Use of distribution models in the conservation of a Mexican endemic lagomorph

Authors

  • Luis José Aguirre-López Universidad Nacional Autónoma de México
  • Tania Escalante Universidad Nacional Autónoma de México

Keywords:

ecological niche modelling, MaxEnt, natural protected area, remote sensing, suitability, volcano rabbit.

Abstract

The volcano rabbit (Romerolagus diazi), endemic to the central-eastern Transmexican Volcanic Belt, is one of the most threatened lagomorphs worldwide. Several factors threaten to decrease its geographical distribution, which is already restricted to the Pelado, Tláloc, Iztaccíhuatl, and Popocatépetl volcanoes. Our study aimed to propose priority areas for the conservation of this rabbit within Iztaccíhuatl-Popocatépetl National Park (IPNP) based on species distribution models. Volcano rabbit presence data were collected through different field sampling techniques and public and private databases. The environmental predictors used to model suitability were obtained from both open-access remote sensors and topographic information. The models’ performance was adjusted by evaluating different sets of variables and data to improve the certainty of the results. We obtained an area of 132.5 km2 within the IPNP potentially occupied by the volcano rabbit and a high suitability area of 7 km2. In addition, four priority conservation polygons for the volcano rabbit were identified within the National Park. We showed that the suitability and potential distribution are not uniform in the park, being the alpine meadow dominated by Muhlenbergia sp., the most suitable area for R. diazi. Therefore, the conservation strategies should focus on preserving these meadows in the prioritized polygons, avoiding tourist and unskilled personnel’s access. This work represents a contribution to the conservation of the volcano rabbit and a theoretical and practical tool for use in the IPNP.

References

AGUILAR-TOMASINI, M. A., T. ESCALANTE, AND M. FARFÁN. 2020. Effectiveness of natural protected areas for preventing land use and land cover changes of the Transmexican Volcanic Belt, Mexico. Regional Environmental Change 20:1-9.

AKAIKE, H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19:716-723.

ANDERSON, B. J., H. R. AKÇAKAYA, M. B. ARAÚJO, D. A. FORDHAM, E. MARTÍNEZ-MEYER, W. THUILLER, AND B. W. BROOK. 2009. Dynamics of range margins for metapopulations under climate change. Proceedings of the Royal Society B: Biological Sciences 276:1415-1420.

ARIZA, A. 2013. Descripción y Corrección de Productos Landsat 8 LDCM (Landsat Data Continuity Mission). Bogotá Instituto Geográfico Agustín Codazzi.

AUSTIN, M. 2007. Species distribution models and ecological theory: A critical assessment and some possible new approaches. Ecological Modelling 200:1-19.

AVDAN, U., AND G. JOVANOVSKA. 2016. Algorithm for automated mapping of land surface temperature using LANDSAT 8 satellite data. Journal of Sensors 2016.

BARRERA, A. 1966. Redefinición de Cediopsylla Jordán y Hoplopyllus nuevas especies, comentarios sobre el concepto de relicto y un caso de evolución convergente. Revista de la Sociedad Mexicana de Historia Natural 27:67-83.

BARSI, J. A., J. R. SCHOTT, S. J. HOOK, N. G. RAQUENO, B. L. MARKHAM, AND R. G. RADOCINSKI. 2014. Landsat-8 thermal infrared sensor (TIRS) vicarious radiometric calibration. Remote Sensing 6:11607-11626.

BARVE, N., V. BARVE, A. JIMÉNEZ-VALVERDE, A. LIRA-NORIEGA, S. P. MAHER, A. T. PETERSON, J. SOBERÓN, AND F. VILLALOBOS. 2011. The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling 222:1810-1819.

BURNHAM, K. P., AND D. R. ANDERSON. 2002. Model selection and multimodel inference: a practical information-theoretic approach. 2nd ed. Springer-Verlag. Berlin, Germany.

CARLSON, T. N., AND D. A. RIPLEY. 1997. On the relation between NDVI, fractional vegetation cover, and leaf area index. Remote Sensing of Environment 62:241-252.

CERVANTES, F. A. 1982. Observaciones sobre la reproducción del zacatuche o teporingo Romerolagus diazi. Mammalia: Lagomorpha. Doñana Acta Vertebrata 9:416-420.

CERVANTES, F. A., AND J. MARTÍNEZ-VÁZQUEZ. 1996. Historia natural del conejo zacatuche o teporingo (Romerolagus diazi). Pp. 29-40, in Ecología y Conservación del conejo zacatuche y su hábitat (Velázquez, A., F. Romero, and J. López-Paniagua, eds.). Universidad Autónoma de México-Fondo de Cultura Económica. Mexico City, Mexico.

CHAMBERLAIN, S., V. BARVE, D. MCGLINN, D. OLDONI, P. DESMET, L. GEFFERT, AND K. RAM. 2020. rgbif: Interface to the Global Biodiversity Information Facility API.

COBOS, M. E., A. T. PETERSON, N. BARVE, AND L. OSORIO-OLVERA. 2019. Kuenm: An R package for detailed development of ecological niche models using Maxent. PeerJ 2019:1-15.

COLWELL, R. K., G. BREHM, C. L. CARDELÚS, A. C. GILMAN, J. T. LONGINO, C. L. CARDELUS, A. C. GILMAN, AND J. T. LONGINO. 2008. Global Warming, Elevational Range Shifts, and Lowland Biotic Attrition in the Wet Tropics. Science 322:258-261.

COMISIÓN NACIONAL DE ÁREAS NATURALES PROTEGIDAS (CONANP). 2013. Programa de manejo Parque Nacional Iztaccíhuatl-Popocatépetl. Mexico City, Mexico.

CUERVO-ROBAYO, A. P., O. TÉLLEZ-VALDÉS, M. A. GÓMEZ-ALBORES, C. S. VENEGAS-BARRERA, J. MANJARREZ, AND E. MARTÍNEZ-MEYER. 2014. An update of high-resolution monthly climate surfaces for Mexico. International Journal of Climatology 34:2427-2437.

DASH, P., F. M. GÖTTSCHE, F. S. OLESEN, AND H. FISCHER. 2005. Separating surface emissivity and temperature using two-channel spectral indices and emissivity composites and comparison with a vegetation fraction method. Remote Sensing of Environment 96:1-17.

ESCALANTE, T. 2014. Modelos de distribución de especies de mamíferos y suculentas de la Faja Volcánica Transmexicana. Database SNIB-CONABIO_Mamíferos, project JM055. Universidad Nacional Autónoma de México. Facultad de Ciencias. Mexico City, Mexico.

FARÍAS, V., Y. GARCÍA-FERIA, O. TÉLLEZ-VALDÉS, AND V. BERNAL-LEGARIA. 2015. ‘Romerolagus diazi (zacatuche). Distribución potencial.’, escala: 1:1000000, in Distribución potencial de las especies de Leporidae en México y las implicaciones para su conservación., project: JM034, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México. Mexico City, Mexico.

GALINDO-LEAL, C., AND A. VELÁZQUEZ. 1996. Recomendaciones para la conservación del zacatuche. Pp. 147-157, in Ecología y Conservación del conejo zacatuche y su hábitat (Velázquez, A., F. Romero, and J. López-Paniagua, eds.). Universidad Nacional Autónoma de México-Fondo de Cultura Económica. Mexico City, Mexico.

GARRIGA, N., X. SANTOS, A. MONTORI, A. RICHTER-BOIX, M. FRANCH, AND G. LLORENTE. 2012. Are protected areas truly protected? The impact of road traffic on vertebrate fauna. Biodiversity and Conservation 21:2761-2774.

GOOGLE INCORPORATED. 2019. Google Roads.

GOTTFRIED, M., H. PAULI, A. FUTSCHIK, M. AKHALKATSI, P. BARANÄŒOK, J. L. BENITO ALONSO, G. COLDEA, J. DICK, B. ERSCHBAMER, M. R. FERNÁNDEZ-CALZADO, G. KAZAKIS, J. KRAJÄŒI, P. LARSSON, M. MALLAUN, O. MICHELSEN, D. MOISEEV, P. MOISEEV, U. MOLAU, A. MERZOUKI, L. NAGY, G. NAKHUTSRISHVILI, B. PEDERSEN, G. PELINO, M. PUSCAS, G. ROSSI, A. STANISCI, J. P. THEURILLAT, M. TOMASELLI, L. VILLAR, P. VITTOZ, I. VOGIATZAKIS, AND G. GRABHERR. 2012. Continent-wide response of mountain vegetation to climate change. Natural Climate Change 2:111-115.

HE, K. S., B. A. BRADLEY, A. F. CORD, D. ROCCHINI, M. N. TUANMU, S. SCHMIDTLEIN, W. TURNER, M. WEGMANN, AND N. PETTORELLI. 2015. Will remote sensing shape the next generation of species distribution models? Remote Sensing in Ecology and Conservation 1:4-18.

HE, K. S., J. ZHANG, AND Q. ZHANG. 2009. Linking variability in species composition and MODIS NDVI based on beta diversity measurements. Acta Oecologica 35:14-21.

HIJMANS, R. J., S. PHILLIPS, J. LEATHWICK, J. ELITH, AND M. R. J. HIJMANS. 2017. Package ‘dismo.’ Circles 9:1-68.

HOFFMAN, A., F. CERVANTES, AND J. MORALES-MALACARA. 1994. Ectoparásitos del conejo zacatuche (Romerolagus diazi). Anales del Instituto de Biología 65:209-215.

HUNTER, M., AND W. CRESSWELL. 2015. Factors affecting the distribution and abundance of the Endangered volcano rabbit Romerolagus diazi on the Iztaccihuatl volcano. Oryx 49:366-375.

INSTITUTO NACIONAL DE ESTADÍSTICA Y GEOGRAFÍA (INEGI). 2010. Censo de Población y Vivienda 2010. Principales resultados por localidad (ITER). Mexico.

INSTITUTO NACIONAL DE ESTADÍSTICA Y GEOGRAFÍA (INEGI). 2013. Continuo de Elevaciones Mexicano (CEM). http://www.beta.inegi.org.mx/app/geo2/elevacionesmex/

LAWLER, J. J., D. WHITE, J. C. SIFNEOS, AND L. L. MASTER. 2003. Rare species and the use of indicator groups for conservation planning. Conservation Biology 17:875-882.

LOBO, J. M., A. JIMÉNEZ-VALVERDE, AND R. REAL. 2008. AUC: A misleading measure of the performance of predictive distribution models. Global Ecology and Biogeography 17:145-151.

MARTÍNEZ-MEYER, E. 2005. Climate change and biodiversity: some considerations in forecasting shifts in species’ potential distributions. Biodiversity Informatics 2:42-55.

MATEO, R. G., Á. M. FELICÍSIMO, AND J. MUÑOZ. 2011. Modelos de distribución de especies: Una revisión sintética. Revista Chilena de Historia Natural 84:217-240.

MEROW, C., M. J. SMITH, AND J. A. SILANDER. 2013. A practical guide to MaxEnt for modeling species’ distributions: What it does, and why inputs and settings matter. Ecography 36:1058-1069.

MONTGOMERY, D., AND E. PECK. 1992. Introduction to linear regression analysis. 2nd ed. Wiley. New York, U. S. A.

MORRONE, J. J., T. ESCALANTE, AND G. RODRÍGUEZ-TAPIA. 2017. Mexican biogeographic provinces: Map and shapefiles. Zootaxa 4277:277-279.

MUSCARELLA, R., P. J. GALANTE, M. SOLEY-GUARDIA, R. A. BORIA, J. M. KASS, M. URIARTE, AND R. P. ANDERSON. 2014. ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods in Ecology and Evolution 5:1198-1205.

OSORIO-OLVERA, L., A. LIRA-NORIEGA, J. SOBERÓN, A. T. PETERSON, M. FALCONI, R. G. CONTRERAS-DÍAZ, E. MARTÍNEZ-MEYER, V. BARVE, AND N. BARVE. 2020. ntbox: An r package with graphical user interface for modelling and evaluating multidimensional ecological niches. Methods in Ecology and Evolution 2020 11:1199-1206.

OSUNA, F., D. GONZÁLEZ, A. E. DE LOS MONTEROS, AND J. A. GUERRERO. 2020. Phylogeography of the Volcano Rabbit (Romerolagus diazi): the Evolutionary History of a Mountain Specialist Molded by the Climatic-Volcanism Interaction in the Central Mexican Highlands. Journal of Mammalian Evolution 27:745-757.

OSUNA, F., R. GUEVARA, E. MARTÍNEZ-MEYER, R. ALCALÁ, AND A. E. DE LOS MONTEROS. 2021. Factors affecting presence and relative abundance of the Endangered volcano rabbit Romerolagus diazi, a habitat specialist. Oryx 1-10.

PETERSON, A. T., M. PAPEŞ, AND J. SOBERÓN. 2008. Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecological Modelling 213:63-72.

PĘKSA, Å., AND M. CIACH. 2015. Negative effects of mass tourism on high mountain fauna: the case of the Tatra chamois Rupicapra rupicapra tatrica. Oryx 49:500-505.

PHILLIPS, S. J., R. P. ANDERSON, AND R. SCHAPIRE. 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190:231-259.

PHILLIPS, S. J., R. P. ANDERSON, M. DUDÍK, R. E. SCHAPIRE, AND M. E. BLAIR. 2017. Opening the black box: an open-source release of Maxent. Ecography 40:887-893.

PRIETO-TORRES, D. A., AND G. PINILLA-BUITRAGO. 2017. Estimating the potential distribution and conservation priorities of Chironectes minimus (Zimmermann, 1780) (Didelphimorphia: Didelphidae). Therya 8:131-144.

QGIS DEVELOPMENT TEAM. 2019. QGIS Geographic Information System. Open Source Geospatial Foundation Project.

RADOSAVLJEVIC, A., AND R. P. ANDERSON. 2014. Making better Maxent models of species distributions: Complexity, overfitting and evaluation. Journal of Biogeography 41:629-643.

RIZO-AGUILAR, A., J. A. GUERRERO, M. G. HIDALGO-MIHART, AND A. GONZÁLEZ-ROMERO. 2015. Relationship between the abundance of the Endangered volcano rabbit Romerolagus diazi and vegetation structure in the Sierra Chichinautzin mountain range. Oryx 49:360-365.

RIZO-AGUILAR, A., J. A. GUERRERO, A. M. P. MONTOYA-LARA, AND C. VALDESPINO. 2014. Physiological stress in volcano rabbit Romerolagus diazi populations inhabiting contrasting zones at the Corredor Biologico Chichinautzin, Mexico. Mammalian Biology 79:357-361.

RÖDDER, D., S. NEKUM, A. F. CORD, AND J. O. ENGLER. 2016. Coupling Satellite Data with Species Distribution and Connectivity Models as a Tool for Environmental Management and Planning in Matrix-Sensitive Species. Environmental Management 58:130-143.

ROUSE, J., R. HAAS, J. SCHELL, AND D. DEERIN. 1973. Monitoring vegetation systems in the Great Plains with ERTS. N. SP-351. Pp. 309-317, in Third ERTS Symposyum. NASA. Washington, U.S.A.

RSTUDIO TEAM. 2018. RStudio: Integrated Development Environment for R. RStudio, Inc. Boston, U. S. A.

SÁNCHEZ-CORDERO, V., M. MUNGUIA, AND A. T. PETERSON. 2004. GIS-based predictive biogeography in the context of conservation. Pp. 311-323, in Frontiers of biogeography: new directions in the geography of nature (Lomolino, M. V., and L. R. Heaney, eds.). Sinauer Associates, Inc. Massachusetts, U. S. A.

SECRETARIA DE MEDIO AMBIENTE Y RECURSOS NATURALES (SEMARNAT). 2013. Diario Oficial. Acuerdo por el que se da a conocer el resumen del Programa de Manejo del Parque Nacional Iztaccíhuatl−Popocatépetl. Mexico.

SOBERÓN, J., L. OSORIO-OLVERA, AND A. T. PETERSON. 2017. Diferencias conceptuales entre modelación de nichos y modelación de áreas de distribución. Revista Mexicana de Biodiversidad 88:437-441.

SOBERÓN, J., AND A. T. PETERSON. 2005. Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodiversity Informatics 2:1–10.

SOBRINO, J. A., AND N. RAISSOUNI. 2000. Toward remote sensing methods for land cover dynamic monitoring: Application to Morocco. International Journal of Remote Sensing 21:353-366.

SOBRINO, J. A., J. C. JIMÉNEZ-MUÑOZ, AND L. PAOLINI. 2004. Land surface temperature retrieval from LANDSAT TM 5. Remote Sensing of Environment 90:434-440.

SOBRINO, J. A., J. C. JIMÉNEZ-MUÑOZ, G. SÃ’RIA, M. ROMAGUERA, L. GUANTER, J. MORENO, A. PLAZA, AND P. MARTÍNEZ. 2008. Land surface emissivity retrieval from different VNIR and TIR sensors. IEEE Transactions on Geoscience and Remote Sensing 46:316-327.

STATHOPOULOU, M., AND C. CARTALIS. 2007. Daytime urban heat islands from Landsat ETM+ and Corine land cover data: An application to major cities in Greece. Solar Energy 81:358-368.

TEAM NETWORK. 2017. Tropical Ecology Assessment and Monitoring Network.

UNITED STATES GEOLOGICAL SURVEY (USGS). 2013. Landsat Missions. https://www.usgs.gov/land-resources/nli/landsat.

UNITED STATES GEOLOGICAL SURVEY (USGS). 2019. Landsat 8. https://earthexplorer.usgs.gov/.

VELAZQUEZ, A., AND G. BOCCO. 1994. Modelling conservation alternatives with ILWIS: a case study of the volcano rabbit. ITC Journal 3:197-204.

VELÁZQUEZ, A., AND J. A. GUERRERO. 2019. Romerolagus diazi. The IUCN Red List of Threatened Species 2019: e.T19742A45180356.

VELÁZQUEZ, A., F. ROMERO, AND L. LEÓN. 1996. Fragmentación del hábitat del conejo zacatuche. Pp. 73-86, in Ecología y Conservación del conejo zacatuche y su hábitat (Velázquez, A., F. Romero, and J. López-Paniagua, eds.). Universidad Nacional Autónoma de México-Fondo de Cultura Económica. Mexico City, Mexico.

VELAZQUEZ, A., AND G. W. HEIL. 1996. Habitat Suitability Study for the Conservation of the Volcano Rabbit (Romerolagus diazi). Journal of Applied Ecology 33:543-554.

VILA-VIÇOSA, C., S. ARENAS-CASTRO, B. MARCOS, J. HONRADO, C. GARCÍA, F. M. VÁZQUEZ, R. ALMEDIA, AND J. GONÇALVES. 2020. Combining Satellite Remote Sensing and Climate Data in Species Distribution Models to Improve the Conservation of Iberian White Oaks (Quercus L.). International Journal of Geo-Information 9:735.

WALTARI, E., AND R. P. GURALNICK. 2008. Ecological niche modelling of montane mammals in the Great Basin, North America: examining past and present connectivity of species across basins and ranges. Journal of Biogeography 36:148-161.

WANG, F., Z. QIN, C. SONG, L. TU, A. KARNIELI, AND S. ZHAO. 2015. An improved mono-window algorithm for land surface temperature retrieval from landsat 8 thermal infrared sensor data. Remote Sensings 7:4268-4289.

WARREN, D. L., AND S. N. SEIFERT. 2011. Ecological niche modeling in Maxent: The importance of model complexity and the performance of model selection criteria. Ecological Applications 21:335-342.

Downloads

Published

2021-08-24

Issue

Section

Articles