Carnivores ( Mammalia ) from areas of Nearctic – Neotropical transition in Puebla , central Mexico : presence , distribution , and conservation

The Nearctic and Neotropical realms converge in central Mexico, where many areas have not been adequately characterized. Our objective was to revise the distribution and conservation status of carnivores in the state of Puebla, central Mexico. Between September 2008 and January 2011, we conducted interviews and fieldwork on seven previously selected areas. We complemented our data with bibliographical research. We obtained 733 records for 21 species, representing 63% of the carnivores reported for Mexico. We expanded known ranges of three species: Ocelot (Leopardus pardalis), Bobcat (Lynx rufus), and Tropical Ringtail (Bassariscus sumichastrii). Fifty percent of the carnivore species we recorded in Puebla are considered under some risk category. We found that carnivores in our study area are vulnerable to hunting pressure, humancarnivore conflicts that result in lethal control practices, and extensive habitat loss.

Ramírez-Bravo and Hernández-Santin | Carnivores in Puebla, Central Mexico the first year, interviews were not structured; that is, we informally interviewed local people with different backgrounds aiming to identify presence and absence of different species in the region.From the second year onwards, we conducted formal interviews, using a pre-made datasheet.Structured interviews focused on determining how many days people spent in the field and the rate of sighting and/or sign encountering of Jaguars, their prey, and other carnivores.Analysis and details of interviewees' profiles can be found in (Petracca et. al. 2014).To allow the correct identification of species reported by interviewees, we used visual aids (pictures) during structured and unstructured interviews.That is, we showed them pictures of different medium-sized and large mammals that could inhabit the area, except skunks.
Besides interviews, sampling was supplemented by camera-trapping, scent station placing, and opportunistic records in areas close to the interviewed communities, including areas where locals had reported sightings (e.g., Petracca et. al. 2014).We set cameratraps along roads, trails, near bodies of water, and other sites with evidence of animal presence (Ramírez-Bravo et al. 2010).We used 23 camera-traps: Wildview Xtreme 4 (Texas, USA; n=9), Cuddeback (Wisconsin, USA; n=4), and Bushnell (Kansas, USA; n=10).We used one or two camera-traps per location and moved them every month to increase the area surveyed (Ramírez-Bravo et al. 2010).We placed scent stations in six vegetation patches in the area of Tehuacan-Sierra Negra from April to May 2010 and from October to December 2010.Given the heterogeneity of the area, we used a web arrangement instead of the typical line transect used by Sargeant et al. (2003).The latter as this trap arrangement has been proved effective to determine species distribution and

Study area
Seven study sites were previously selected based on the objectives of a long-term research project known as "The Jaguar in Puebla: Presence and Human relations" (Ramírez-Bravo et al. 2010).The selection process of the study sites was based on habitat suitability maps developed for Jaguars, based on environmental and anthropogenic variables (Ramirez-Bravo et al. 2010).These maps showed areas of high habitat suitability that were inferred to pose higher probability of Jaguar occurrence.Final selection of the seven sites was based on accessibility and connection with neighboring communities and municipalities (Figure 1).Five sites were located in northern Puebla along the Sierra Norte mountain range, one in the southwestern portion of the state along Mixteca, and one in the southwestern portion of the state along Tehuacan-Sierra Negra.Sierra Norte is characterized by relatively untouched vegetation that varied with elevation, including tropical forests (TF), cloud forests (CF), oak forests (OF), and pine forests (PF).Mixteca is characterized by tropical deciduous forests (TDF) with patches of xeric scrub (XS).Tehuacán-Sierra Negra is characterized by xeric scrub intermixed with tropical deciduous forests, oak forests, cloud forests, and tall-treed tropical forests (TTF).

data collection
We conducted interviews and fieldwork between September 2008 and January 2011 (Petracca et al. 2014).On arrival in a community, we interviewed local authorities, non-governmental organizations (NGOs), rancher associations, and people with different degrees of specialization and knowledge on local wildlife such as veterinarians, hunters, and other local people.During Ramírez-Bravo and Hernández-Santin | Carnivores in Puebla, Central Mexico patch usage in heterogeneous areas (Taki et al. 2007).In each study site, we set seven stations: one in the center and six forming an hexagon with a distance of 200 m from each station.We identified tracks using the field guide by Aranda (2000).Opportunistic evidence of presence included scats, tracks, and other sign that could indicate carnivore or prey presence.Tracks were transferred to acrylic casts and then to plastic bags.We collected scats in Tehuacán-Sierra Negra for another portion of a larger project that includes analyzing food habits.Scats found in Sierra Norte and Mixteca were only identified using external characteristics such as size and shape (Aranda 2000) and then photographed.Collection sites were georeferenced using a GPS device, and integrated into a statewide animal sign database that is currently under development.
To complement our fieldwork, we conducted a bibliographic research that included voucher-based published records (López-Wilchis and López Jardines 1998), mammal databases including the Mexican National Commission for Knowledge and Use of Biodiversity (CONABIO), published journal articles, and Bachelor theses from two local universities (Universidad de las Américas-Puebla, San Andres Cholula, Puebla) and Benemérita Universidad Autónoma de Puebla, Puebla, Puebla).We subdivided all records by type, as 'indirect observations', 'signs', 'photographs', and 'interviews with physical evidence' that were records obtained from interviews (human accounts) accompanied by physical evidence (Appendix).
Finally, we developed a distribution map for each species using ArcView 3.2 (ESRI).We overlaid our records on a layer representing natural protected areas (Comisión Nacional de Áreas Naturales Protegidas 2011) with the distribution map for each species obtained from InfoNatura (InfoNatura 2007).When a record was located outside the known distribution of a given species, we measured the straight-line distance between the new record and the closest edge of the current known distribution.

RESuLtS And dIScuSSIOn
We surveyed 110 localities distributed throughout the seven survey-sites and obtained 519 records (Table 1).Of these, 156 correspond to field data and 363 to oral reports.Additionally, bibliographical research resulted in 214 records of carnivores in Puebla.Published reports contained 163 records within our study site (Table 1).
We increased the number of carnivores known to occur in Puebla from 18 (Ramírez-Pulido et al. 2005) Table 1.List of carnivores present in Puebla, including their risk categories under different classifications and their evidence type recorded during this project.For each classification of risk category, we kept original acronyms and categories.The second column "SEM" represents those listed under the Official Mexican Norm, given by SEMARNAT (Diario Oficial, 2010): P (in danger of extinction), A (threatened), Pr (under special protection).The third column "CITES" corresponds to risk categories from CITES (UNEP-WCMC, 2011): Appendix SI (threatened), II (species that are not threatened but could become threatened without regulations on their commercialization), III (species included by a party that currently regulates that species commercialization and needs cooperation from other countries to avoid illegal non-sustainable exploitation).The fourth column "IUCN" represents risk categories from IUCN (IUCN, 2011): EN (endangered), DD (incomplete information), VU (vulnerable), and NT (nearly threatened).Columns 5 to 8 correspond to the type of evidence found during this project with the number of record locations in parenthesis: "DO" stands for direct observation, "S" for sign, "P" for photograph, and "AR" for additional record.Eleven of the 21 species we found are listed under some kind of risk category (SEMARNAT 2010).Four are listed as endangered, five are as threatened, and two are under special protection (Table 1), which means that 50% of the carnivore species in Puebla are under some risk category.In general, carnivores are vulnerable to human-carnivore conflicts, and to habitat loss (Woodroffe and Ginsberg 1998).This holds true in our study area.Hunting has been reported in several regions of Puebla (Ramírez-Pulido et al. 2005).Human-carnivore issues result in control practices such as poisoning, which interviewees admitted as a common practice aimed at eliminating some species, such as Coyotes (Canis latrans) and Coatis (Nasua narica), from agricultural areas.Habitat loss has been high in some regions such as Sierra Norte (Evangelista et al. 2010).
Most of the carnivore records were outside protected areas and were more frequent in forest fragments (see maps in Appendix).Thus, it is imperative to revise the natural preserve network to improve carnivore conservation in Puebla and to include habitats that have not yet been protected.In addition, more efforts should be made to involve local people in sustainableuse practices that aid carnivore conservation outside of protected areas.

AcKnOwLEdgEMEntS
We thank National Geographic Society who provided funding necessary to launch the Project during 2008-2009, to the Panthera organization, which gave support for our work in the north of Puebla during 2010, and to the Durrell Wildlife Conservation Trust, which provided funds for fieldwork in the Tehuacan-Sierra Negra region during 2011.We also acknowledge the Departamento de Ciencias Químico Biológicas de la Universidad de las Américas, Puebla for providing access to their facilities and other support during this project.Moreover, we would like to thank each municipality for providing all the information about the situation within their territories.Special thanks go to the Oficina de Turismo in Hueytamalco and to regiduría de Ecología de Cuetzalan del Progreso.We thank the association ARS de la Mixteca, A.C., the Tehuacán Cuicatlán biosphere reserve, the Natural Protected Area of Cuenca Hidrológica Río Necaxa, Ecoturismo Ixkit, Ojo de Agua, and Xochiquetzal for giving us the support to carry out this project.We hope to have the support of local communities that will allow us to continue with the project.We would also like to thank all the institutions that have supported us throughout these two years and to the people who have so kindly answered our interviews within their jobs, associations, and communities.Finally, we would like to thank the anonymous referees and the editor for the valuable commentaries and suggestions.

APPEndIX distribution maps and species records found during our study
Here we present species records subdivided by type.Thus, records obtained through physical evidence, mainly skins and mounted specimens appear under "direct observation", records made from indirect observation such as tracks, scats, and scrapes are listed under "sign", under "photograph" we listed pictures taken using camera-traps are unless stated otherwise, and "additional records" refers to those found from bibliographical research.Records obtained from interviews (human accounts) without physical evidence are not considered in these maps.The number of records is given in parenthesis, following the category, location, or source where each record was found.We attached a map of the records and potential distribution from Info-Natura (2007) for each species to compare them with reported distribution.
Photograph (1): Sierra Norte.This record is a photograph of a juvenile puma, hunted in CF near the community Xicotepec (ca.2001) (Figure A2).

Lynx rufus
Photograph (1): Mixteca.It was taken on an unused trail on TDF with patches of Acacia forest near Chiautla de Tapia (Figue A3).
Additional records ( 13   Leopardus pardalis (Linnaeus, 1758) Common name: Ocelote, Ocelot Direct observation (2): Sierra Norte.We found skins owned by hunters.The first was hunted near Villa Lázaro Cárdenas where the coastal prairies are dominated by agricultural areas with patches of TF.The second, found in Cuetzalán, was collected on CF; however, it is an old record and its collection date remains uncertain (Figure A4).
Photograph (1): Sierra Norte.We camera-trapped an adult male in Sierra Norte (near Vega Chica) in TF.

Leopardus wiedii (Schinz, 1821) Common name: Tigrillo
Direct observation (8): Sierra Norte.These records correspond to skins, mounted specimens, and one kept as pet in communities found in a stretch of TF and CF (Figure A6).
Photographs (2): Sierra Norte.We caught L. weidii several times during nights in January and June 2010 near the community Telolotla , another one was photographed during July near the community of El Tecomate (Figure A6).

Canis latrans (Say, 1823) Common name: Coyote
Direct observation (3): Mixteca, Sierra Norte, Tehuacan-Sierra Negra.These records are skins; the one we found in Mixteca (near Santa Ana Tecolapa) was hunted on December 2010 in TDF with moderate perturbation.The one in Sierra Norte (near Olintla) occurred in patches of TDF.Moreover, we found  Ramírez-Bravo and Hernández-Santin | Carnivores in Puebla, Central Mexico skins at a local museum, within the botanical garden named "Helia Bravo Hollis" in Zapotitlán de las Salinas (Tehuacan-Sierra Negra), which are thought to have been hunted in XS with moderate perturbation (Figure A7).
Sign ( 6): Mixteca, Sierra Norte (2), Tehuacan-Sierra Negra (3).We found tracks and heard vocalizations in Mixteca (near Agua Dorada within TDF).In Sierra Norte we also heard vocalizations near a canyon with TF close to Tuzamapan de Galeana, and found tracks in a ranch close to Villa Lázaro Cárdenas.In Tehuacan-Sierra Negra we found tracks in TDF with XS near the communities San Esteban Necoxcalco, San Antonio Cañada, and Corral Macho; where local people indicated that coyotes might be rare due to a strong poisoning campaign targeted towards feral dogs (Figure A7).
Photographs (8): Mixteca (3), Sierra Norte (2), Tehuacan-Sierra Negra (3).We obtained pictures of grey fox in a mix of TDF with XS in communities of Mixteca (Santa Ana Tecolapa, Chiautla de Tapia, and Agua Dorada) and of Tehuacan-Sierra Negra (San Antonio Cañada, Corral Macho, and San Esteban Necoxcalco).In Sierra Norte we obtained pictures in CF near Cuetzalan and TF near Tuxtla.Given the species habits, all pictures were taken indistinctly of time of day and month (Figure A8).

Familia Mustelidae
Taxidea taxus (Schreber, 1778) Common name: Tejon, Badger Signs (1): Mixteca.We found digging along the edge of a wall; our findings were corroborated by locals who had seen the species around (Figure A9).

Galictis vittata (Schreber, 1776) Common name: Grison
Direct observation (2): Sierra Norte.We found 2 mounted specimens of unknown sex in Tuzamapan.The hunter he found them in a coffee plantation in a canyon from the Tecolutla river.Moreover, in a canyon with TF near Jopala, a male was hunted in April 2010.This specimen was later purchased for a regional dance called "Los Huehues" in the community Vicente Guerrero, where it was later found mummified.Given its unprofessional mummification, most of its hair had been lost, but the remnant hair and shape helped to its identification (Figure A12).

Family Procyonidae
Nasua narica (Linnaeus, 1766) Common name: Coatié, White-nosed Coati This is one of the species with the widest distribution and most records in Puebla.
Direct observation (9): Sierra Norte.We found pets, skins, and individuals observed in the wild while conducting fieldwork.In all cases, hunted and pet specimens had been found close to the communities where they were taken (Figure A17).
Signs (6): Sierra Norte, Tehuacan-Sierra Negra (5).We found tracks in Sierra Norte (San Diego) or from different communities close to the preserve Tehuacan-Cuicatlan in XS with patches of TDF (Figure A18).

Potos flavus
Additional records (2): Sierra Norte (2).Ocotal and Las Margaritas (Ramírez-Pulido et al. 2005) (Figure A20).(Linnaeus, 1758) Common name: Mapache, Raccoon This is one of the widest spread species in the state because it can be found in different ecosystems.

Procyon lotor
Direct observation (6): Sierra Norte.These include pets, skins, and individuals observed while conducting   field work.In all cases, the individuals were found near the communities where they had been captured or hunted (Figure A21).

Figure 1 .
Figure 1.Survey areas in the state of Puebla, delimited according to their accessibility and connection with neighboring municipalities.

Figure A1 .
Figure A1.Jaguar records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure 3 .
Figure 3. Bobcat records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A4 .
Figure A4.Ocelot records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A5 .
Figure A5.Jaguarundi records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A6 .
Figure A6.Margay records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A7 .
Figure A7.Coyote records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A8 .
Figure A8.Gray Fox records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A10 .
Figure A10.Otter records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A11 .
Figure A11.Tayra records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A12 .
Figure A12.Grison records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A13 .
Figure A13.Long-tailed weasel records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A14 .
Figure A14.Hooded skunk records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A15 .
Figure A15.Spotted skunk records in the state of Puebla and distribution obtained from Infonatura.

Figure A16 .
Figure A16.Eastern hog-nosed skunk records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A17 .
Figure A17.Coatie records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A18 .
Figure A18.Ringtail records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A20 .
Figure A20.Kinkajou records in the state of Puebla and distribution obtained from InfoNatura (2007).

Figure A21 .
Figure A21.Raccoon records in the state of Puebla and distribution obtained from InfoNatura (2007).

Common name Species Risk category Evidence type SEM CITES IUCN DO S P AR
Bobcat (Lynx rufus), and Tropical Ringtail (Bassariscus sumichrasti) (Appendix).The distribution of Ocelot is expanded northwards by 51 km into Mixteca.The distribution of Bobcat is expanded northward by 56 km in Sierra Norte.There was a report of a female Tropical Ringtail collected in Mixteca in 1970 (López-Wilchis and López-Jardines 1998).We expand the distribution of tropical ringtail 86 km north into Mixteca.