander von Humboldt, Colombia. MPUJ = Museo de Historia Natural – Pontificia Universidad Javeriana, Colombia (Hoyos and ͳͺ Forero,muisca 2016). IUCN = InternationalCR Union 1991 for Conservation 1996 of Nature. MHUA MF-P = Museo de HerpetologíaMF-FF-S-P – Universidad9 de Antioquia, ColombiaIUCN (Daza, 2016). ͳͻ MLSpedimarmoratus = Museo de La Salle,CR Colombia (Espitia, 1963 2016). 1990 MF FF-G none IAvH ʹͲ petriruizi CR 1999 1998 MF-RF MF 1 IUCN ʹͳ ʹʹ subornatus CR 1899 1999 MF-SF MF-S-C-P none IUCN ʹ͵ Bolitoglossa ʹͶ capitana CR 1963 2005 MF-SF SF-G-S-C 1 Chaves-Portilla et al., 2006 ʹͷ lozanoi VU 2001 2014 MF FF-C-G-U 4 MHN-UIS-A pedimarmoratuspandi , A. subornatusEN 1963) were only 2011 recordedRF populationsSF-C of some amphibiannone Del species, Río-García especially et al., 2014 those Centrolene outside buckleyi of PAs, with VU the last 1882 geographical 2014 records P-SF withoutMF-RF-S-G-C recent sightings, 6 is paramount.IAvH Locations such dating backdaidaleum to 1984, VU 1990, and 1991 1999, 2010 respectively. MF-RF as Chingaza,MF-SF-S-C Pisba, and none the CordilleraMCN-UP de Los Picachos, Similarly,geckoideum the majority VUof species 1872 with occurrences 2007 MF-RFare areas thatM F-Gmay harbournone remnant populations M. Rada, pers. comm. of Atelopus petrophilum EN 1991 1983 MF-SF-RF MF-G-C 1 ICN currentlyColomascirtus found in areas with human impact (primarily species, would be important to survey. These National crops) (Fig. 3). Association with this habitat type could Natural Parks (NNPs) may also harbour indicated be causing local extinctions, given that most of these species of the genus Pristimantis, which includes the species were historically associated with areas covered largest number of threatened species in the Cordillera by forest or páramo, which have been gradually lost. Oriental (IUCN, 2016). Furthermore, it is necessary to This information reinforces the need to establish new undertake surveys to determin the diversity in PAs and PAs, or expand existing ones, in order to safeguard surrounding buffer areas, since in the Cordillera Oriental threatened amphibian populations that may currently studies on the diversity, conservation, and ecology only occur outside PAs. However, resources and funds are generally still very limited. We highlight the work for the acquisition of habitat is generally limited. Thus, conducted in areas like SFF Guanentá, where 14 species expansion efforts must be accompanied by the proper were found, with Pristimantis being the dominant management of existing PAs (Naughton-Treves et al., genus (Gutiérrez-Lamus et al., 2004). The discovery 2005; Le Saout et al., 2013). Moreover, the need to of new species, such as Atelopis muisca (Rueda- increase studies that allow identification of remnant Almonacid and Hoyos, 1992) and Pristimantis dorado

Figure 3. Bar graphs displaying geographical records in the Cordillera Oriental of Colombia according to land cover inside and outside Protected Areas. Abbreviations include G = grassland, S = shrub, P = páramo, FF = fragmented forest, MF = mature forest, SF = secondary forest, RF = riparian forest, C = crops, UA = urban area. Protected areas assessment for the conservation of amphibians in Colombia 693

(Rivera-Correa et al., 2016) in the NNP Chingaza, A. a finding of 11 amphibian species was reported from guitarraensis in the NNP Sumapaz (Osorno-Muñoz et the NNP Tayrona, including Dendrobates truncatus and al., 2001), and Bolitoglossa leandrae and B. tamaense Colostethus ruthveni (Rueda-Solano and Castellanos- in the NNP Tamá (Acevedo et al., 2013) are also Barliza, 2010). Epidemiological surveillance and important indicators for our lack of knowledge of the monitoring of key amphibian species has been done in area. Also, there is a need to study the natural history the Sierra Nevada de Santa Marta (Rueda-Solano et al., of little-known species, such as Gastrotheca helenae 2016). Guevara and De la Ossa (2009) found 17 species, (Acevedo et al., 2011). Another essential factor is to predominantly in the family Hylidae (6 species), in the establish appropriate protocols to diagnose emerging RFP Serrania de Coraza in the Department of Sucre. diseases, such as chytridiomycosis, a disease caused Fully 25% of amphibian species worldwide are not by the fungus Batrachochytrium dendrobatidis (Bd), protected within PAs (Nori et al., 2015), indicating which has been proven to reduce taxonomic diversity that PAs are not completely achieving the conservation (Crawford et al., 2010). This fungus was previously objectives of protecting all biological diversity (Primack reported in Colombia (Ruiz and Rueda-Almonacid, et al., 2001; Weeks et al., 2010; Porter-Bolland et al., 2008), where it was reported to infect species in the 2012), which especially includes conservation of rare or Cordillera Oriental (Ruíz and Rueda-Almonacid, 2008; endangered species (Toledo 2005; Gaston et al., 2008). Vásquez-Ochoa et al., 2012; Acevedo et al., 2016a,b). Of the 25 PAs we evaluated (Table 1), according to According to these data, 23 infected species were present the Protected Areas Categories of IUCN (Dudley, in NNP Tamá in northeastern Colombia (Acevedo et al., 2008), none could be considered in Category Ia (Strict 2016a,b). Populations of Atelopus muisca, A. lozanoi, Nature Reserve) and Ib (Wilderness Area), defined as Bolitoglossa adspersa, and Hyloxalus subpunctatus areas where there is little or no alteration of ecosystems, are declining in the NNP Chingaza (Rueda-Almonacid have no human occupation, and have a management and et al., 2004, Ruíz and Rueda-Almonacid 2008). Thus, strict protection to ensure their conservation, and that this PA and several areas outside PAs should receive in addition the scientific research and the monitoring the highest priority for protection when generating of species and ecosystems are paramount (Chape et initiatives to conserve amphibian species in the country al. 2005; Dudley, 2008). Among the PAs with records (Rueda-Almonacid, 1999). of amphibians, only 14 (9 NNP and 5 RNP; Table 1) Fortunately, in the Cordillera Occidental important correspond to Category II, identified as areas that are contributions to the knowledge of amphibians have typically large and have good ecosystem function, though been made from studies in PAs. For example, in NNP they may need an appropriate ecological management Munchique eight species of the genus Pristimantis and maintenance of areas of protection outside limits of have been reported (García-R. et al., 2005). In the PNN the PAs, such as buffer zones (Dudley, 2008). Paramillo 52 species, mostly of the genus Pristimantis Other areas were found in Category IV (6 RFP, 3 (19.2% of the total) have been sighted (Romero- RDIM, 1 RSNC; Table 1) characterized as help protect Martínez et al., 2008). In another type of PA, the nature or restore ecosystems altered, maintaining species of reserves Maravelez, Panabi, Madremonte, Acaime, and flora of international, national or local significance, and El Bosque in the department of Quindío, studies have which usually have a varied area in terms of size, being allowed the characterization of the amphibians diversity, generally small (Dudley, 2008). One PA is placed in comprising mainly species in the genus Pristimantis Category VI (Sanctuary of Flora and Fauna Guanentá (69% of the total); diversity in this genus is apparently Alto Río Fonce; Table 1), which is characterized by a prominent feature in most areas in western Colombia the conservation of ecosystems and habitats associated (Cadavid et al., 2005). Furthermore, new species have to cultural values and traditional systems of natural been described from specimens collected within PAs, resource management. They are usually large, with the including Atelopus carauta in the NNP Las Orquideas greater part of the area under natural conditions (Dudley, (Ruiz-Carranza and Hernández-Camacho, 1978) and 2008). Bolitoglossa tatamae in the NNP Tatamá (Acosta and Therefore, the low level of protection granting by PAs Hoyos, 2006). The status of species under threat has and the high number of records outside the protected been evaluated in PAs, including A. spurrelli in the NNP areas threatens the species’ long-term survival, especially Utria in the Department of Chocó (Gomez-Hoyos et al., those that are most threatened, taking into account 2014). On the other hand, in PAs located outside the the types of land use mostly present in PAs included Andean cordillera work has also been conducted, and in the category IV and the accelerated processes of 694 Mónica M. Albornoz-Espinel et al. transformation and fragmentation of the coverage of Bernal, M.H., Lynch, J.D. (2008): Review and analysis of altitudinal natural in the Andes of Colombia (Etter and Villa, 2000; sistribution of the Andean anurans in Colombia. Zootaxa 1826: Etter and Van-Wynngaarden, 2000; Etter et al., 2008), 1–25. Bertzky, B., Corrigan, C., Kemsey, J., Kenney, S., Ravilious, C., even within protected areas (Armenteras et al., 2003, Besançon, C., Burgess, N. (2012): Protected Planet Report 2009) thus, in addition to generating new PAs to ensure 2012: Tracking progress towards global targets for protected the conservation of biological diversity (Sepulveda et al, areas. Gland, Switzerland, IUCN. 1997), reassessing the current PA protection category, Butchart, S.H.M., Clarke, M., Smith, R.J., Sykes, R.E., and national parks and regional corporations should Scharlemann, J.P.W., Harfoot, M., Buchanan, G.M., Angulo, encourage frequent studies of surveys and monitoring A., Balmford, A., Bertzky, B., Brooks, T.M., Carpenter, K.E., of the populations of amphibians threatened within and Comeros-Raynal, M.T., Cornell, J., Ficetola, G.F., Fishpool, outside protected areas. L.D.C., Fuller, R.A., Geldmann, J., Harwell, H., Hilton-Taylor, C., Hoffmann, M., Joolia, A., Joppa, L., Kingston, N., May, I., Milam, A., Polidoro, B., Ralph, G., Richman, N., Rondinini, Acknowledgments. Special thanks to the Vicerrectoría Académica C., Segan, D., Skolnik, B., Spalding, M., Stuart, S. N., Symes, and the Vicerrectoría de Investigaciones at the Universidad de A., Taylor, J., Visconti, P., Watson, J., Wood, L., Burgess, N.D. Pamplona for their student research program. Thanks to John D. (2015): Shortfalls and solutions for meeting national and global Lynch at the Universidad Nacional de Colombia, and to National conservation area targets. Conservation Letters 8: 329–337. Natural Parks of Colombia. We also thank L. Sánchez for a Cadavid, J.G., Román-Valencia, C., Gómez, A.F. (2005): review of the text and the reviewers for their valuable comments Composición y estructura de anfibios anuros en un transecto that helped to improve this manuscript significantly. altitudinal de los Andes Centrales de Colombia. Revista del Museo Argentino de Ciencias Naturales 7: 103–118. References Chape, S., Harrison, J., Spalding, M., Lysenko, I. (2005): Measuring the extent and effectiveness of protected areas as an indicator for Acevedo, A., Silva, K., Franco, R., Lizcano, D.J. (2011): Distribución, meeting global biodiversity targets. Philosophical Transactions historia natural y conservación de una rana marsupial poco of the Royal Society B, Biological Sciences 360: 443–455. conocida, Gastrotheca helenae (Anura: Hemiphractidae), en el Chaves-Portilla, G., Cortés-Herrera, O., Morales-Sánchez, J.E. Parque Nacional Natural Tamá, Colombia. Boletín Científico, (2006): Redescubrimiento y ampliación del área de distribución Museo de Historia Natural, Universidad de Caldas 15: 68–74. de Bolitoglossa capitana (Caudata: Plethodontidae), especie Acevedo, A., Wake, D.B., Amezquita, A., Márquez, R., Silva, K., endémica y amenazada de Colombia. Revista de la Academia Franco, R. (2013): Two new species of salamanders, genus Colombiana de Ciencias Exactas Fisicas y Naturales 30(117): Bolitoglossa (Amphibia: Plethodontidae), from the eastern 615–617. Colombian Andes. Zootaxa 3609: 69–84. Chinchilla-Lemus, W., Meneses-Pelayo, E. (2016): Pristimantis Acevedo, A., Franco, R. Carrero, D.A. (2016a): Diversity of Andean bacchus (wine robber frog). parental care and clusth size. amphibians of the Tamá National Natural Park in Colombia: a Herpetological Review 47(4): 646–647. survey for the presence of Batrachochytrium dendrobatidis. Animal Biodiversity and Conservation 39: 1–10. Crawford, A.J., Lips, K.R., Bermingham, E. (2010): Epidemic Acevedo, A., Martínez, M., Armesto, L.O., Solano, L., Silva, disease decimates amphibian abundance, species diversity, K., Lizcano, D. (2016b): Detection of Batrachochytrium and evolutionary history in the highlands of central Panama. dendrobatidis in amphibians from northeastern Colombia. Proceedings of the National Academy of Sciences 107: 13777– Herpetological Review 47: 220–226. 13782. Acosta, A.R., Hoyos, J.M. (2006): A new species of salamander Cooper, N., Bielby, J., Thomas, G.H., Purvis, A. (2008): (Caudata: Plethodontidae: Bolitoglossa) from the subandean Macroecology and extinction risk correlates of frogs. Global forest Western Cordillera of Colombia. Herpetologica 62: 302– Ecology and Biogeography 17: 211–221. 308. Cushman, S.A. (2006): Effects of habitat loss and fragmentation on Acosta-Galvis, A.R. (2017): Lista de los Anfibios de Colombia. amphibians: a review and prospectus. Biological Conservation Available at: http://www.batrachia.com. Accessed on 10 128: 231–240. February 2017. Daza, J.M. (2016): Colección de anfibios - Museo de Herpetología Anganoy-Criollo, M., Ramírez, J.P. (2017): New records of de la Universidad de Antioquia. Version 7.0. Universidad de Pristimantis carranguerorum (Anura: Craugastoridae) from the Antioquia. Available at: https://doi.org/10.15472/zn2bkv via Cordillera Oriental of Colombia. Check List 13(3): 2138. GBIF.org. Accessed on 16 June 2017. Armenteras, D., Gast, F., Villareal, H. (2003): Andean forest Del Río-García, J.S., Serrano-Cardozo, V.H., Ramírez-Pinilla, fragmentation and the representativeness of protected natural M.P. (2014): Diet and Microhabitat Use of Bolitoglossa cf. areas in the eastern Andes, Colombia. Biological Conservation pandi (Caudata: Plethodontidae) from the Cordillera Oriental 113: 245–256. of Colombia. South American Journal of Herpetology 9(1): Armenteras, D., Rodríguez, N., Retana, J. (2009): Are conservation 52–61. strategies effective in avoiding the deforestation of the Colombian Dudley, N. (2008): Guidelines for Applying Protected Area Guyana Shield? Biological Conservation 142: 1411–1419. Management Categories. Gland, Switzerland, IUCN. Protected areas assessment for the conservation of amphibians in Colombia 695

Espitia, J.E. (2016): Colección de Anfibios Museo de La Salle Badman, T., Rodrigues, A.S.L. (2013): Protected areas and Bogotá. Universidad de La Salle. Available at: https://doi. effective biodiversity conservation. Science 342: 803–805. org/10.15468/dvte4z via GBIF.org. Accessed on 16 June 2017. McCallum, M.L. (2007): Amphibian decline or extinction? ESRI (2011): ArcGIS Desktop: Release 10. Redlands, California, Current declines dwarf background extinction rate. Journal of USA, Environmental Systems Research Institute. Herpetology 41: 483–491. Etter, A., Villa, L.A. (2000): Andean forests and farming systems Meneses-Pelayo, E., Chinchilla-Lemus, W., Ramírez-Pinilla, in part of the Eastern Cordillera (Colombia). Mountain Research M.P. (2017): Filling gaps and update of the distribution and Development 20: 236–245. of Strabomantis ingeri (Cochran & Goin, 1961) (Anura: Etter, A., Van Wyngaarden, W. (2000): Patterns of landscape Craugastoridae) in Colombia. Check List 13(4): 17–20. transformation in Colombia, with emphasis in the Andean Morales, M., Otero, J., Van der Hammen, T., Torres, A., Cadena, region. Ambio 29: 432–439. C., Pedraza, C., Rodríguez, N., Franco, C., Betancourth, J.C., Etter, A., McAlpine, C., Possingham, H. (2008): Historical patterns Olaya, E., Posada, E., Cárdenas, L. (2007): Atlas de Páramos and drivers of landscape change in Colombia since 1500: a de Colombia. Bogotá, Colombia, Instituto de Investigación de regionalized spatial approach. Annals of the Association of Recursos Biológicos Alexander von Humboldt. American Geographers 98: 2–23. Naughton-Treves, L., Holland, M., Brandon, K. (2005): The role of Forero-Medina, G., Joppa, L. (2010): Representation of global and protected areas in conserving biodiversity and sustaining local national conservation priorities by Colombia’s protected area livelihoods. Annual Review of Environment and Resources 30: network. PLoS One 5: e13210. 219–252. Fund, W. (2014): Cordillera Oriental montane forests. Available Nori, N., Lemes, P., Urbina-Cardona, N., Baldo, D., Lescano, J., at: http://www.eoearth.org/view/article/151498. Accessed on 21 Loyola, R. (2015): Amphibian conservation, land-use changes January 2017. and protected areas: a global overview. Biological Conservation García-R., J.C., Castro-H., F., Cárdenas-H., H. (2005): Relationship 191: 367–374. among anurans distribution and habitat variables at La Romelia, Osorno-Muñoz, M., Ardila-Robayo, M.C., Ruiz-Carranza, P.M. Munchique National Park (Cauca, Colombia). Caldasia 27: (2001): Tres nuevas especies del género Atelopus A. M. C. 299–310. Dumeril & Bibron 1841 (Amphibia: Bufonidae) de las partes Gardner, T. (2001): Declining amphibian populations: a global altas de la Cordillera Oriental Colombiana. Caldasia 23: 509– phenomenon in conservation biology. Animal Biodiversity and 522. Conservation 24: 25–44. Parques Nacionales de Colombia. (2017): Áreas protegidas de Gaston, K.J., Jackson, S.F., Cantú-Salazar, L., Cruz-Piñón, G. Colombia. Available at: http://www.parquesnacionales.gov.co/ (2008): The ecological performance of protected areas. Annual portal/es/servicio-al-ciudadano/datos-abiertos/. Accessed on 01 review of ecology, evolution, and systematics 39: 93–113. November 2016. Gómez-Hoyos, D.A., Bolívar-García, W., Burbano-Yandi, C.E., Porter-Bolland, L., Ellis, E.A., Guariguata, M.R., Ruiz-Mallén, I., García, J.L. (2014): Evaluación poblacional y estrategia de Negrete-Yankelevich, S., Reyes-García, V. (2012): Community monitoreo para Atelopus spurrelli en el Parque Nacional Natural managed forests and forest protected areas: An assessment Utría, Colombia. Revista Biodiversidad Neotropical 4: 104– of their conservation effectiveness across the tropics. Forest 112. Ecology and Management 268: 6–17. Guevara, S.G., De la Ossa, J. (2009): Herpetofauna registrada para Primack, R., Rozzi, R., Feinsinger, P. (2001): XV. Establecimiento el área de influencia de la reserva forestal protectora Serranía de áreas protegidas. En: Fundamentos de conservación biológica: de Coraza, Colosó, Sucre, Colombia. Revista Colombiana de perspectivas latinoamericanas. México City, México, Fondo de Ciencia Animal 1: 250–258. Cultura Económica. Gutiérrez-Lamus, D.L., Serrano, V.H., Ramírez-Pinilla, M.P. Ramírez, M.P. (2016): Colección Herpetológica (anfibios) de la (2004): Composición y abundancia de anuros en dos tipos de Universidad Industrial de Santander. Version 3.0. Universidad bosque (natural y cultivado) en la cordillera Oriental colombiana. Industrial de Santander. Available at: https://doi.org/10.15472/ Caldasia 26: 245–264. 64jz3q via GBIF.org Accessed on 17 June 2017. Hoyos, J.M., Forero, I.D. (2016): Colección de anfibios del Museo Raz, L., Agudelo, H., Sarmiento, C. (2016): ICN - Universidad de Historia Natural de la Pontificia Universidad Javeriana. Nacional de Colombia. Version 2.2. Universidad Nacional de Version 4.0. Pontificia Universidad Javeriana. Available at: Colombia. Available at: https://doi.org/10.15472/v2lnzj via https://doi.org/10.15472/y6rwfq via GBIF.org. Accessed on 17 GBIF.org. Accessed on 17 June 2017. June 2017. Rivera-Correa, M. (2012): Colombian amphibians: cryptic diversity IDEAM (2010): Leyenda Nacional de Coberturas de la Tierra. and cryptic taxonomy. FrogLog 100: 36–37. Metodología CORINE Land Cover adaptada para Colombia Rivera-Correa, M., Lamadrid-Feris, F., Crawford, A.J. (2016): Escala 1:100.000. Bogotá, Colombia, Instituto de Hidrología, A new small golden frog of the genus Pristimantis (Anura: Meteorología y Estudios Ambientales. Craugastoridae) from an Andean cloud forest of Colombia. IUCN (2016): The IUCN Red List of Threatened Species. Version Amphibia-Reptilia 37: 153–166. 2016.3. Available at: https://www.iucnredlist.org. Accessed on Rodrigues, A.S.L., Akcakaya, H.R., Andelman, S.J., Bakarr, M.I., 01 February 2017. Boitani, L., Brooks, T.M., Chanson, J.S., Fishpool, L.D.C., Da Le Saout, S., Hoffmann, M., Yichuan, S., Hughes, A., Bernard, Fonseca, G.A.B., Gaston, K.J., Hoffmann, M., Marquet, P.A., C., Brooks, T.M., Bertzky, B., Butchart, S.H. M., Stuart, S.N., Pilgrim, J.D., Pressey, R.L., Schipper, J., Sechrest, W., Stuart, 696 Mónica M. Albornoz-Espinel et al.

S.N., Underhill, L.G., Waller, R.W., Watts, M.E.J., Yan, X. Sánchez-Cuervo, A.M., Aide, T.M., Clark, M.L., Etter, A. (2012): (2004): Global gap analysis: priority regions for expanding the Land cover change in Colombia: surprising forest recovery global protected-area network. BioScience 54: 1092–1100. trends between 2001 and 2010. PLoS ONE 7: e43943. Romero-Martínez, H.J., Vidal-Pastrana, C.C., Lynch, J.D., Dueñas, Sepúlveda, C., Moreira, A., Villarroel, P. (1997): Conservación P.R. (2008): Estudio preliminar de la fauna Amphibia en el biológica fuera de las áreas silvestres protegidas. Ambiente y cerro Murrucucú, Parque Natural Nacional Paramillo y zona Desarrollo 13: 48–58. amortiguadora, Tierralta, Córdoba, Colombia. Caldasia 30: SiB-Colombia, Catálogo de la Biodiversidad de Colombia. 209–229. Available at: http://www.biodiversidad.co. Accessed on 10 June Rueda-Almonacid, J.V. (1999): Anfibios y reptiles amenazados de 2017. extinción en Colombia. Revista de la Academia Colombiana de Stuart, S.N. (2012): Responding to the amphibian crisis: too little, Ciencias Exactas, Físicas y Naturales 23: 475–498. too late? Alytes 29: 9–12. Rueda-Almonacid, J.V., Hoyos, J.M. (1992): Atelopus musica, Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, nueva especie de anfibio (Anura: Bufonidae) para el Parque A.S.L., Fischman, D.L., Waller, R.W. (2004): Status and trends Nacional Natural Chingaza, Colombia. Trianea 4: 471–480. of amphibian declines and extinctions worldwide. Science 306: Rueda-Almonacid, J.V., Lynch, J.D., Amézquita, A. (2004): Libro 1783–1786. Rojo de Anfibios de Colombia. Serie Libros Rojos de Especies Toledo, V.M. (2005): Repensar la conservación:¿ Áreas naturales Amenazadas de Colombia. Conservación Internacional- protegidas o estrategia bioregional? Gaceta Ecológica 77: 67– Colombia. Bogotá, Colombia, Instituto de Ciencias Naturales, 83. Universidad Nacional de Colombia, Ministerio de Medio Vásquez-Ochoa, A., Bahamón, P., Prada, L.D., Franco-Correa, Ambiente. M. (2012): Detección y cuantificación de Batrachochytrium Rueda-Solano, L.A., Castellanos-Barliza, J. (2010): Herpetofauna dendrobatidis en anfibios de las regiones Andina Central, of Neguanje, Tayrona National Natural Park, Colombian Oriental, Orinoquia y Amazonia de Colombia. Herpetotropicos Caribbean. Acta Biológica Colombiana 15: 195–206. 8: 13–21. Rueda–Solano, L.A., Flechas, S.V., Galvis-Aparicio, M., Rocha- Venter, O., Fuller, R.A., Segan, D.B., Carwardine, J., Brooks, Usuga, A.A., Rincón-Barón, E.J., Cuadrado-Peña, B., Franke- T., Butchart, S.H.M., Di Marco, M., Iwamura, T., Joseph, L., Ante, R. (2016): Epidemiological surveillance and amphibian Grady, D.O’., Possingham, H.P., Rondinini, C., Smith, R.J., assemblage status at the Estación Experimental de San Lorenzo, Venter, M., Watson, J.E.M. (2014): Targeting global protected Sierra Nevada de Santa Marta, Colombia. Amphibian & Reptile area expansion for imperiled biodiversity. Plos Biology 12 (6): Conservation 10: 7–19. e1001891. Ruiz-Carranza, P.M., Ardila-Robayo, M.C., Lynch, J.D. (1996): Weeks, R., Russ, G.R., Alcala, A.C., and White, A.T. (2010): Lista actualizada de la fauna Amphibia de Colombia. Revista Effectiveness of marine protected areas in the Philippines for de la Academia Colombiana de Ciencias Exactas, Físicas y biodiversity conservation. Conservation Biology 24: 531–540. Naturales 20: 365–415. Zimmerer, K.S., Galt, R.E., Buck, M.V. (2004): Globalization Ruiz-Carranza, P.M., Hernández-Camacho, J.I. (1978): Una nueva and multispatial trends in the coverage of protected-Area especie Colombiana de Atelopus (Amphibia: Bufonidae). Conservation (1980–2000). Ambio 33: 520–529. Caldasia 12: 181–197. Ruiz, A., Rueda-Almonacid, J.V. (2008): Batrachochytrium dendrobatidis and chytridiomycosis in anuran amphibians of Colombia. EcoHealth 5: 27–33.

Accepted by Javier Cortés Suárez