Peru supports approximately 588 amphibian species, of which 492 have been assessed on the IUCN Red List of Threatened Species. Of these, 111 are classified as Threatened, with 69 species classified as Critically Endangered or Endangered. In addition, 140 amphibian species remain Data Deficient. We re-assessed the conservation status of 38 amphibian species originally identified as potentially Threatened by von May et al. (2008), using the IUCN Red List Categories and Criteria. Fourteen species assessments changed as a result of re-assessment, of which eight changed from Data Deficient to Threatened; two changed from Data Deficient to Near Threatened and Least Concern respectively; two were up-listed from Least Concern to a Threatened status; two were down-listed. None of the changes were due to a known genuine change since the previous assessment. All changes were justified by an increase in knowledge. The eight species with a change from Data Deficient to a Threatened category belonged to four anuran families: Craugastoridae, Dendrobatidae, Hemiphractidae and Telmatobiidae. The reasons for a change in assessment status were: changes in taxonomy, distribution, population status, threat status, or previously incorrect information. The main threat affecting re-assessed amphibian species was habitat loss, with other threats including pollution, disease outbreaks, and collection for the pet trade. Only 53% of the re-assessed species were found to occur in a protected area. Findings of this study indicate the continuing fragility of many Peruvian amphibians and highlight the need for improving their protection and for further research into their population status and threats.
Introduction
Peru supports approximately 588 amphibian species [1], of which some 278 (48%) are known to be endemic [2]. This is partly due to the large number of life zones in the country (84 life zones and 17 transitional zones) [3], including the unique and complex range of habitats and ecological conditions which occur in the montane and pre-montane forests, grasslands, and deep valleys within the Andean Cordillera and surrounding regions [4]. Between January 2010 and October 2014, 49 new amphibian species were described for Peru [2], highlighting the importance of this country's speciose amphibian fauna and the need for continued taxonomic research in this large, megadiverse country. According to the latest version of The IUCN (International Union for Conservation of Nature) Red List of Threatened Species (the IUCN Red List), there are currently 111 Threatened amphibian species in Peru, of which 28 are classified as Critically Endangered, 41 as Endangered and 42 as Vulnerable [5]. In addition, more than two-thirds of these species are endemic [6] and 140 amphibian species in Peru are classified as Data Deficient [5] due to a lack of knowledge about many aspects of species ecology, including: population status, distribution outside their type locality, and current threats. The most recent check list for Peruvian amphibians was presented by Aguilar et al. [7] listing 538 described species for Peru. Catenazzi and von May [4] reviewed this list in addition to two online databases (AmphibiaWeb [2] and Amphibian Species of the World [1]), and consulted with other herpetologists, concluding that 571 species (550 anurans, 3 salamanders, and 18 caecilians) were known to occur in Peru by early 2014. As of 17 June 2015, the two leading online databases for amphibian taxonomy list the following numbers of amphibian species for Peru: AmphibiaWeb: 561 species, Amphibian Species of the World: 588 species.
The state of conservation knowledge on Threatened amphibians in Peru was assessed by von May et al. in 2008 [6], compiling a list of 83 amphibian species for which field data were available, including species listed in the IUCN Red List and the Peruvian government's Servicio Nacional Forestal y de Fauna Silvestre (formerly the Instituto Nacional de Recursos Naturales) threatened species list. This research highlighted a number of issues relating to conservation and further research requirements, including improved surveys and monitoring of these species. Due to a lack of information at the time, 28 (34%) of the species within the 83 originally examined either had not been assessed in the IUCN Red List, or were assessed as Data Deficient. Since 2008, there have been increasing reports of threats to habitats and amphibian species in the country [8, 9, 101112–13], resulting in a pressing need to assess the extinction risk of these species, which may aid in their conservation and that of their habitats.
In this paper we re-assessed the extinction risk of a sub-set of the amphibian species originally identified as potentially Threatened by von May et al. in 2008 [6] using the IUCN Red List Categories and Criteria [14]. The IUCN Red List is widely recognized as the most comprehensive, objective global approach for evaluating the extinction risk of plant and animal species [5]. The IUCN Red List identifies particular species at risk of extinction [5], which is essential for formulating species action plans and conservation action. As a result of our present study, the IUCN Red List updated the threat status of several of these species during 2013 and 2014.
Recently, the Peruvian government issued an updated list of Threatened and Near-Threatened fauna (henceforth, the national list) that included amphibians, reptiles, birds, mammals, and invertebrates [15]. Four categories, Critically Endangered (CR), Endangered (EN), Vulnerable (VU) and Near Threatened (NT) were considered in this national assessment process (although NT is not regarded as Threatened by the IUCN), and volunteer scientists who participated in this process followed the IUCN Red List methodology for regional assessments. We compared the number of Peruvian amphibians included in each category according to both the IUCN Red List and the national list. As in von May et al. in 2008 [6], we included the NT category to allow comparisons between both lists. This comparison was motivated by the previously observed discordance between the IUCN Red List and the national list (see Fig. 2 in [6]). Finally, we propose a correction to the national list because it includes two amphibian species not known to occur in Peru.
Methods
A sub-set of 39 Peruvian amphibian species, originally presented in Appendix 2 of von May et al. [6], were used for this study. All species listed in Appendix 2 of this study were originally listed as Data Deficient, Least Concern or Not Evaluated. However subsequent assessment/re-assessment after publication of von May et al. [6] changed seven to a Threatened category (Vulnerable, Endangered or Critically Endangered). Since the publication of the original paper by von May et al. [6], six species had undergone taxonomic revisions, resulting in name changes. Gastrotheca monticola was split into two species (G. monticola and G. lojana, of which only the former was re-assessed); Hyalinobatrachium lemur was synonymised with H. pellucidum; Phrynopus ayacucho was placed into the genus Oreobates (now Oreobates ayacucho); Ranitomeya biolat and R. lamasi were synonymised with R. sirensis; and R. intermedia was synonymised with R. imitator. In addition, in 2014, after the re-assessment process had taken place, Cochranella croceopodes was synonymized with Rulyrana saxiscandens [16]. R. saxiscandens was previously assessed as Endangered, but given the change in taxonomic concept the species needs to be re-assessed. Since this occurred after the re-assessment process, we did not include it in the analysis.
We used the IUCN Species Information Service (SIS) database for entering, storing and managing data on each species, as well as for querying results. The primary database fields included: Geographic Range, Population, Habitat and Ecology, Threats, Conservation Actions, Taxonomy and Assessment Information. Distribution maps depicting species ranges and used as proxies for the extent of occurrence (EOO) or area of occupancy (AOO) were drawn or revised for each species using ESRI ArcMap (version 10.2). We also used information from field observations and published studies (i.e., studies reporting the infection caused by the chytrid fungus (e.g., [9]); presence/absence in natural protected areas (e.g. [7]). We followed the same criteria used in IUCN species assessments [14] in order to assign threats to each species. Information on threats faced by other amphibians is also available in Table 3 in [7].
To update each assessment, three main methods were used: email, online forum and primary literature. The first involved email discussion with experts in the field. These were often researchers who had published original information on each species, as well as those actively conducting research in the field. The second involved issuing a call to experts in Peruvian herpetology through the Herpetologos Perú list server to solicit information, and creating a new online forum on iNaturalist to collate this information ( www.inaturalist.org): the Perú Amphibian Red List Assessment Forum ( http://www.inaturalist.org/projects/peru-amphibian-redlist-assessment-forum). The forum allowed researchers and, in some cases, citizen-scientists, to post their observations and provide feedback on the draft IUCN Red List assessments. This facilitated reaching a wider audience and allowed findings to be documented that may otherwise have gone unrecorded. The open, easy-to-use online format made documenting these data relatively simple. Although reports of many amphibian species, endemic to Perú were recorded on this forum, relatively few (less than 20) comments related to the species under re-assessment. This may be due to the small geographic distribution range of many of the species along with lack of survey effort.
The third method of obtaining information on the status of the amphibian species involved searching literature published since 2008. This comprised a range of peer-reviewed and other publications, including on-line internet resources. Websites containing relevant information were consulted, but the material was always confirmed with experts in the field. Once information had been collated and documented in SIS, each species was re-assessed using the current versions of the IUCN Red List Categories and Criteria and the Guidelines for Using the IUCN Red List Categories and Criteria [14]. Once completed, all submitted assessments were reviewed by at least one external Reviewer designated by the Amphibian Red List Authority (RLA), and finally, consistency was checked by the Red List Unit before being published on the IUCN Red List.
Results
A total of 38 Peruvian amphibian species were re-assessed. Fourteen species re-assessments (37%) resulted in a change of status, while the remaining 24 remained unchanged (Appendix 1). Of the 14 species that underwent an assessment change, eight changed from Data Deficient to Threatened (21%), two changed from Data Deficient to Near Threatened and Least Concern respectively (5%), two were up-listed from Least Concern to Threatened (5%) and two were down-listed (5%). None of the changes in assessment were as a result of a known genuine change in status since the previous assessment; all were due to an increase in knowledge of one or more factors (IUCN criteria A–E) used to evaluate if a taxon belongs in a Threatened category (e.g. population reduction, small population size and decline) [14]. The species that changed from Data Deficient to Threatened came from four anuran families: Craugastoridae, Dendrobatidae, Hemiphractidae and Telmatobiidae. Twenty-four species (63%) had no change in their assessment status. Of these, 11 were Least Concern and nine were Data Deficient, with the remaining four listed as Vulnerable, Endangered, or Critically Endangered.
Species assessments changing from Data Deficient and up-listed species
Appendix 2 summarises the main reasons for changes in assessment status, which can be broadly classified into five categories, due to changes in: taxonomy, distribution, population status, threat status, or inaccurate information. For all species, new information or a combination of the above factors was responsible for a change in assessment status.
Of the 12 species with a change in status that was not a down-listing, three had new information on distribution (Ameerega pongoensis, Oreobates ayacucho and Ranitomeya flavovittata) and were previously assessed as Data Deficient. Two species (Phrynopus peruanus and Telmatobius atahualpai) were experiencing habitat loss or fragmentation. For two species, there was a reduction in population status or number of mature individuals noted (Silverstone's Poison Frog Ameerega silverstonei and Telmatobius timens). Two species, Pristimantis ornatus and Pristimantis cruciocularis, were previously assessed based on information that is now considered inaccurate or inaccurate application of criteria. Both of these species were presumed to have much wider distributions. New information relating to specific threats and/or new information on distribution were the biggest factors leading to a change in assessment of nine species (Ameerega pongoensis, Ameerega silverstonei, Gastrotheca atympana, Oreobates ayacucho, Phrynopus peruanus, Pristimantis pardalinus, Ranitomeya flavovittata, Telmatobius atahualpai and T. timens).
Down-listed species
As a result of taxonomic revisions, Hyalinobatrachium lemur, formerly assessed as Endangered, was synonymised under H. pellucidum. This change resulted in the known distribution of H. pellucidum being much larger, thus being classified as Near Threatened. Ranitomeya biolat and R. lamasi were recently synonymised under R. sirensis. This synonymy resulted in a much larger distribution, and thus, the species was down-listed from Endangered to Least Concern.
Species with no change
No new information was available for over half of the species re-assessed. These 24 species (63%) comprised 15 genera, with five species belonging to the genus Ranitomeya. The only two caecilians to be re-assessed (the Ringed Caecilian Siphonops annulatus and Epicrionops bicolor) retained the same status. Of the nine species still listed as Data Deficient, a continuing lack of data was the main reason for a lack in change of status.
Threats
The main threat affecting the 38 re-assessed species was habitat loss, primarily due to logging and agriculture, with 29 (76%) species being affected (Appendix 1). Other threats included pollution from mining operations, chytrid infection, tourism development resulting in disturbance and habitat loss, and collection for the pet trade. Figure 1 shows the threats affecting Threatened (Critically Endangered, Endangered and Vulnerable), non-Threatened (Near Threatened, Least Concern) and Data Deficient species. For four of the species, the threats were unknown. The biggest threats to species of Ranitomeya are potential habitat loss due to logging and illegal collecting for the pet trade, though the degree to which the latter is a problem remains unknown. Human-induced fires are considered a threat to two montane species: Phrynopus peruanus and Pleurodema marmoratum. The Harlequin Frog Atelopus patazensis, one of the most highly Threatened species (CR), is threatened primarily with chytridiomycosis and stream mining operations.
Presence in protected areas
A total of 20 species (53%) are known to occur in at least one protected area (Appendix 1), a figure based on the known occurrence of each species. An additional five species may occur in protected areas, but this needs further clarification. Five Threatened species (Atelopus patazensis, Phrynopus peruanus, Phrynopus tautzorum, Pristimantis ornatus and Pristimantis pardalinus) are not known to occur in any protected areas. These species urgently need protection of their type locality due to their limited distribution. The remaining nine Data Deficient species are not known to occur in protected habitats, but since their distributions remain poorly known, additional data may change this status. Five species are known to be in protected areas in at least part of their range.
Comparison between the IUCN Red List and the national list of Threatened species
The number of Peruvian amphibians included in each category according to The IUCN Red List was very similar to the number of Peruvian amphibians included in the national list [15] (Fig. 2). A thorough inspection of the national list further revealed that the occurrence of two amphibian species, Hemiphractus bubalus and Psychrophrynella wettsteini in Peru is uncertain given that no collections of voucher specimens (or photographic vouchers) are available from the country.
Fig. 3.
Species with a change in assessment. A. Pristimantis pardalinus. Photo R. von May; B. Phrynopus peruanus. Photo R. von May; C. Pristimantis cruciocularis. Photo A. Angulo; D. Ranitomeya flavovittata. Photo A. Angulo; E Telmatobius timens. Photo A. Catenazzi; F. Pleurodema marmoratum. Photo A. Catenazzi.
Discussion
This re-assessment of 38 amphibian species of Peru has resulted in improved understanding and consequent changes in assessment of 14 species on The IUCN Red List of Threatened Species. Eight of these species changed their status from Data Deficient to a Threatened category and two were up-listed from Least Concern to Threatened, demonstrating the potential fragility of many endemic Peruvian species. Despite an improved knowledge of the distribution and population status of these species, basic distributional and life history data are still lacking. The lack of information on the remaining nine Data Deficient species should be of great concern, considering the continued decline in many Threatened species in Peru and of their habitats. The IUCN Red List Index (RLI) measures trends in the overall extinction risk of sets of species, as an indicator of trends in the status of biodiversity [17]. The RLI is based on the movement of species status through the IUCN Red List Categories [17]. However, since no species in this re-assessment underwent a known genuine change, this tool could not be used.
It is encouraging that, for Peruvian amphibians, there is currently more congruence between The IUCN Red List of Threatened Species and the national list of threatened fauna recognized by the Peruvian government (Figure 2). The close similarity between both lists is in part a result of the application of the IUCN Red List methodology in Peru's national assessments of threatened and near-threatened wildlife [15], and represents a considerable improvement over a previous national assessment [18].
Threats to species
Habitat loss was identified as a major threat to over three quarters (76%) of the 38 amphibian species in this re-assessment. Globally, loss and alteration of habitats is cited as one of the biggest factors contributing to amphibian declines [19, 20, 21] and is considered a major threat to amphibians in Peru [4]. The Global Amphibian Assessment (GAA) identified habitat loss as affecting 89% of all Threatened species in the New World [22]. In the majority of cases, individual species are being affected by multiple threats. This may result in synergistic interactions and possible population declines, both of which have been documented in many amphibian populations worldwide [23, 24, 25].
According to Catenazzi & von May [4], the most Threatened amphibian species in Peru belong to five amphibian families: Craugastoridae, Telmatobiidae, Bufonidae, Dendrobatidae and Centrolenidae. Findings from our re-assessment of Peruvian species support this statement, with 21% of the total re-assessed belonging to two of these families: Dendrobatidae and Craugastoridae. In Peru, the two main threats to dendrobatids appear to be habitat loss due to agriculture [26] and illegal harvesting for the pet trade [6, 27, 28]. The latter could be an increasing problem for these and other species within the genera Ranitomeya and Ameerega [28, 29]. The extent of these threats is largely unknown for most of the poison dart frogs belonging to Ranitomeya, where additional research is required.
Over half (60%) of the species with a change in threat status belong to Craugastoridae, specifically in the genera Pristimantis and Phrynopus. Species belonging to these genera are terrestrial breeding frogs that are threatened with habitat loss, primarily through agricultural expansion in the form of extensive cattle grazing [30]. The majority are high-elevation species, usually with small ranges, and are vulnerable to human habitat modification. Grass burning to fertilise fields and subsequent habitat loss have resulted in reported habitat decline in some areas, especially in the case of Phrynopus peruanus and Oreobates ayacucho [31]. The remaining six species within these genera are all assessed as Data Deficient, with virtually no information available on population, distribution, or threats affecting these species.
Several members of the Telmatobiidae are at risk from water pollution, chytridiomycosis, intensive livestock farming and collection for food [4, 9, 32, 33, 34]. Telmatobius atahualpai and T. timens are threatened due to pollution of water bodies, intensive livestock farming driving habitat loss and chytridiomycosis [9, 35]. They could also be threatened by harvesting for human consumption and impacts of introduced freshwater species [4]. Chytridiomycosis has been cited as a key threat to amphibian populations within Peru [4, 9, 36], especially those within Atelopus and Telmatobius genera [9, 10, 13, 37]. Synergistic interactions between disease and habitat loss could be exacerbating population losses of T. atahualpai and T. timens, which are currently assessed as Near Threatened and Critically Endangered, respectively.
All known individuals within Gastrotheca atympana (family: Hemiphractidae) were recorded in a reserve, Pampa Hermosa National Sanctuary, which is surrounded by primary forest. However, the area is facing ongoing threats including encroaching illegal logging, slash and burn agriculture, mining activities and road construction [38]. It is estimated that 85% of the habitat beyond Pampa Hermosa's buffer zone has been lost due to deforestation [39]. Although classified as Vulnerable (VU D2) in this latest assessment, due to the potential severity of the threats, future assessments may further up-list this species. In addition, protection of the primary forests surrounding this reserve is required.
Species in protected areas
This study revealed that 53% of the species examined had some part of their known distributions within a protected area. The remaining species either have no formal protection or the degree of protection is unknown. This is consistent with recent findings at the global level [40]. Considering that habitat loss is the main threat to amphibians in Peru [4], there is an urgent need to protect these species' habitats. Of the re-assessed species, just three (8%) occur within Manu National Park, which is Peru's second largest protected area [9]. However, in recent years, in frog communities between 1,200 m and 3,700 m asl, 47% fewer frog species of Manu's montane forests were recorded in 2008/2009 compared to 1999 [9]. The causes of the declines are unknown, but chytridiomycosis appears to be the main suspect in declines [41], and has been implicated in at least 10% of the species re-assessed. These findings are of concern and strongly suggest that additional conservation strategies are required to address population declines when diseases are identified as a potential driver.
Changes in species' taxonomic resolution
Changes in taxonomy, and therefore in the biological concept of the assessed populations/species, have the potential to significantly impact species' extinction risk assessments [42]. In the case of taxonomic splits (a common scenario where cryptic species complexes are concerned), while it is possible that extinction risk may increase or decrease, as ranges become more circumscribed and assuming threats continue, many species will likely experience an increase in their extinction risk. Similarly, in the case of taxonomic synonymizations, while extinction risk can increase or decrease, it is likely to decrease as ranges typically increase with the amalgamation of new populations into the new species concept. In this instance, the scenario of decreased extinction risk is evidenced by our results, where the synonymy with Ranitomeya biolat and R. lamasi rendered the previously Endangered Ranitomeya sirensis as Least Concern, and the synonymy of Hyalinobatrachium lemur into H. pellucidum changed the latter species' assessment from Endangered to Near Threatened. While it is difficult to predict exactly how extinction risk may change as a result of taxonomic change (these will vary on a case by case basis), we should expect to see more changes in extinction risk assessments as more changes take place in amphibian taxonomy.
Implications for conservation
Up-to-date Red List assessments are crucial for understanding the geographic distribution, population size and threats which may affect species, all of which are required for effective conservation programmes. Our research will enable conservation programmes and protection to target the specific needs of these species. In addition, our research has highlighted three further areas as priorities for future work. First, basic life history information on the ecology, distribution and threats affecting species needs to be collected for the remaining nine Data Deficient species. For many of these species, records only exist for the holotype or a limited number of specimens collected at the type locality, particularly those within the genus Phrynopus (e.g. Phrynopus bufoides, P. kotosh and P. oblivius). Surveys and monitoring are required to determine their distribution and abundance, as well as threats affecting these species. Second, there is a need for more detailed information on the status and degree to which threats are impacting the highly Threatened species, assessed as Critically Endangered or Endangered. In particular, further research, monitoring and protection are required for Atelopus patazensis, Phrynopus peruanus, P. tautzorum, Pristimantis pardalinus and Telmatobius timens, which are experiencing population or habitat declines, or both. Third, some Least Concern species appear to be at risk of becoming Near Threatened in the coming years, especially Pleurodema marmoratum and Rhinella limensis, populations of which appear to have declined and are under increasing threats. Therefore, programmes to monitor their population status are required.
It is important that findings of studies such as the ones reported here make it into relevant conservation plans and national policy. By virtue of being published on The IUCN Red List of Threatened Species the information is publicly available and can be used to inform granting agencies where to best channel their conservation investments. In addition, the authors are committed to ensuring that relevant national authorities are made aware of updates and changes to inform necessary policy action. We are also committed to sharing the results of this study and engage in discussions with relevant parties and stakeholders.
Overall, our findings indicate the continuing fragility of many Peruvian amphibians and highlight the need for improving their protection and for further research into their population status and threats.
Acknowledgments
We thank all contributors to the Peru Amphibian Red List Assessment Forum who contributed valuable information relating to the observed distribution and threats affecting amphibian species in Peru. We are grateful to the Amphibian Red List Authority, and in particular Jennifer Luedtke, for assessment reviews, and the IUCN Red List Unit, especially Caroline Pollock, who kindly provided queries from the IUCN Species Information Service (SIS) Toolkit. Thanks are also due to Steve Bunce at Epping Forest Field Centre for providing computer and internet facilities to LEJ, which were crucial for completion of this research. This is publication 4 of the Peru branch of the Amphibian Specialist Group (ASG Perú).
References
Appendices
Appendix 1.
Assessment status and change for the 38 re-assessed Peruvian amphibian species; known threats to species and recorded presence in protected areas.
Appendix 2.
Main reasons for change for the 14 Peruvian amphibian species which had a change in status.
Appendix 3.
Distribution of all 38 re-assessed Peruvian species. Full distribution information can be found at < www.iucnredlist.org>.
