Un analisis actualizado de la distribucion de especies de carnivoros peruanos listados por CITES para prioridades de conservacion.
For effective conservation of species, researchers and managers require knowledge of its current distribution, population status, ecological requirements, among other factors (Wilson, 2000). Furthermore, the knowledge of historical and contemporary species distribution ranges is important especially for wide ranging and endangered species (Morrison et al., 2007). Baseline distributions can be used to assess changes in distribution ranges and determine expansions or reductions of populations after human colonization, exotic species introductions, extirpation of top predators, climate change, conservation efforts, and identify research gaps (Abbitt and Scott, 2001; Senyatso et al., 2012; Ripple et al., 2013; Rochlin et al., 2013; Ogutu et al., 2014; Parlato et al., 2015). The Order Carnivora consists of medium- to large-sized mammals that often need extensive areas to fulfill their basic habitat and resource requirements, and therefore are greatly affected by anthropogenic disturbances (Gittleman and Harvey, 1982; Noss et al., 1996). The need for large spatial areas, naturally low population densities, high persecution by humans, and vulnerability to habitat fragmentation, deforestation, and climate change make extinction risk higher for Carnivora than for other species (Woodroffe and Ginsberg, 1998; Crooks, 2002; Voigt et al., 2003; Cardillo et al., 2005; Ordenana et al., 2010; McCain and King, 2014). Moreover, because of their extensive spatial requirements and unique ecosystem functions, such as top-down control of a food chain (Terborgh, 1988), most carnivores can be considered keystone species, contributing to the balance of the ecosystem by maintaining its structure, regulating prey densities and avoiding competitive exclusion (Ucarli, 2011; Ripple et al., 2013; Ripple et al., 2014 ). Furthermore, the habitat conservation of large areas to protect some of these carnivores will indirectly aid the protection of co-distributed species (Branton and Richardson, 2011; Breckheimer et al., 2014).
Globally, carnivores are facing large reductions in distribution range due to continuous anthropogenic land use change and urbanization (Kerr and Currie, 1995; Laliberte and Ripple, 2004). However, information about carnivore distribution in Peru is scarce and based mainly on new records or inventories in specific regions (Cossios et al., 2007; Cossios et al., 2012; Garcia-Olaechea et al., 2013; Hurtado and Pacheco, 2015). Some probable reasons for this scarcity of knowledge may be explained by carnivores' elusive behavior, the cost of methods such as genetic sampling to confirm presence of a species from scat or hair, and the logistics of covering large study areas (Long et al., 2008). The Order Carnivora is represented in Peru by 34 species (Pacheco et al., 2009), 21 listed in the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES, 2015) and five of them internationally threatened with extinction (IUCN, 2012).
The purpose of this research was to update and analyze the distributions and range maps of carnivore species, focusing on the 21 species that are considered at most risk from illegal trade (CITES species), which also include species in national threatened categories, with the exception of Otaria flavescens. Our specific objectives were: (a) to generate species range maps based on confirmed records, (b) to describe their distribution in Peruvian ecoregions, (c) to describe changes in species richness of these carnivores through time, and (d) to identify geographic areas and species in need of further research.
MATERIALS AND METHODS
We examined 21 species of Peruvian carnivores included in CITES (Table 1) and reviewed the available literature from 1903 to 2014. We also compiled carnivore localities from 13 museum databases: American Museum of Natural History, New York, USA (AMNH); Field Museum of Natural History, Chicago, USA (FMNH); Museo de Historia Natural, Lima, Peru (MUSM); Louisiana Museum of Natural History, Baton Rouge, USA (LSUMZ); Museum of Comparative Zoology, Harvard, USA (MCZ); Museum of Natural History at the University of Kansas, Lawrence, USA (KU); Georgian National Museum, Tbilisi, Georgia (GNM); Museum of Vertebrate Zoology, Berkeley, USA (MVZ); Royal Ontario Museum, Toronto, Canada (ROM); Texas Cooperative Wildlife Collection, College Station, USA (TCWC); Museum of Zoology, University of Michigan, Ann Arbor, USA (UMMZ); National Museum of Natural History, Smithsonian Institution, Washington D.C., USA (USNM); Yale Peabody Museum of Natural History, New Haven, USA (YPM ); and non-published records from the authors and other biologists working in Peru (C. Jimenez, C. Mercord, C. Tello, E. Salas, E. Vivar, F. Cornejo, G. Llerena, J. Barrio, J. Onofre, M. Guissa, M. Mamani, P. Bueno, P. Venegas, P. Villegas, pers. comm.). All known localities, collection dates, record type, and geographic reference were entered into an Excel spreadsheet. Coordinates were taken from published literature, requested from the authors if unpublished, or obtained from the ornithological gazetteer of Stephens and Traylor (1983). Online gazetteers such as geonames.org and fallingrain.com were also used as supplementary source for an accurate geographic estimate. Doubtful records, such as unclear coordinates or lacking evidence, were not used for analyses.
Each record was classified according to the type of evidence in: direct evidence (sightings, photographic records, DNA analysis of scats, and captures for GPS/VHF collars), indirect evidence (scats, tracks, hair, dens, vocalizations and interviews), and specimen collections (skull, skin, complete or incomplete skeletons). Furthermore, we defined contemporary records as locations obtained after 2001 based on the increase in popularity (from 27% to 51%) of modern methods to register medium to large mammals such as remote cameras, DNA analyses and GPS equipment (Long et al., 2008). Historic records were considered those made prior to 2001. Differences among type of records were assessed using a chi-square analysis in R software (R Core Team, 2014) with the package MASS.
Mapping and geographical analysis was performed using the ArcGIS 9.3 software, we integrated record occurrences within 20 km for better definition and display in the figures. A point density analysis was used to identify geographic gaps and areas with concentrated number of records that were independent of species richness. To determine species occurrence per ecoregion we used a shape file approximation of the ecoregions classification of Brack-Egg (1986) and considered known elevational ranges when coordinates placed records on the border of two ecoregions. A raster file with grid cell size of 55 x 55 km was created to generate species richness maps and allow better resolution for the geographic area studied. We followed Wilson and Reeder (2005) and Pacheco et al. (2009) for nomenclature.
We obtained 1939 records for 21 carnivore species (Table 1): 411 from museum collections, 114 from field notes, and 1414 from the literature. The family Felidae, with eight species listed in CITES, had the highest number of records (815) followed by the families: Mustelidae (519), Canidae (208), Ursidae (156), Procyonidae (148), and Otariidae (93). Leopardus colocolo was the species with the most records (245), followed by Lontra felina (172), and Puma concolor and Eira barbara (158). The species with the fewest records in Peru were Leopardus tigrinus (10), Chrysocyon brachyurus (4), and Arctocephalus philippii (2).
The ecoregions with the highest total number of records (75-104), independent of species number, were concentrated in the Amazon Lowland Rainforest around Parque Nacional Manu (11.88[grados] S, 71.41[grados] W) in Madre de Dios Department, and in the Puna ecoregion, around the Reserva Paisajistica Nor Yauyos-Cochas (12.03[grados] S, 75.86[grados] W) in Lima and Junin departments (Fig. 1). We found that large geographic areas in Loreto, Piura, Huancavelica, and Ayacucho departments lacked carnivore records (Fig. 1).
At least one species was documented in each ecoregion (Brack-Egg, 1986), and the Amazon Lowland Forest had the highest number of CITES carnivores with 12 species (Table 2). The Tropical Ocean was represented by only one species, whose taxonomic identity is still under debate and is here designated Arctocephalus cf. australis but may represent a new species (Camaratta et al., 2008) (Table 2). Leopardus jacobita, L. tigrinus, and C. brachyurus were restricted to a single region, found only in the Puna, Montane Forest, and Sabana de Palmeras, respectively (Fig. 2). Puma concolor was the only carnivore documented in all terrestrial habitats except for the Sabana de Palmeras ecoregion (Table 2).
The richness analysis, including historic and contemporary records (1903-2014), showed that northern Peru (Tumbes, Cajamarca and Loreto) and Madre de Dios Department, including its adjacent areas in the Cuzco and Ucayali departments, had the highest species richness of CITES carnivores. These areas correspond to the Pacific Tropical Rainforest, northern Montane Forest, and Amazon Lowland Rainforest (Fig. 3A), each with 9 to 11 species of carnivores.
When the same analysis was performed including only recent records (2001-2014), the highest richness was in the northern Montane Forest and Amazon Lowland Rainforest in Loreto and Ucayali departments (Fig. 3B). Furthermore, the Pacific Tropical Rainforest species richness in Tumbes was reduced by at least three species while northern Cuzco species number was reduced by one.
Historic and contemporary distribution
We found that 879 of 1939 records (45.3%) were obtained after the year 2001 (Table 1) and were characterized by greater number of direct evidence (51%) and indirect evidence (38%), while specimen collections represented only 11% of the total. Historic records showed a significantly higher number of records ([X.sup.2] = 326.7, d.f. = 2 p<0.005) derived from specimen collections (51%), whereas direct and indirect evidence constituted only 27% and 22%, respectively (Fig. 4).
Lontra felina was the only species with detailed, updated information about its distribution whereas species with few contemporary records were Leopardus tigrinus, Lycalopex griseus, Speothos venaticus, and Galictis vittata (Fig. 2). Arctocephalus philippii and C. brachyurus were represented only by four and two records, respectively. Furthermore, historic records of Tremarctos ornatus, Puma concolor, and Lycalopex culpaeus were concentrated in coastal areas (Fig. 2). For Lontra longicaudis, Potos flavus, Panthera onca, Pteronura brasiliensis, E. barbara, and Puma yagouaroundi, there is little knowledge concerning their occurrence in central Peru.
Distribution assessments are extensive for Lontra felina (Apaza and Romero, 2012), T ornatus (Garcia-Rangel, 2012), Leopardus colocolo, and Leopardus jacobita (Cossios et al., 2007). This is probably a consequence of their restricted distributions (to one or a few ecoregions) and their at-risk categorization (endangered for Lontra felina and Leopardus jacobita, vulnerable for T ornatus, and near threatened for Leopardus colocolo). However, L. colocolo still requires direct evidence that its distribution reaches to northwestern Peru and the northern limits of its distribution (Cossios et al., 2012). Cossios et al. (2007) considered L. jacobita distribution in the northern region of Ancash Department as unknown, suggesting two natural protected areas (Reserva Paisajistica Huayhuash and Parque Nacional Huascaran in the Ancash Department) as the northern distribution for this species.
Despite a considerable reduction in the A. australis population (Arias-Schreiber, 2000; Oliveira et al., 2009), there have been no recent published analyses of the distributions of viable colonies on the Peruvian coast. Furthermore, the small colony of Arctocephalus cf. australis, found on Foca Island in Piura Department (Novoa et al., 2010), more than 700 km from the nearest locality in Peru, is living in an ecotone of warm and cold oceanic currents with average ocean temperatures of about 19-23[grados]C (IMARPE, 2010); this compares with A. australis, whose distribution suggests that it prefers temperatures ranging from 13-16[grados]C (Brack-Egg, 1986). Camaratta et al. (2008) reported preliminary genetic analysis that suggests that Arctocephalus cf. australis could be a hybrid population of A. galapagoensis and A. australis; in any case, its taxonomic status needs to be resolved.
The lack of records for A. philippii and C. brachyurus could be due to their restricted distribution in Peru or constituting occasional vagrants. Chrysocyon brachyurus in Peru is restricted to a grassland type ecosystem found in the Parque Nacional Bahuaja Sonene. According to a recent distribution update, this species was photographed again since 1996 confirming that it still remains within Peruvian boundaries (Williams et al., 2012). In the case of A. philippii, lack of records could be attributed to its accidental appearance on the Peruvian coast, as described by some authors (Jefferson et al., 2011; Cossios et al., 2012). However, Pacheco et al. (2009) and Aurioles-Gamboa (2015) considered A. philippii a resident, probably because of its ability to travel long distances. The northernmost record for this species is at Buenaventura, Colombia, 3700-4600 km from its primary range (Avila et al., 2014), suggesting a larger distribution range than previously thought. Moreover, Majluf and Reyes (1989) indicated that mixed colonies of this species and A. australis were seen for at least 12 consecutive years in the Peruvian coast (1973-1984) and highlighted the possibility of undetected individuals inhabiting southern areas. If mixed colonies existed in the past, we suggest that trained biologists able to detect the differences between this two similar species in the field should assess southern localities and update the knowledge of this species for Peru.
Even though Nasua narica is listed for Peru (Pacheco et al., 2009) and is listed on Appendix III of CITES, we did not include this species in the analyses because of the ambiguous evidence for its occurrence in Peru. Records of this species were based on observations made on specimens from Tumbes (Pacheco et al., 2009) that have a snout coloration lighter than the Amazonian coati Nasua nasua; however, this pattern is not similar to the white coloration of the N. narica from Central America (Gompper, 1995). Furthermore, the closest collected specimen and confirmed sightings are from northeastern Colombia on the Gulf of Uraba (Gonzales-Maya et al., 2011), approximately 1378 km north of Tumbes. After reviewing the five specimens from Tumbes, this population differs from N. narica not only in external morphology but dental characteristics as well (CMH unpublished data).
Tropical rainforests are considered among the most diverse ecosystems for mammals (Ceballos and Ehrlich, 2006; Kier et al., 2009), and in Peru the Lowland Rainforest, Montane Forest, and Pacific Tropical Rainforest contain between 9 and 11 species of CITES carnivores. Contemporary records showed a decrease in record localities, especially for central Peru; however, the number of species was maintained in certain localities of Loreto, Madre de Dios and Cajamarca. Furthermore, the reduction in the Pacific Tropical Rainforest species richness in Tumbes has being described as potential local extinction of T ornatus, Panthera onca and the lack of confirmed records of Leopardus colocolo (Hurtado and Pacheco, 2015). Similar situations in other Peruvian areas may be going through the same local process and the need of exhaustive distribution assessments becomes necessary to develop conservation measures.
Historic and contemporary distribution
According to Dirzo et al. (2014) who followed IUCN bird and mammal species categorized as declining, South America is the largest geographic area experiencing this decline in population. Usually, the reduction in species ranges is attributed to areas of high urban development (Kerr, 1995; Channell and Lomolino, 2000; Ogutu et al., 2014; Li et al., 2015). Our maps show that T. ornatus, Lycalopex culpaeus, and Puma concolor lack confirmed contemporary records in coastal areas where the biggest Peruvian cities are found, a pattern that may suggest range contractions. A distributional assessment of Puma concolor in Latin America found that 40% of its range is lost or threatened, including populations in coastal and central regions of Peru (Laundre and Hernandez, 2010). Furthermore, the most important factor in record reduction appears to have been concentrated urban development, which pushes species to less urbanized areas that were not formerly occupied (Laundre and Hernandez, 2010).
Previous distribution maps of Lycalopex culpaeus did not include the Peruvian desert ecoregion as part of its distribution range (Novaro, 1997). However, updated assessments consider the southern desert as a current habitat for this fox (IUCN, 2008a; Wilson et al., 2009). In this research, we found that historic records in the desert were primarily from Lomas type ecosystem (Velarde Falconi, 1983; Falero and Sanchez, 1986, Zeballos et al., 2000), which are episodic phytogeographic units within the desert characterized by seasonal development of plant communities under winter fog influences (Sotomayor Melo and Jimenez Milon, 2008). Therefore, the Peruvian desert ecoregion should be assessed to determine if L. culpaeus distribution is limited only to Lomas and to identify its distribution limits.
Furthermore, in Tumbes, both Panthera onca and T. ornatus have suffered local extinction due to population isolation (Garcia-Rangel et al., 2012; Hurtado and Pacheco, 2015). Therefore, special attention to urban development and anthropogenic activities such as agriculture, farming, mining, hunting, logging and roads need to be taken into consideration because habitat fragmentation is inversely correlated with species richness and loss of connectivity within populations (Crooks et al., 2011).
Other anthropogenic activities such as the construction of the Interoceanic highway PeruBrazil, mining, and oil and gas extraction might generate general and localized impacts (Finer et al., 2008). Therefore, large-scale distributional assessments of poorly known species and analyses of changes in distributional patterns of wide spread species at a regional scale should be explored and used as indicators of risk to prevent biodiversity loss. Also, previous and rapid inventories mainly using transect census and interviews may have failed to detect rare species and therefore underestimated total carnivore richness. New reliable methods such as camera traps would improve understanding of carnivore's distribution.
Research gaps and conservation priorities
Further research is needed in unexplored areas. Huancavelica Department and its surroundings, Ucayali Department, and the central region of Loreto are three main areas that lack carnivore records or are poorly documented, likely due to conflict and lack of access. In Huancavelica, constant social conflicts caused by drug trafficking, present since the 1980's, have made this area inaccessible and dangerous for research (Pacheco et al. 2007). For Ucayali and Loreto, the high cost and complicated logistics to access these remote areas limits research. Quintana et al. (2009) indicated that unexplored areas in Ucayali could hold higher diversity than hitherto reported, and indicated several threats to wildlife such as logging, highway construction, and lax control in natural protected areas, among others. These are difficult areas to explore, but future efforts should be made for research and to assess potential threats for carnivores and other species.
Even though a major effort to monitor terrestrial species is being made by the Tropical Ecology Assessment and Monitoring (TEAM) network in Central and South eastern Peru (Yanachaga and Cocha Cashu National Parks), central Peru still requires updated carnivore distribution assessments. Other natural protected areas such as Cordillera Azul and Rio Abiseo National Parks should be considered priorities to confirm presence and maintain connectivity between northern and southern populations. Special emphasis should be given to G. vittata, Lontra longicaudis, Potos flavus, Panthera onca, Pteronura brasiliensis, E. barbara, and Puma yagouaroundi to update their distribution in central Peru and assess the connectivity of their southern and northern populations.
For species priorities, Leopardus tigrinus, which has only a single published contemporary record (Amanzo et al., 2003), is the species that most urgently needs a distributional update; of the ten records found, four were from museum specimens and six from literature review, all within the Yungas region (Fig. 2). In Ecuador, this species inhabits coastal dry forests, lowland rainforests, and Yungas from 0 to 3000 m (Tirira, 2007), but its distribution and several records still need confirmation (Tirira, 2011). In Colombia, this species is considered rare but is widely distributed across montane forests (Payan and Gonzalez-Maya, 2011), whereas in Brazil it is found in the Atlantic rainforest (Bianchi et al., 2011). This distribution patterns across several habitats reinforces the need for an exhaustive distribution assessment of this species.
Lycalopex griseus population's trend is considered stable (IUCN, 2008b); however, the IUCN does not consider Peru as part of this species distribution range. According to Peruvian legislation, L. griseus is considered Data Deficient which is also reflected in the number of records obtained in this study, 17 total records including a single contemporary record. Based on morphological evidence, Vivar and Pacheco (2014) provided support for the presence of this species in southern Peru and suggested that Peruvian populations may represent a new subspecies, based on discontinuous distribution and the Atacama Desert as a potential geographic barrier. On the other hand, Iriarte and Jaksic (2012) acknowledged a continuous distribution of L. griseus from Peru to Argentina and described it as occurring in different extreme habitats from the Atacama Desert to cold forests in Tierra del Fuego. Further studies are needed to elucidate these contrasting distributional patterns and to determine habitat requirements for L. griseus in Peru.
Similarly, Speothos venaticus, which also has few contemporary records, should also be prioritized for a distribution and conservation assessment. This species is considered rare and extremely elusive which may represent a challenge for its study (Michalski and Peres, 2005; DeMatteo and Loiselle, 2008, DeMatteo et al., 2014). Speothos venaticus was categorized as Near Threatened by the IUCN, and although not much is known about it in Peru, it was not given a Data Deficient category. Several areas within its distributional range were, until recently, considered distributional gaps especially for Brazil (Guimaraes et al., 2015; da Rocha et al., 2015). Similarly, northern Peru in Amazonas, where we have only historic records, is still a gap in knowledge even though this area was considered suitable for S. venaticus by DeMatteo and Loiselle (2008). We encourage an updated evaluation in this region using non-invasive techniques such as camera trapping and genetic identification of scats using trained dogs for collection; the latter technique was proven to be successful for rare species studies (DeMatteo et al., 2014).
Other techniques such as the use of VHF and GPS collars and specimen collections are important to the understanding of the ecology, morphology and function of these carnivores in their ecosystems (Long et al., 2008). Museum specimens and the importance of museum collections are well recognized (Suarez and Tsutsui, 2004; Gippoliti et al., 2014 ); however, our analysis showed contrasting patterns of carnivore records in which specimens collections were the best source of tangible information only for historic records. Whereas technology has improved providing other direct evidence such as photographs and direct sightings which form the base of most contemporary records, there is also the rejection of collecting charismatic species, such as carnivores (De Vivo, 2007). It is certain that carnivore collections must be well justified; nonetheless, opportunistic salvage operations involving hunted animals or their skeletal remains by field biologists provide an invaluable way to enrich museum collections and all the science they support, without the need to kill a single specimen. Moreover, contemporary data such as photographs involve difficulties in verifying the information they contain. This problem can be reduced by implementing a digital museum database, where low-density or rare species photographs can be found in one place and are available for other researchers.
In conclusion, different methods can provide information about distribution and habitat use of carnivores. This information is crucial for species conservation (Rondinini et al., 2011), especially under changing land-use, which is a global trend (Di Minin et al., 2016). We hope that this regional perspective of carnivore distribution assessment and recommendations will help conservation biologists and managers redirect efforts and funds to select areas for more research including possible biological corridors (Sepulveda et al., 1997), as well as develop accurate monitoring plans and other tools to conserve carnivores.
We would like to thank the Peruvian Ministry of Environment for funding this project, Melisa del Alcazar for her assistance in the data collection, Jose Serrano-Villavicencio, Lily McFeeters, and Alvaro Garcia-Olaechea for their comments, Anjali Kumar, Bruce Patterson, Diego Lizcano and the reviewers for their edits and comments improving this manuscript. We are also grateful to C. Jimenez, C. Mercord, C. Tello, E. Salas, E. Vivar, F. Cornejo, G. Llerena, J. Barrio, J. Onofre, M. Guissa, M. Mamani, P. Bueno, P. Venegas and P. Villegas who provided information for this manuscript.
ABBITT RJ and JM SCOTT. 2001. Examining differences between recovered and declining endangered species. Conservation Biology 15:1274-1284. doi: 10.1111/j.1523-1739.2001.00430.x.
AMANZO J, R ACOSTA, C AGUILAR, K ECKHARD, B SEVERO and T PEQUENO. 2003. Evaluacion biologica rapida del Santuario Nacional TabaconasNambelle y zonas aledanas, WWF, INRENA. Peru.
APAZA M and L ROMERO. 2012. Distribucion y Observaciones sobre la poblacion de la nutria marina Lontra felina (Molina 1782) en el Peru. Revista Peruana de Biologia 19:285-298. doi: 10.15381/rpb.v19i3.1064.
ARIAS-SCHREIBER M. 2000. Distribucion, tamano y estructura de las poblaciones de lobos marinos Arctocephalus australis y Otaria byronia en el litoral Peruano durante 1999. Informe Anual 1999. Informe Interno del Instituto del Mar del Peru
AURIOLES-GAMBOA D. 2015. Arctocephalus philippii. The IUCN Red List of Threatened Species 2015: e.T2059A61953525. doi: 10.2305/IUCN.UK.2015-2. RLTS.T2059A61953525.en. Downloaded on 20 September 2015.
AVILA IC, JJ ALAVA and CA GALVIS RIZO. 2014. On the presence of a vagrant Juan Fernandez fur seal (Arctocephalus philippii) in the Pacific coast of Colombia: A new extralimital record. Mastozoologia Neotropical 21:109-114.
BIANCHI RDC, AF ROSA, A GATTI and S L MENDES. 2011. Diet of margay, Leopardus wiedii, and jaguarundi, Puma yagouaroundi (Carnivora: Felidae), in Atlantic Rainforest, Brazil. Zoologia 28:127-132. doi: 10.1590/ S1984-46702011000100018.
BRACK-EGG A. 1986. Las ecorregiones del Peru. Boletin de Lima 44:57-70.
BRANTON M and JS RICHARDSON. 2011. Assessing the value of the umbrella-species concept for conservation planning with meta-analysis. Conservation Biology 25:9-20. doi: 10.1111/j.1523-1739.2010.01606.x.
BRECKHEIMER I, NM HADDAD, WF MORRIS, AM TRAINOR, RT JOBE, BR HUDGENS et al. 2014. Defining and evaluating the umbrella species concept for conserving and restoring landscape connectivity. Conservation Biology 28:1584-1593. doi: 10.1111/cobi.12362.
CAMARATTA D, D GARCIA, L DE OLIVEIRA, S CARDENAS, J MARQUEZ and S BONATTO. 2008. Status taxonomico dos lobos-marinhos de Isla Foca (Peru): Arctocephalus australis, A. galapagoensis (Carnivora: Otariidae) ou hibridos? IX Salao de Iniciado Cientiica Pontificia Universidade Catolica do Rio Grande do Sul.
CARDILLO M, GM MACE, KE JONES, J BI EL BY, OR BININDA-EMONDS, W SECHREST and A PURVIS. 2005. Multiple causes of high extinction risk in large mammal species. Science 309:1239-1241. doi: 10.1126/science.1116030.
CEBALLOS G and PR EHRLICH. 2006. Global mammal distributions, biodiversity hotspots, and conservation. Proceedings of the National Academy of Sciences 103:19374-19379. doi: 10.1073/pnas.0609334103.
CHANNELL R and MV LOMOLINO. 2000. Dynamic biogeography and conservation of endangered species. Nature 403:84-86. doi:10.1038/47487.
COSSIOS ED, A MADRID, J CONDORI and U FAJARDO. 2007. Update on the distribution of the Andean cat Oreailurus Jacobita and the pampas cat Lynchailurus Colocolo in Peru. Endangered Species Research (3):313-20. doi:10.3354/esr00059.: 285-98.
COSSIOS D, P ALCAZAR, U FAJARDO, K CHAVEZ, J ALFARO-SHIGUE, J VALQUI, FG MONTERO, et al. 2012. El Orden Carnivora (Mammalia) en el Peru: estado del conocimiento y prioridades de investigacion para su conservacion. Revista Peruana de Biologia 19:17-26. doi:10.15381/rpb.v19i1.783.
CROOKS KR. 2002. Relative sensitivities of mammalian carnivores to habitat fragmentation. Conservation Biology 16:488-502. doi: 10.1046/j. 15231739.2002.00386.x
CROOKS KR, CL BURDETT, DM THEOBALD, C RONDININI and L BOITANI. 2011. Global patterns of fragmentation and connectivity of mammalian carnivore habitat. Philosophical Transactions of the Royal Society of Biological Sciences 366:2642-2651. doi: 10.1098/rstb.2011.0120.
DA ROCHA DG, EE RAMALHO, GC ALVARENGA, DM GRABIN and WE MAGNUSSON. 2015. Records of the bush dog (Speothos venaticus) in Central Amazonia, Brazil. Journal of Mammalogy 96:1361-1364.
DEMATTEO KE and BA LOISELLE. 2008. New data on the status and distribution of the bush dog (Speothos venaticus): Evaluating its quality of protection and directing research efforts. Biological Conservation 141:2494-2505.
DEMATTEO KE, MA RINAS, CF ARGUELLES, JP ZURANO, N SELLESKI, MS BITETTI and LS EGGERT. 2014. Noninvasive techniques provide novel insights for the elusive bush dog (Speothos venaticus). Wildlife Society Bulletin 38:862-873.
DE VIVO M. 2007. Problemas da mastozoologia brasileira. Boletim da Sociedade Brasileira de Mastozoologia 48:1-4.
DI MININ E, R SLOTOW, LT HUNTER, FM POUZOLS, T TOIVONEN, PH VERBURG, N LEADERWILLIAMS, L PETRACCA and A MOILANEN. 2016. Global priorities for national carnivore conservation under land use change. Scientific Reports 6:1-9.
DIRZO R, HS YOUNG, M GALETTI, G CEBALLOS, NJ ISAAC and B COLLEN. 2014. Defaunation in the Anthropocene. Science 345:401-406. doi: 10.1126/ science.1251817.
FALERO M and E SANCHEZ. 1986. Comportamiento alimentario del zorro andino (Dusicyon culpaeus) en la Reserva Nacional de Lachay. X Congreso Latinoamericano de Zoologia. Vina del Mar Chile.
FINER M, CN JENKINS, SL PIMM, B KEANE and C ROSS. 2008. Oil and gas projects in the western Amazon: Threats to wilderness, biodiversity, and indigenous peoples. PLoS ONE 3:2932. doi:10.1371/ journal.pone.0002932.
GARCIA-OLAECHEA A, C CHAVEZ-VILLAVICENCIO and J NO VO A COVA. 2013. Leopardus pajeros (Desmarest, 1816) (Carnivora: Felidae) in Northern Peru: First record for the Department of Piura, at the Mangroves San Pedro de Vice, and geographic extension. Check List 9:1596-99.
GARCIA-RANGEL S. 2012. Andean bear Tremarctos ornatus Natural history and conservation. Mammal Review 42:85-119. doi:10.1111/j.1365-2907.2011.00207.x.
GIPPOLITI S, G AMORI, R CASTIGLIA, P COLANGELO and E CAPANNA. 2014. The relevance of Italian museum collections for research and conservation: The case of mammals. Rendiconti Lincei 25(3):351-357.
GITTLEMAN JL and PH HARVEY. 1982. Carnivore home range size, metabolic needs and ecology. Behavioural Ecology and Sociobiology 10:57-63. doi: 10.1007/ BF00296396.
GOMPPER ME. 1995. Nasua narica. Mammalian Species 487:1-10.
GONZALEZ-MAYA JF, A RODRIGUEZ-BOLANOS, D PINTO and A JIMENEZ-ORTEGA. 2011. Recent confirmed records and distribution of the white-nosed coati Nasua narica in Colombia. Small Carnivore Conservation 45:26-30.
GUIMARAES VY, LCC CESCA, DF TROMBIN and L PINDER. 2015. New records of Speothos venaticus Lund, 1842 (Carnivora: Canidae) in the state of Para, Brazil. Brazilian Journal of Biology 75: 176-178. http:// dx.doi.org/10.1590/1519-6984.02514BM
HURTADO CM and V PACHECO. 2015. Nuevos registros de mamiferos en el Parque Nacional Cerros de Amotape, noroeste de Peru. Revista Peruana de Biologia 22:077-086. doi: 10.15381/rpb.v22i1.11124.
IMARPE. 2010. (on line) Temperatura superficial del mar. http://www.imarpe.gob.pe/paita/tsm/tsm.htm. Access el 10/18/2015.
IRIARTE A and F JAKSIC. 2012. Los carnivoros de Chile. Ediciones Flora y Fauna Chile y CASEB, PU Catolica de Chile. 260pp.
IUCN. 2008a. Pseudalopex culpaeus. The IUCN Red List of Threatened Species. Version 2015-4
IUCN. 2008b. Pseudalopex griseus. The IUCN Red List of Threatened Species. Version 2015-4
IUCN. 2012. (on line). IUCN Red list of threatened species. Version 2012 <www.iucnredlist.org>. Access 27/11/2014.
JEFFERSON TA, MA WEBBER and RL PITMAN. 2011. Marine mammals of the world: A comprehensive guide to their identification. Academic Press. London.
KERR JT and DJ CURRIE. 1995. Effects of human activity on global extinction risk. Conservation Biology 9:1528-1538. doi: 10.1046/j.1523-1739.1995.09061528.x.
KIER G, H KREFT, TM LEE, W JETZ, PL IBISCH, et al. 2009. A global assessment of endemism and species richness across island and mainland regions. Proceedings of the National Academy of Sciences 106:9322-9327. doi: 10.1073/pnas.0810306106.
LALIBERTE AS and WJ RIPPLE. 2004. Range contractions of North American carnivores and ungulates. BioScience 54:123-138. doi:10.1641/00063568(2004)0 54[0123:RCONAC]2.0.CO
LAUNDRE J and L HERNANDEZ. 2010. What we know about pumas in Latin America. In: Cougar: ecology and conservation (M Hornocker and N Sharon, eds.). The University of Chicago Press, London.
LI X, G JIANG, H TIAN, L XU, C YAN, Z WANG, et al. 2015. Human impact and climate cooling caused range contraction of large mammals in China over the past two millennia. Ecography 38:74-82. doi: 10.1111/ecog.00795.
LONG R, P MACKAY, W ZIELINSKI and JR JUSTINA. 2008. Noninvasive survey methods for carnivores. Island Press. Washington DC.
MAJLUF P and JC REYES. 1989. The marine mammals of Peru: A review. Pp. 344-363, in: The Peruvian upwelling ecosystem: dynamics and interactions (D Pauly, P Muck, J Mendo and I Tsukayama, eds.). ICLARM Conference Proceedings 18.
MCCAIN CM and SRB KING. 2014. Body size and activity times mediate mammalian responses to climate change. Global Change Biology 20:1760-9. doi: 10.1111/gcb.12499.
MICHALSKI F and CA PERES. 2005. Anthropogenic determinants of primate and carnivore local extinctions in a fragmented forest landscape of southern Amazonia. Biological Conservation 124:383-396.
MORRISON JC, W SECHREST, E DINERSTEIN, DS WILCOVE and JF LAMOREUX. 2007. Persistence of large mammal faunas as indicators of global human impacts. Journal of Mammalogy 88:1363-1380.
NOSS RF, HB QUIGLEY, MG HORNOCKER, T MERRILL and PC PAQUET. 1996. Conservation biology and carnivore conservation in the Rocky Mountains. Conservation Biology 10:949-963.
NOVARO AJ. 1997. Pseudalopex culpaeus. Mammalian species 558:1-8.
NOVOA J, Y HOOKER and A GARCIA. 2010. Isla Foca, Guia de Fauna Silvestre. Primera Edicion. Naturaleza y Cultura Internacional--CONCYTEC. Piura-Peru. 112 pp.
OGUTU JO, HP PIEPHO, MY SAID and SC KIFUGO. 2014. Herbivore dynamics and range contraction in Kajiado County Kenya: Climate and land use changes, population pressures, governance, policy and humanwildlife conflicts. Open Ecology Journal 7:9-31. doi: 10.2174/1874213001407010009.
OLIVEIRA LR, D MEYER, JI HOFFMAN, P MAJLUF and JS MORGANTE. 2009. Evidence of a genetic bottleneck in an El Nino affected population of South American fur seals, Arctocephalus australis. Journal of the Marine Biological Association of the United Kingdom 89:1717-1725. doi: 10.1017/ S0025315409000162.
ORDENANA MA, KR CROOKS, EE BOYDSTON, RN FISHER, LM LYREN, S SIUDYLA and DH VAN VUREN. 2010. Effects of urbanization on carnivore species distribution and richness. Journal of Mammalogy 91:1322-1331. doi: 10.1644/09-MAMM-A-312.1.
PACHECO V, R CADENILLAS, E SALAS, C TELLO and H ZEBALLOS. 2009. Diversidad y endemismo de los mamiferos del Peru. Revista Peruana de Biologia 16:005-032.
PACHECO V, E SALAS, L CAIRAMPOMA, M NOBLECILLA, H QUINTANA, F ORTIZ, P PALERMO and R LEDESMA. 2007. Contribucion al conocimiento de la diversidad y conservacion de los mamiferos en la cuenca del rio Apurimac, Peru. Revista Peruana de Biologia 14:169-180.
PARLATO EH, DP ARMSTRONG and JG INNES. 2015. Traits influencing range contraction in New Zealand's endemic forest birds. Oecologia 1-10. doi:10.1007/ s00442-015-3330-6.
PAYAN E and JF GONZALEZ-MAYA. 2011. Distribucion geografica de la oncilla (Leopardus tigrinus) en Colombia e implicaciones para su conservacion. Revista Latinoamericana de Conservacion 2:51-59.
QUINTANA H, V PACHECO, and E SALAS. 2009. Diversidad y conservacion de los mamiferos de Ucayali, Peru. Ecologia Aplicada 8:91-103.
R CORE TEAM. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.Rproject.org/.
RIPPLE WJ, AJ WIRSING, CC WILMERS and M LETNIC. 2013. Widespread mesopredator effects after wolf extirpation. Biological Conservation 160:70-79. doi:10.1016/j.biocon.2012.12.033
RIPPLE WJ, JA ESTES, RL BESCHTA, CC WILMERS, EG RITCHIE, M HEBBLEWHITE, et al. 2014. Status and ecological effects of the world's largest carnivores. Science 343: 1241484. Doi: 10.1126/science.1241484
ROCHLIN I, DV NINIVAGGI, ML HUTCHINSON and A FARAJOLLAHI. 2013. Climate change and range expansion of the Asian tiger mosquito (Aedes albopictus) in Northeastern USA: Implications for public health practitioners. PLoS ONE 8(4):60874. doi:10.1371/journal.pone.0060874.
RONDININI C, M DI MARCO, F CHIOZZA, G SANTULLI, D BAISERO, P VISCONTI, et al. 2011. Global habitat suitability models of terrestrial mammals. Philosophical Transactions of the Royal Society of London B: Biological Sciences 366:2633-2641.
SENYATSO KJ, NJ COLLAR and PM DOLMAN. 2012. Assessing range-wide conservation status change in an unmonitored widespread African bird species. Diversity and Distributions 19:106-119. doi: 10.1111/j.1472-4642.2012.00909.x
SOTOMAYOR MELO DA and JIMENEZ MILON P. 2008. Condiciones meteorologicas y dinamica vegetal del ecosistema costero Lomas de Atiquipa (Caraveli--Arequipa) en el sur del Peru. Ecologia Aplicada 7:1-8.
STEPHENS L and MA TRAYLOR JR. 1983. Ornithological gazetteer of Peru. Museum of Comparative Zoology. Harvard University. Cambridge.
SUAREZ AV and ND TSUTSUI. 2004. The value of museum collections for research and society. BioScience 54: 66-74.
SEPULVEDA C, A MOREIRA and P VILLARROEL. 1997. Conservacion biologica fuera de las areas silvestres protegidas. Ambiente y Desarrollo 13:48-58.
TERBORGH J. 1988. The big things that run the world--a sequel to E. O. Wilson. Conservation Biology 2:402-403.
TIRIRA D. 2007. Mamiferos del Ecuador. Guia de Campo. Publicacion Especial 6. Ediciones Murcielago Blanco. Quito.
TIRIRA DG. 2011. Libro rojo de los mamiferos del Ecuador. 2a Edicion. Fundacion Mamiferos y Conservacion. Pontificia Universidad catolica del Ecuador y Ministerio del Ambiente de Ecuador. Quito.
UCARLI Y. 2011. Usability of large carnivore as a keystone species in Eastern Black Sea Region, Turkey. African Journal of Biotechnology 10:2032-2036.
VELARDE FALCONI D. 1983. Evaluacion de la fauna de vertebrados de las Lomas de Iguanil. Zonas Aridas 3:101-110.
VIVAR E and V PACHECO. 2014. Estado del zorro gris Lycalopex griseus (Gray, 1837) (Mammalia: Canidae) en el Peru. Revista Peruana de Biologia 21:071-078.
VOIGT W, J PERNER, A DAVIS, T EGGERS, J SCHUMACHER, R BAHRMANN, et al. 2003. Trophic levels are differentially sensitive to climate. Ecology 84:2444-2453. Doi: 10.1890/02-0266
WILLIAMS RS, E TORRES, J MAGAN, A CRUZ and R LEITE PITMAN. 2012. Continued presence of the maned wolf in Peru. Available at: http://www.canids. org/canidsnews/15/Maned_wolf_in_Peru.pdf.
WILSON EO. 2000. On the future of conservation biology. Conservation Biology 14:1-3.
WILSON DE and DM REEDER. 2005. Mammal species of the world: A taxonomic and geographic reference. The Johns Hopkins University Press, Baltimore.
WILSON DE, RA MITTERMEIER, P CAVALLINI and T LLOBET. 2009. Handbook of the mammals of the world. Barcelona: Lynx editions. 727 pp.
WOODROFFE R and JR GINSBERG. 1998. Edge effects and the extinction of populations inside protected areas. Science 280:2126-2128. doi:10.1126/science.280.5372.2126.
ZEBALLOS H, L VILLEGAS, R GUTIERREZ, K CABALLERO and P JIMENEZ. 2000. Vetebrados de las Lomas de Atiquipa y Mejia, Sur del Peru. Revista de Ecologia Latino-Americana 7: 11-18.
Cindy M. Hurtado (1,3,4), Victor Pacheco (2, 3), Ursula Fajardo (3), and Angie Uturunco (3)
(1) Towson University, 8000 York Rd., Towson, MD, 21252, USA [Correspondence: Cindy Hurtado <firstname.lastname@example.org>]
(2) Instituto de Ciencias Biologicas "Antonio Raimondi", Facultad de Ciencias Biologicas, Universidad Nacional Mayor de San Marcos, Lima, Peru
(3) Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Av. Arenales 1256, Lima 14, Peru
(4) Centro de Investigacion Biodiversidad Sostenible (BioS), Francisco de Zela 1556, Lima 14, Peru
Recibido 29 diciembre 2015. Aceptado 14 junio 2016. Editor asociado: T Lacher
Leyenda: Fig. 1: Total number of carnivores records, indicating intensity of existing surveys. Red areas show more carnivore records whereas greener areas, less. 1: Tumbes, 2: Piura, 3: Lambayeque, 4: Cajamarca, 5: Amazonas, 6: Loreto, 7: La Libertad, 8: San Martin, 9: Ancash, 10: Huanuco, 11: Lima, 12: Pasco, 13: Junin, 14: Ucayali, 15: Ica, 16: Huancavelica, 17: Ayacucho, 18: Apurimac, 19: Cuzco, 20: Madre de Dios, 21: Arequipa, 22: Puno, 23: Moquegua, 24: Tacna.
Leyenda: Fig. 2: Distribution maps of 21 carnivore species. Circles represent contemporary records (from 2001-2014) and triangles represent historic records (before 2001).
Leyenda: Fig. 4. Type of evidence for historic records (white bars) and contemporary records (grey bars). Direct evidence: sightings, photographic records, DNA scat analysis, and captures. Indirect evidence: scats, tracks, footprints, vocalizations, dens and interviews. Specimen collection: skins, skulls, skeletons from museums and private collections.
Table 1 Species list of CITES-listed carnivores and the number of total and contemporary records per species. The conservation status of each species as designated by the International Union for Conservation of Nature (IUCN) (2012) is included, with their population trend and the Peruvian Government D.S. 004-2014 category. NT: near threatened, EN: endangered, VU: vulnerable, DD: data deficient; De: decreasing, In: increasing, Un: Unknown, St: stable; TR: Total records, CR: Contemporary records (2001-2014). Species Common CITES Names FELIDAE Leopardus colocolo (Molina, 1782) Pampas cat II Puma concolor (Linnaeus, 1771) Cougar, Puma II Leopardus pardalis (Linnaeus, 1758) Ocelot I Panthera onca (Linnaeus, 1758) Jaguar I Puma yagouaroundi (E. Geoffroy Jaguarundi II Saint-Hilaire, 1803) Leopardus wiedii (Schinz, 1821) Margay I Leopardus jacobita (Cornalia, 1865) Andean Cat I Leopardus tigrinus (Schreber, 1775) Oncilla I MUSTELIDAE Lontra felina (Molina, 1782) Marine otter I Eira barbara (Linnaeus, 1758) Tayra III Lontra longicaudis (Olfers, 1818) Neotropical I otter Pteronura brasiliensis (Gmelin, 1788) Giant otter I Galictis vittata (Schreber, 1776) Greater grison III CANIDAE Lycalopex culpaeus (Molina, 1782) Andean fox II Speothos venaticus (Lund, 1842) Bush dog I Lycalopex griseus (Gray 1837) South American II grey fox Chrysocyon brachyurus (Illiger, 1815) Maned wolf II URSIDAE Tremarctos ornatus (F. G. Cuvier, Andean bear I 1825) PROCYONIDAE Potos flavus (Schreber, 1774) Kinkajou III OTARIDAE Arctocephalus australis (Zimmermann, South American II 1783) fur seal Arctocephalus philippii (Peters, 1866) Juan Fernandez II fur seal IUCN Species 2012 Population trend FELIDAE Leopardus colocolo (Molina, 1782) NT De Puma concolor (Linnaeus, 1771) De Leopardus pardalis (Linnaeus, 1758) De Panthera onca (Linnaeus, 1758) NT De Puma yagouaroundi (E. Geoffroy Saint-Hilaire, 1803) Leopardus wiedii (Schinz, 1821) NT De Leopardus jacobita (Cornalia, 1865) EN De Leopardus tigrinus (Schreber, 1775) VU De MUSTELIDAE Lontra felina (Molina, 1782) EN De Eira barbara (Linnaeus, 1758) De Lontra longicaudis (Olfers, 1818) NT De Pteronura brasiliensis (Gmelin, 1788) EN De Galictis vittata (Schreber, 1776) St CANIDAE Lycalopex culpaeus (Molina, 1782) St Speothos venaticus (Lund, 1842) NT De Lycalopex griseus (Gray 1837) St Chrysocyon brachyurus (Illiger, 1815) NT Un URSIDAE Tremarctos ornatus (F. G. Cuvier, VU De 1825) PROCYONIDAE Potos flavus (Schreber, 1774) De OTARIDAE Arctocephalus australis (Zimmermann, In 1783) Arctocephalus philippii (Peters, 1866) In DS. Species TR CR 004-2014 FELIDAE 815 424 Leopardus colocolo (Molina, 1782) DD 245 198 Puma concolor (Linnaeus, 1771) NT 158 74 Leopardus pardalis (Linnaeus, 1758) 143 41 Panthera onca (Linnaeus, 1758) NT 114 48 Puma yagouaroundi (E. Geoffroy 65 15 Saint-Hilaire, 1803) Leopardus wiedii (Schinz, 1821) DD 47 15 Leopardus jacobita (Cornalia, 1865) EN 33 30 Leopardus tigrinus (Schreber, 1775) DD 10 3 MUSTELIDAE 519 244 Lontra felina (Molina, 1782) EN 172 149 Eira barbara (Linnaeus, 1758) 158 39 Lontra longicaudis (Olfers, 1818) 90 31 Pteronura brasiliensis (Gmelin, 1788) EN 64 18 Galictis vittata (Schreber, 1776) 35 7 CANIDAE 208 72 Lycalopex culpaeus (Molina, 1782) 150 60 Speothos venaticus (Lund, 1842) 37 10 Lycalopex griseus (Gray 1837) DD 17 1 Chrysocyon brachyurus (Illiger, 1815) 4 1 URSIDAE 156 88 Tremarctos ornatus (F. G. Cuvier, VU 156 88 1825) PROCYONIDAE 148 40 Potos flavus (Schreber, 1774) 148 40 OTARIDAE 93 4 Arctocephalus australis (Zimmermann, EN 91 4 1783) Arctocephalus philippii (Peters, 1866) 2 0 Table 2 Percentage of CITES-listed carnivore records from Peru per ecoregion (sensu Brack-Egg, 1986) and total number of records per ecoregion. TO: Tropical Ocean, PCO-D: Peruvian Current Ocean and Desert, De: Desert, EDF: Equatorial Dry Forest, PTR: Pacific Tropical Rainforest, SE: Serrania Esteparia, Pu: Puna, Pa: Paramo, MF: Montane Forest, LR: Amazon Lowland Rainforest, SP: Sabana de Palmeras Species TO PCO-D De EDF PTR SE Leopardus colocolo 4 1 1 4 Leopardus jacobita Leopardus pardalis 3 8 Leopardus tigrinus Leopardus wiedii 11 Puma concolor 2 6 3 6 Puma yagouaroundi 2 2 Panthera onca 4 Chrysocyon brachyurus Lycalopex culpaeus 9 17 Lycalopex griseus 76 24 Speothos venaticus Tremarctos ornatus 5 1 4 Arctocephalus australis 1 99 Arctocephalus philippii 100 Lontra felina 99 1 Lontra longicaudis 1 9 Pteronura brasiliensis Eira barbara 1 5 Galictis vittata Potos flavus 1 Total number of records 1 262 43 28 51 58 Species Pu Pa MF LR SP Leopardus colocolo 82 8 Leopardus jacobita 100 Leopardus pardalis 19 70 Leopardus tigrinus 100 Leopardus wiedii 4 79 6 Puma concolor 28 1 15 39 Puma yagouaroundi 23 73 Panthera onca 6 86 4 Chrysocyon brachyurus 100 Lycalopex culpaeus 58 16 Lycalopex griseus Speothos venaticus 3 97 Tremarctos ornatus 2 82 6 Arctocephalus australis Arctocephalus philippii Lontra felina Lontra longicaudis 19 71 Pteronura brasiliensis 98 2 Eira barbara 25 68 1 Galictis vittata 18 82 Potos flavus 22 75 2 Total number of records 361 4 361 754 16