Protected areas assessment for the conservation of ... - Biotaxa

Introduction

South America harbours more than 2300 of the more than 6500 known amphibian species (IUCN, 2016). However, around 600 species are listed under some type of national or international threat category, and more than 700 remain in the data deficient category (IUCN, 2016). It is well established that amphibians are one of the most threatened groups of vertebrates globally (e.g., Stuart et al., 2004; Stuart, 2012).

Colombia is ranked as a megadiverse country for amphibians, and it is home to 812 species in 14 families. The highest representation is from the families Craugastoridae (31%), Hylidae (15%), Bufonidae

(10%), Dendrobatidae (10%), and Centrolenidae (9%), and the country is classified second in South American species richness after Brazil (Rivera-Correa, 2012; Acosta-Galvis, 2017). Colombia comprises 13 ecoregions and six biomes (Sánchez-Cuervo et al., 2012) that offer suitable habitats for amphibians, and these offer a variety of climatic and orographic characteristics that doubtlessly facilitated the establishment of the observed diversity (e.g., Ruiz-Carranza et al., 1996). On the flipside, Colombia has one of the highest numbers of threatened amphibians in the world, with 277 species listed according to national and international criteria (Rueda-Almonacid et al., 2004; IUCN, 2016). Known genera for which species are declining in this country include Pristimantis, Dendrobates, Colostethus, Centrolene, and Atelopus (Rueda-Almonacid, 1999; IUCN, 2016), of which most are distributed in the Andean region, probably due to intrinsic and extrinsic factors that act synergistically (Cooper et al., 2008).

Since the late 1980s, the sudden disappearance of many amphibian populations at several sites in America, Europe, and Australia has been documented (Stuart et al., 2004), suggesting that the current extinction rate of amphibians is 105 times the estimated historical rate for the class (McCallum, 2007). These declines, in population densities as well as in diversity, continue to

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,*

1 Grupo de Investigación en Ecología y Biogeografía, Universidad de Pamplona, Barrio El Buque, Km 1, Vía a Bucaramanga, Pamplona, Colombia

2 Grupo de Investigación en Ecología y Conservación de Fauna Silvestre, Universidad Nacional de Colombia, Sede Medellín, Calle 59A No. 63-20, Medellín, Colombia

3 Programa de Doctorado en Ciencias Biológicas, Laboratorio de Biología Evolutiva, Pontificia Universidad Católica de Chile, Avenida Libertador Bernardo O’Higgins 340, Santiago, Chile

* Corresponding author e-mail: [email protected]

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

Mónica M. Albornoz-Espinel et al.686

accelerate, affecting amphibians occupying deforested and intervening spaces but also those occupying pristine and remote sectors within the country’s system of Protected Areas (PAs; Gardner, 2001; Rueda-Almonacid et al., 2004; Nori et al., 2015). Factors that contribute to the decrease of amphibians include pollution, climate change and the resulting emerging diseases, and destruction and fragmentation of habitat that create isolated patches of forest. Habitat isolation has a negative impact on biotic components, affecting dispersion patterns and gene flow of amphibians (Gardner, 2001; Rueda-Almonacid et al., 2004; Cushman, 2006).

PAs are natural regions of ecological importance that safeguard biodiversity (Dudley, 2008) over roughly 13% of the Earth’s habitable area (Bertzky et al., 2012). The rate of PA expansion has varied in different regions of the world, with North and South America representing the fastest-growing regions (Zimmerer et al., 2004). This fast rate of expansion is the result of government support, placing emphasis on PA expansion strategies (Naughton-Treves et al., 2005; Le Saout et al., 2013; Nori et al., 2015). However, gaps in the efficiency at protecting biodiversity are evident in some regions, particularly for certain organismal groups (Rodrigues et al., 2004; Venter et al., 2014; Butchart et al., 2015; Nori et al., 2015), including amphibians. Amphibians are considered the group with the most gaps in terms of protection, which is demonstrated by the high number of species that occur in the various threat categories (Rodrigues et al., 2004; IUCN, 2016).

The PA system of Colombia covers 9.98% of the national territory, and is distributed across 59 National Natural Parks and more than 700 other protected areas (Parques Nacionales de Colombia, 2017). However, the scope of protection provided by these PAs remains limited, considering that the areas with high species richness do not generally coincide with areas that may have a high number of threatened or endemic species and which are not spatially protected under any special management area (Forero-Medina and Joppa, 2010).

The Cordillera Oriental is considered one of the areas lacking information about threatened amphibian species, yet it is the region with most of the endemic species (Bernal and Lynch, 2008). Only nine National Natural Parks exist in this region as of this writing, and this small number severely limits the level of protection given to several species of amphibians. Our study in the Cordillera Oriental aims to determine the percentage of amphibian species found there that are listed as threatened by the International Union for the Conservation of Nature (IUCN) and in the Red Book

of Amphibians of Colombia (Rueda-Almonacid et al., 2004), both inside and outside the PAs. In parallel, we assessed the conservation status of amphibians using information on changes in land coverage where occurrences of threatened amphibian species have been registered.

Materials and Methods

Study site.—The study was carried out in the Cordillera Oriental of Colombia, including the inter-Andean valley of the Magdalena River (Fig. 1). This region is one of the three main branches into which the Andean Cordillera in Colombia is divided. The region extends in a southwest-to-northeast direction from the Colombian Massif in Cauca to the Serranía de Perijá in La Guajira (Morales et al., 2007). Different life zones are represented within this ecoregion, including premontane humid forest, montane forest, rainforest, and premontane dry forest, with foothills supporting forests in the south that are connected to the humid forests of the northwestern Amazonas (Fund, 2014).

Data collection.—A list of threatened amphibian species in the Cordillera Oriental was assembled and species were categorized as Vulnerable, Endangered, or Critically Endangered according to IUCN criteria and the Red Book of Amphibians of Colombia (Rueda-Almonacid et al., 2004). Once species were identified, a search of their occurrences was conducted by reviewing scientific publications, original descriptions, online databases (IUCN, SiB-Colombia, Amphibian Species of the World, HerpNET, GBIF, ICN online collection at the Universidad Nacional de Colombia), and an on-site review of the biological collection of amphibians at the Insituto de Ciencias Naturales at the Universidad Nacional de Colombia and the biological Collection José Celestino Mutis at the University of Pamplona. At the same time, we included the time interval between the oldest record, taken from the original descriptions, and the most recent record, obtained from scientific publications and a review of national and international databases.

Each amphibian record was verified by checking against the original description and examination of museum specimen, and each geographic record was georeferenced using ArcGIS 10.1 (ESRI, 2011), producing a buffer of 500 m around each record to represent a possible margin of error for the locality. We then developed a database of amphibian species to determine the historical distribution of each species. This database was later supplemented with information

on the conservation status of each species, type of vegetation, and year of the last sighting.

The layers associated with PAs in the database were obtained from the Parques Nacionales de Colombia (2017). One hundred and ninety PAs corresponding to the Cordillera Oriental and some of the Orinoquía and Amazonia of Colombia were selected. These PAs included National Natural Parks (NNP = 16; Parques Nacionales Naturales de Colombia), Fauna and Flora Sanctuaries (SFF = 3; Santuarios de Flora y Fauna), Regional Natural Parks (RNP = 18; Parques Naturales Regionales), National Protective Forest Reserves (NPFR = 32; Reservas Forestales Protectoras Nacionales), Regional Protective Forest Reserves (RPFR = 40; Reservas Forestales Protectoras Regionales), Regional Districts of Integrated Management (IMRD = 22; Distritos Regionales de Manejo Integrado), Civil Society Natural Reserves (RNSC = 58; Reservas Naturales de la Sociedad Civil), and Unique Natural Areas (ANU = 1; Area Natural Única).

Land cover was classified as páramo, mature forest, secondary forest, fragmented forest, riverine forest,

grassland, crop, and urban area. These categories were established using the spatial layers of land cover from 2005–2009 (scale 1:100,000) (IDEAM, 2010).

Analysis.—For the historical record of each assessed amphibian species, we overlapped layers of land cover and PAs using ArcGIS 10.1 (ESRI, 2011). This technique produced spatial relationships from which we determined the frequency of geographical records available for each species inside and outside the PAs. Historical records and reports of year of last sighting for each species of amphibian were evaluated, and the descriptions of the original habitats were compared with recent layers on land cover.

Results

Numbers of amphibian species and PAs.—Fifty-two species of threatened amphibians in all endangered categories were analysed from 509 geographical records compiled for the entire Cordillera Oriental (Fig. 1). Of the 190 selected PAs, amphibians were only recorded in 25 PAs, specifically nine National Natural Parks, one

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

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. 1 PA1 / IUCN Category2 Date established

as PA Species Records

NNP Chingaza / II 1977

Atelopus lozanoi 3 Atelopus mandingues 2 Atelopus muisca 8 Pristimantis affinis 2 Pristimantis carranguerorum 1 Pristimantis elegans 8 Pristimantis frater 1

NNP Serranía de Los Yariguíes / II 2005

Bolitoglossa lozanoi 4 Hyloscirtus denticulentus 1 Pristimantis bacchus 4 Pristimantis bicolor 6 Pristimantis merostictus 3 Rulyrana adiazeta 2

NNP Tamá / II

1977

Allobates juanii 1 Pristimantis frater 2 Tachiramantis douglasi 1

NNP Pisba / II 1977 Atelopus marinkellei 1

NNP Sumapaz / II 1997 Pristimantis elegans 2 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

SFF Guanentá Alto Río Fonce / IV 1993

Atelopus mittermeieri 2 Atelopus monohernandezi 2 Centrolene buckleyi 1 Hyloscirtus piceigularis 1 Pristimantis bacchus 2 Pristimantis elegans 1 Pristimantis jorgevelosai 1 Pristimantis merostictus 3

Centrolene buckleyi 1


Hyalinobatrachium ibama 1Hyloscirtus piceigularis 1Pristimantis bicolor 3Pristimantis jorgevelosai 2Pristimantis merostictus 6

RNP El Rasgon / II 2009

Tachiramantis douglasi 3

Hyloscirtus lynchi 2Pristimantis bicolor 1Pristimantis jorgevelosai 2

RNP Cerro La Judía / II 2009


Atelopus lozanoi 1RNP 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 2Hyloxalus edwardsi 1FRPN Bosque Oriental de Bogotá / VI 1976

Pristimantis elegans 4

Atelopus lozanoi 1FRPN Ríos Blanco y Negro / VI 1990

Atelopus muisca 1

FRPN Quebrada Honda / VI 1945 Allobates juanii 1

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


FRPR Colombia / VI 2008 Atelopus mandingues 1

FRPR Cuchilla de Peñas Blancas / VI 1983 Hyloxalus vergeli 1

Andinobates virolinensis 5Atelopus mittermeieri 3Atelopus monohernandezi 3Hyalinobatrachium ibama 1Hyloscirtus denticulentus 1Hyloscirtus lynchi 1Hyloscirtus piceigularis 1Pristimantis acutirostris 3Pristimantis bacchus 3

RDIM Páramos Guantiva-La Rusia / VI 2011

Pristimantis bicolor 6

Sanctuary of Fauna and Flora, five Regional Natural Parks, three National Protective Forest Reserves, three Regional Protective Forest Reserves, three Regional Integrated Management Districts, and one Civil Society Natural Reserves (Table 1).

In relation to the date of creation of the protected areas, the majority of national parks in the Cordillera Oriental were created in the 1970s, sheltering more than 20 species of which some (e.g., Atelopus marinkellei, Pristimantis affinis, P. elegans, P. frater) were described before the of the PA was established (Table 1). However, some NNPs, including the Serranía de Los Yariguíes and the Serranía del Perijá, were created after 2000, and the NNP Sumapaz in the 1990s. These now harbor eight threatened species, mainly in the NNP Los Yariguíes (Table 1).

Species records inside and outside of PAs.—Evaluation of the geographical distribution of the amphibian species showed that 33 species (63%) represented by 160 geographical records (31%) were reported at least once in a protected area (Fig. 2A, PAs). However, just 19 species (36%) were reported in at least one National Natural Park (Table 1). In contrast, all evaluated species were recorded outside PAs (353 geographical records; 69%; Fig. 2A, OPAs). Concerning the threat categories, nine Critically Endangered species (17%) are found within protected areas and 14 (27%) outside, 11 Endangered species (21%) within and 16 (31%) outside, and 12 Vulnerable (21%) within and 22 (42%) outside (Fig. 2B).

Of the PAs with the largest area (10,000–60,000 ha), SFF Guanentá Alto Río Fonce holds the largest number


Table 1. Continued.Table 1. Amphibian species in protected areas (PAs) in the Cordillera Oriental of Colombia. 1 PA1 / IUCN Category2 Date established

as PA Species Records

NNP Chingaza / II 1977

Atelopus lozanoi 3 Atelopus mandingues 2 Atelopus muisca 8 Pristimantis affinis 2 Pristimantis carranguerorum 1 Pristimantis elegans 8 Pristimantis frater 1

NNP Serranía de Los Yariguíes / II 2005

Bolitoglossa lozanoi 4 Hyloscirtus denticulentus 1 Pristimantis bacchus 4 Pristimantis bicolor 6 Pristimantis merostictus 3 Rulyrana adiazeta 2

NNP Tamá / II

1977

Allobates juanii 1 Pristimantis frater 2 Tachiramantis douglasi 1

NNP Pisba / II 1977 Atelopus marinkellei 1

NNP Sumapaz / II 1997 Pristimantis elegans 2 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

SFF Guanentá Alto Río Fonce / IV 1993

Atelopus mittermeieri 2 Atelopus monohernandezi 2 Centrolene buckleyi 1 Hyloscirtus piceigularis 1 Pristimantis bacchus 2 Pristimantis elegans 1 Pristimantis jorgevelosai 1 Pristimantis merostictus 3

Centrolene buckleyi 1

Hyalinobatrachium ibama 1Hyloscirtus piceigularis 1Pristimantis bicolor 3Pristimantis jorgevelosai 2Pristimantis merostictus 6

RNP El Rasgon / II 2009


Hyloscirtus lynchi 2Pristimantis bicolor 1Pristimantis jorgevelosai 2

RNP Cerro La Judía / II 2009


Atelopus lozanoi 1RNP 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 2Hyloxalus edwardsi 1FRPN Bosque Oriental de Bogotá / VI 1976


Atelopus lozanoi 1FRPN Ríos Blanco y Negro / VI 1990

Atelopus muisca 1

FRPN Quebrada Honda / VI 1945 Allobates juanii 1

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


FRPR Colombia / VI 2008 Atelopus mandingues 1

FRPR Cuchilla de Peñas Blancas / VI 1983 Hyloxalus vergeli 1

Andinobates virolinensis 5Atelopus mittermeieri 3Atelopus monohernandezi 3Hyalinobatrachium ibama 1Hyloscirtus denticulentus 1Hyloscirtus lynchi 1Hyloscirtus piceigularis 1Pristimantis acutirostris 3Pristimantis bacchus 3

RDIM Páramos Guantiva-La Rusia / VI 2011

Pristimantis bicolor 6Pristimantis elegans 1 Pristimantis merostictus 3 Pristimantis renjiforum 3 Rulyrana adiazeta 1 Strabomantis ingeri 2

RDIM Rio Subachoque y Pantano de Arcey / VI 1997 Pristimantis elegans 2 RDIM Salto de Tequendama y Cerro Manjui / VI 1999 Bolitoglossa capitana 1 RNCS El Horadero de San Alejo / VI 2008 Hyloxalus edwardsi 1 1 Protected area categories: National Natural Parks (NNP), Fauna and Flora Sanctuaries (SFF), Regional 2

Natural Parks (RNP), National Protective Forest Reserves (NPFR), Regional Protective Forest Reserves 3 (RPFR), Regional Districts of Integrated Management (IMRD), Civil Society Natural Reserves (RNSC), 4 and Unique Natural Areas (ANU). 5

2 Protected Area Categories IUCN: II = National Park, IV = Habitat/Species Management Area, VI = 6 Protected area with sustainable use of natural resources. 7

8 9

of species (n = 8), followed by the NNP Chingaza (n = 7) and the NNP Serranía de los Yariguíes (n = 6) (Table 1). In comparison, the largest number of geographical records of amphibians was concentrated in small natural reserves and protection zones (< 10,000 ha), such as the Páramo Guantiva - La Rusia (n = 15 species) (Table 1).

Land cover and geographical records of amphibians.—For areas outside the PAs 44 species (85%) with 213 records (42%) were recorded in areas that currently have some degree of disturbance of the vegetation (crops, forest fragmentation) (Table 2, Fig. 2C, OPAs). Among areas within PAs, 18 species (35%) have 41 records (8%) in areas modified by human activity (Table 2, Fig. 2C, PAs).

Whereas 46 species (88%) represented by 141 geographical records (28%) were outside of any PA (Fig. 2D, OPAs), the areas from which these records derive currently have an acceptable vegetation cover. A total of 116 geographical records (23%), corresponding to 29 species, were within a PA with vegetation cover (Table 2, Fig. 2D, PAs).

Collected reports and original descriptions of each examined species show that species originally occupied

habitat that has now been transformed from pristine forest to areas with mosaics of fragmented forests, crops, or pastures (Table 2), as evidenced by the high number of records that currently overlap areas of crops (22%) and grasslands (19%), representing by more than 70% of the species (Table 2, Fig. 3). Nevertheless, within the PAs most records (11%) fall in areas that still retain mature forests (Table 2, Fig. 3).

Discussion

Our findings confirm the limited level of conservation that most species of amphibians have in the Cordillera Oriental of Colombia. We show that these species are not well represented regarding their distribution in PAs, with just 25 of the 190 PAs in the Cordillera Oriental harbouring threatened amphibians. All assessed species were recorded at least once outside PAs, with 37% of species without any PA protection at all (Table 2). However, 63% of species have limited presence in some areas with environmental protection (Table 2). For example, seven species of more threatened genera, such as Atelopus, are represented within a PA. However, three species in this genus (A. minutulus, A.

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.



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.

Year of Species Red List Status1

description last seen2

Original habitat3

Land cover (2005–2009)4

Records in PAs

Source for when last seen5

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. 3 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.5 MCNUP-H = Museo de Ciencias Naturales – Universidad de Pamplona, Colombia. ANDES-A = Museo de Historia Natural, Colección de Anfibios –

Universidad de Los Andes, Colombia. MHN-UIS-A = Museo de Historia Natural, Colección Herpetológica (Anfibios) – Universidad Industrial de Santander, Colombia (Ramírez, 2016). ICN = Instituto de Ciencias Naturales – Universidad Nacional, Colombia (Raz et al., 2016). IAvH = Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Colombia. MPUJ = Museo de Historia Natural – Pontificia Universidad Javeriana, Colombia (Hoyos and Forero, 2016). IUCN = International Union for Conservation of Nature. MHUA = Museo de Herpetología – Universidad de Antioquia, Colombia (Daza, 2016). MLS = Museo de La Salle, Colombia (Espitia, 2016).

pedimarmoratus, A. subornatus) were only recorded outside of PAs, with the last geographical records dating back to 1984, 1990, and 1999, respectively. Similarly, the majority of species with occurrences are currently found in areas with human impact (primarily crops) (Fig. 3). Association with this habitat type could be causing local extinctions, given that most of these species were historically associated with areas covered by forest or páramo, which have been gradually lost. This information reinforces the need to establish new PAs, or expand existing ones, in order to safeguard threatened amphibian populations that may currently only occur outside PAs. However, resources and funds for the acquisition of habitat is generally limited. Thus, expansion efforts must be accompanied by the proper management of existing PAs (Naughton-Treves et al., 2005; Le Saout et al., 2013). Moreover, the need to increase studies that allow identification of remnant

populations of some amphibian species, especially those without recent sightings, is paramount. Locations such as Chingaza, Pisba, and the Cordillera de Los Picachos, areas that may harbour remnant populations of Atelopus species, would be important to survey. These National Natural Parks (NNPs) may also harbour indicated species of the genus Pristimantis, which includes the largest number of threatened species in the Cordillera Oriental (IUCN, 2016). Furthermore, it is necessary to undertake surveys to determin the diversity in PAs and surrounding buffer areas, since in the Cordillera Oriental studies on the diversity, conservation, and ecology are generally still very limited. We highlight the work conducted in areas like SFF Guanentá, where 14 species were found, with Pristimantis being the dominant genus (Gutiérrez-Lamus et al., 2004). The discovery of new species, such as Atelopis muisca (Rueda-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.

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

Year of Species Red List Status1

description last seen2

Original habitat3

Land cover (2005–2009)4

Records in PAs

Source for when last seen5

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

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. 3 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.5 MCNUP-H = Museo de Ciencias Naturales – Universidad de Pamplona, Colombia. ANDES-A = Museo de Historia Natural, Colección de Anfibios –

Universidad de Los Andes, Colombia. MHN-UIS-A = Museo de Historia Natural, Colección Herpetológica (Anfibios) – Universidad Industrial de Santander, Colombia (Ramírez, 2016). ICN = Instituto de Ciencias Naturales – Universidad Nacional, Colombia (Raz et al., 2016). IAvH = Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Colombia. MPUJ = Museo de Historia Natural – Pontificia Universidad Javeriana, Colombia (Hoyos and Forero, 2016). IUCN = International Union for Conservation of Nature. MHUA = Museo de Herpetología – Universidad de Antioquia, Colombia (Daza, 2016). MLS = Museo de La Salle, Colombia (Espitia, 2016).

(Rivera-Correa et al., 2016) in the NNP Chingaza, A. guitarraensis in the NNP Sumapaz (Osorno-Muñoz et al., 2001), and Bolitoglossa leandrae and B. tamaense in the NNP Tamá (Acevedo et al., 2013) are also important indicators for our lack of knowledge of the area. Also, there is a need to study the natural history of little-known species, such as Gastrotheca helenae (Acevedo et al., 2011). Another essential factor is to establish appropriate protocols to diagnose emerging diseases, such as chytridiomycosis, a disease caused by the fungus Batrachochytrium dendrobatidis (Bd), which has been proven to reduce taxonomic diversity (Crawford et al., 2010). This fungus was previously reported in Colombia (Ruiz and Rueda-Almonacid, 2008), where it was reported to infect species in the Cordillera Oriental (Ruíz and Rueda-Almonacid, 2008; Vásquez-Ochoa et al., 2012; Acevedo et al., 2016a,b). According to these data, 23 infected species were present in NNP Tamá in northeastern Colombia (Acevedo et al., 2016a,b). Populations of Atelopus muisca, A. lozanoi, Bolitoglossa adspersa, and Hyloxalus subpunctatus are declining in the NNP Chingaza (Rueda-Almonacid et al., 2004, Ruíz and Rueda-Almonacid 2008). Thus, this PA and several areas outside PAs should receive the highest priority for protection when generating initiatives to conserve amphibian species in the country (Rueda-Almonacid, 1999).

Fortunately, in the Cordillera Occidental important contributions to the knowledge of amphibians have been made from studies in PAs. For example, in NNP Munchique eight species of the genus Pristimantis have been reported (García-R. et al., 2005). In the PNN Paramillo 52 species, mostly of the genus Pristimantis (19.2% of the total) have been sighted (Romero-Martínez et al., 2008). In another type of PA, the nature reserves Maravelez, Panabi, Madremonte, Acaime, and El Bosque in the department of Quindío, studies have allowed the characterization of the amphibians diversity, comprising mainly species in the genus Pristimantis (69% of the total); diversity in this genus is apparently a prominent feature in most areas in western Colombia (Cadavid et al., 2005). Furthermore, new species have been described from specimens collected within PAs, including Atelopus carauta in the NNP Las Orquideas (Ruiz-Carranza and Hernández-Camacho, 1978) and Bolitoglossa tatamae in the NNP Tatamá (Acosta and Hoyos, 2006). The status of species under threat has been evaluated in PAs, including A. spurrelli in the NNP Utria in the Department of Chocó (Gomez-Hoyos et al., 2014). On the other hand, in PAs located outside the Andean cordillera work has also been conducted, and

a finding of 11 amphibian species was reported from the NNP Tayrona, including Dendrobates truncatus and Colostethus ruthveni (Rueda-Solano and Castellanos-Barliza, 2010). Epidemiological surveillance and monitoring of key amphibian species has been done in the Sierra Nevada de Santa Marta (Rueda-Solano et al., 2016). Guevara and De la Ossa (2009) found 17 species, predominantly in the family Hylidae (6 species), in the RFP Serrania de Coraza in the Department of Sucre.

Fully 25% of amphibian species worldwide are not protected within PAs (Nori et al., 2015), indicating that PAs are not completely achieving the conservation objectives of protecting all biological diversity (Primack et al., 2001; Weeks et al., 2010; Porter-Bolland et al., 2012), which especially includes conservation of rare or endangered species (Toledo 2005; Gaston et al., 2008).

Of the 25 PAs we evaluated (Table 1), according to the Protected Areas Categories of IUCN (Dudley, 2008), none could be considered in Category Ia (Strict Nature Reserve) and Ib (Wilderness Area), defined as areas where there is little or no alteration of ecosystems, have no human occupation, and have a management and strict protection to ensure their conservation, and that in addition the scientific research and the monitoring of species and ecosystems are paramount (Chape et al. 2005; Dudley, 2008). Among the PAs with records of amphibians, only 14 (9 NNP and 5 RNP; Table 1) correspond to Category II, identified as areas that are typically large and have good ecosystem function, though they may need an appropriate ecological management and maintenance of areas of protection outside limits of the PAs, such as buffer zones (Dudley, 2008).

Other areas were found in Category IV (6 RFP, 3 RDIM, 1 RSNC; Table 1) characterized as help protect or restore ecosystems altered, maintaining species of flora of international, national or local significance, and which usually have a varied area in terms of size, being generally small (Dudley, 2008). One PA is placed in Category VI (Sanctuary of Flora and Fauna Guanentá Alto Río Fonce; Table 1), which is characterized by the conservation of ecosystems and habitats associated to cultural values and traditional systems of natural resource management. They are usually large, with the greater part of the area under natural conditions (Dudley, 2008).

Therefore, the low level of protection granting by PAs and the high number of records outside the protected areas threatens the species’ long-term survival, especially those that are most threatened, taking into account the types of land use mostly present in PAs included in the category IV and the accelerated processes of


transformation and fragmentation of the coverage of natural in the Andes of Colombia (Etter and Villa, 2000; Etter and Van-Wynngaarden, 2000; Etter et al., 2008), even within protected areas (Armenteras et al., 2003, 2009) thus, in addition to generating new PAs to ensure the conservation of biological diversity (Sepulveda et al, 1997), reassessing the current PA protection category, and national parks and regional corporations should encourage frequent studies of surveys and monitoring of the populations of amphibians threatened within and outside protected areas.

Acknowledgments. Special thanks to the Vicerrectoría Académica and the Vicerrectoría de Investigaciones at the Universidad de Pamplona for their student research program. Thanks to John D. Lynch at the Universidad Nacional de Colombia, and to National Natural Parks of Colombia. We also thank L. Sánchez for a review of the text and the reviewers for their valuable comments that helped to improve this manuscript significantly.

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