Factors affecting the abundance of Peters’s squirrel, Sciurus oculatus, in a population of Central Mexico




Palabras clave:

Royle-Nichols model, Camera trap, Habitat covariates, Detectability, Human disturbance, Small mammal


Peters’s squirrel, Sciurus oculatus, is an endemic species distributed in fragmented populations in Central Mexico, which is one of the most densely populated areas in Mexico. No study has estimated the abundance of this species yet, and the effects of human-environmental factors on its abundance and distribution are unknown. Understanding the role of these factors on its abundance is crucial to its management and conservation. We used the Royle-Nichols model to estimate the abundance and detection probability with detection-non-detection data collected from a camera trap survey. The human-environmental factors that might influence the abundance and distribution of squirrel were modeled. Distance to nearest human settlements had a positive effect on abundance; meanwhile, the presence of the main predator species of the squirrel was a negative factor for detection probability. These findings suggest less abundance or/and a decrease in-ground use in areas with the presence of predators and nearest to human settlements. These results indicate the negative effect of human activities on squirrel abundance and the possible anti-predatory behavior of Peters’s squirrel.


Ahumada, J. A., Hurtado, J., & Lizcano, D. (2013). Monitoring the status and trends of tropical forest terrestrial vertebrate communities from camera trap data: a tool for conservation. Plos One, 8, e73707. https://doi.org/10.1371/journal.pone.0073707

Ariefiandy, A., Purwandana, D., Seno, A., Chrismiawati, M., Ciofi, C., & Jessop, T. S. (2014). Evaluation of three field monitoring-density estimation protocols and their relevance to Komodo dragon conservation. Biodiversity and Conservation, 23, 2473–2490. https://doi.org/10.1007/s10531-014-0733-3

Balmford, A., Green, R. E., & Jenkins, M. (2003). Measuring the changing state of nature. Trends in Ecology and Evolution, 18, 326–330. https://doi.org/10.1016/S0169-5347(03)00067-3

Best, T. L. (1995). Sciurus oculatus. Mammalian species, 498, 1–3. https://doi.org/10.1644/0.498.1

Clare, J. D., Linden, D. W., Anderson, E. M., & MacFarland, D. M. (2016). Do the antipredator strategies of shared prey mediate intraguild predation and mesopredator suppression? Ecology and Evolution, 6, 3884–3897. https://doi.org/10.1002/ece3.2170

De Bondi, N., White, J. G., Stevens, M., & Cooke, R. (2010). A comparison of the effectiveness of camera trapping and live trapping for sampling terrestrial small-mammal communities. Wildlife Research, 37, 456–465. https://doi.org/10.1071/WR10046

de Oliveira, T. G., Ramalho, E. E., & de Paula, R. C. (2012). Red List assessment of the jaguar in Brazilian Amazonia. Cat News, 7, 8–13.

Di Cerbo, A. R., & Biancardi, C. M. (2013). Monitoring small and arboreal mammals by camera traps: effectiveness and applications. Acta Theriologica, 58, 279–283. https://doi.org/10.1007/s13364-012-0122-9

Delibes-Mateos, M., Díaz-Ruiz, F., Caro, J., & Ferreras, P. (2014). Activity patterns of the vulnerable guiña (Leopardus guigna) and its main prey in the Valdivian rainforest of southern Chile. Mammalian Biology-Zeitschrift für Säugetierkunde, 79, 393–397. https://doi.org/10.1016/j.mambio.2014.04.006

Dixon, P. M., Olsen, A. R., & Kahn, B. M. (1998). Measuring trends in ecological resources. Ecological Applications, 8, 225–227. https://doi.org/10.1890/1051-0761(1998)008[0225:mtier]2.0.co;2

Fancourt, B. A., Hawkins, C. E., Cameron, E. Z., Jones, M. E., & Nicol, S. C. (2015). Devil declines and catastrophic cascades, is mesopredator release of feral cats inhibiting recovery of the eastern quoll? Plos One, 10, e0119303. https://doi.org/10.1371/journal.pone.0119303

Gärdenfors, U., Hilton‐Taylor, C., Mace, G. M., & Rodríguez, J. P. (2001). The application of IUCN Red List criteria at regional levels. Conservation Biology, 15, 1206–1212. https://doi.org/10.1111/j.1523-1739.2001.00112.x

Gelman, A., Carlin, J. B., Stern, H. S., & Rubin, D. B. (2003). Bayesian data analysis. London: Chapman and Hall.

Gill, J. A., & Sutherland, W. J. (2000). Predicting the consequences of human disturbance from behavioral decisions. En L. M. Gosling, & W. J. Sutherland (Eds.), Behavior and conservation (pp. 51–64). Cambridge: Cambridge University Press.

Guillera-Arroita, G., Ridout, M. S. & Morgan, B. J. T. (2010). Design of occupancy studies with imperfect detection. Methods in Ecology and Evolution, 1, 131–139. https://doi.org/10.1111/j.2041-210X.2010.00017.x

Hall, E. R. (1981). The mammals of North America. New York: Wiley.

Hernández-Flores, S. D., & Rojas-Martínez, A. E. (2010). Lista actualizada y estado de conservación de los mamíferos del Parque Nacional El Chico, Hidalgo, México. Acta Zoológica Mexicana, 26, 563–583. https://doi.org/10.21829/azm.2010.263800

Kellner, K. (2015). Jags UI, a wrapper around rjags to streamline JAGS analyses. R package version, 1.3.7. Retrieved 12 February 2018, from: http://cran.r-roject.org/package=jagsUI

Kuo, L. & Mallick, B. (1998). Variable selection for regression models. Sankhya, The Indian Journal of Statistics, 60, 65–81.

Lima, S. L., Valone, T. J., & Caraco, T. (1985). Foraging-efficiency-predation-risk trade-off in the grey squirrel. Animal Behaviour, 33,155–165. https://doi.org/10.1016/S0003-3472(85)80129-9

Linden, D. W., Fuller, A. K., Royle, J. A., & Hare, M. P. (2017). Examining the occupancy–density relationship for a low‐density carnivore. Journal of Applied Ecology, 54, 2043–2052. https://doi.org/10.1111/1365-2664.12883

Linkie M. Y., Dinata A., Nugroho A., & Haidir I. A. (2007). Estimating occupancy of a data deficient mammalian species living in tropical rainforests, Sun bears in the Kerinci Seblat region, Sumatra. Biological Conservation, 137, 20–27. https://doi.org/10.1016/j.biocon.2007.01.016

MacKenzie, D. I., Nichols, J. D., Royle, J. A., Pollock, K. H., Bailey, L. L., & Hines, J. E. (2006). Occupancy estimation and modeling, inferring patterns and dynamics of species occurrence. New York: Academic Press.

McCarthy, J. L., Fuller, T. K., McCarthy, K. P., Wibisono, H. T., & Livolsi, M. C. (2012). Using camera trap photos and direct sightings to identify possible refugia for the Vulnerable Sumatran striped rabbit Nesolagus netscheri. Oryx, 46, 438–441. https://doi.org/10.1017/S0030605312000051

McDonald, P. J., Griffiths, A. D., Nano, C. E., Dickman, C. R., Ward, S. J., & Luck, G. W. (2015). Landscape-scale factors determine occupancy of the critically endangered central rock-rat in arid Australia, the utility of camera trapping. Biological Conservation, 191, 93–100. https://doi.org/10.1016/j.biocon.2015.06.027

Monterrubio-Rico, T. C., Guido-Lemus, D., Charre-Medellín, J. F., Zavala-Paramo, M. G., Padilla-Jacobo, G., Cano-Camacho, H. et al. (2013). Nuevos registros de la ardilla de Peters Sciurus oculatus (Peters 1863) para Michoacán y primera genotipificación molecular de la especie. Acta Zoológica Mexicana, 29, 304–316. https://doi.org/10.7550/rmb.34419

Munari, D. P., Keller, C., & Venticinque, E. M. (2011). An evaluation of field techniques for monitoring terrestrial mammal populations in Amazonia. Mammalian Biology-Zeitschrift für Säugetierkunde, 76, 401–408. https://doi.org/10.1016/j.mambio.2011.02.007

O’Connell A. F., Jr., Talancy, N. W., Bailey, L. L., Sauer, J. R., Cook, R., & Gilbert, A. T. (2006). Estimating site occupancy and detection probability parameters for meso and large mammals in a coastal ecosystem. Journal of Wildlife Management, 70, 1625–1633. https://doi.org/10.2193/0022-541X(2006)70[1625:ESOADP]2.0.CO;2

Paull, D. J., Claridge, A. W., & Barry, S. C. (2011). There's no accounting for taste, bait attractants and infrared digital cameras for detecting small to medium ground-dwelling mammals. Wildlife Research, 38, 188–195. https://doi.org/10.1071/WR10203

Plummer, M. (2003). JAGS, a program for analysis of Bayesian graphical models using Gibbs sampling. Proceedings of the 3rd International Workshop on distributed statistical computing. DSC, Vienna, Austria. 20–22 March 2003.

QGIS Development Team (2015). QGIS Geographic Information System. Open Source Geospatial Foundation Project. Retrieved 12 February 2018, from https://qgis.org/es/site/

R Core Team (2017). R: A language and environment for statistical computing’, R Foundation for Statistical Computing. Version 2. Vienna, Austria, R foundation for statistical computing. Retrieved 12 February 2018, from https://www.r-project.org/

Ramos-Lara, N., & López-González, C. A. (2017). Niche segregation between Sciurus aureogaster and S. oculatus in a disturbed forest in central Mexico. Journal of Mammalogy, 98, 1780–1790. https://doi.org/10.1093/jmammal/gyx136

Ridout, M. S., & Linkie, M. (2009). Estimating overlap of daily activity patterns from camera trap data. Journal of Agricultural, Biological, and Environmental Statistics, 14, 322–337. https://doi.org/10.1198/jabes.2009.08038

Royle, J. A. (2004). N-mixture models for estimating population size from spatially replicated counts. Biometrics, 60, 108–115. https://doi.org/10.1111/j.0006-341X.2004.00142.x

Royle, J. A., Chandler, R. B., Sollmann, R., & Gardner, B. (2014). Spatial capture-recapture. Waltham, Massachusetts, Elsevier, Academic Press.

Royle, J. A., & Dorazio, R. M. (2008). Hierarchical Modeling and Inference in Ecology. The Analysis of Data from Populations Metapopulations and Communities. San Diego: Academic Press.

Royle, J. A., & Nichols, J. D. (2003). Estimating abundance from repeated presence–absence data or point counts. Ecology, 84, 777–790. https://doi.org/10.1890/0012-9658(2003)084[0777:EAFRPA]2.0.CO;2

Royle, J. A., Nichols, J. D., & Kéry, M. (2005). Modelling occurrence and abundance of species when detection is imperfect. Oikos, 110, 353–359. https://doi.org/10.1111/j.0030-1299.2005.13534.x

Sánchez-Cordero, V., Illoldi-Rangel, P., Linaje, M., Sarkar, S., & Peterson, A. T. (2005). Deforestation and extant distributions of Mexican endemic mammals. Biological Conservation, 126, 465–473. https://doi.org/10.1016/j.biocon.2005.06.022

Sánchez-Rojas G., Hernández-Flores, S. D., Castillo-Cerón, J., Mejenes-López, S., Aguilar-López, M., &Bravo-Cadena, J. (2016). Riqueza, composición y conservación de los mamíferos del estado de Hidalgo, México. En M. Briones-Salas, Y. Hortelano-Moncada, G. Magaña-Cota, G. Sánchez-Rojas y J. E. Sosa-Escalante (Eds.), Riqueza y conservación de los mamíferos en México a nivel estatal (pp. 281–309). Ciudad de México: Instituto de Biología, Universidad Nacional Autónoma de México/ Asociación Mexicana de Mastozoología A.C./ Universidad de Guanajuato.

Semarnat (Secretaría de Medio Ambiente y Recursos Naturales). (2010). Norma Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. Diario Oficial de la Federación, segunda sección, jueves 30 de diciembre de 2010.

Stanley, T. R., & Royle, J. A. (2005). Estimating site occupancy and abundance using indirect detection indices. Journal of Wildlife Management, 69, 874–883. https://doi.org/10.2193/0022-541X(2005)069[0874:ESOAAU]2.0.CO;2

Suwanrat, S., Ngoprasert, D., Sutherland, C., Suwanwaree, P., & Savini, T. (2015). Estimating density of secretive terrestrial birds (Siamese fireback) in pristine and degraded forest using camera traps and distance sampling. Global Ecology and Conservation, 3, 596–606. https://doi.org/10.1016/j.gecco.2015.01.010

Thorington, R., & Ferrell, K. (2006). Squirrels, the animal answer guide. Baltimore: The John Hopkins University Press.

Towerton, A. L., Penman, T. D., Kavanagh, R. P., & Dickman, C. R. (2011). Detecting pest and prey responses to fox control across the landscape using remote cameras. Wildlife Research, 38, 208–220. https://doi.org/10.1071/WR10213

Valdez-Alarcón, M., & Téllez-Girón, G. (2005). Sciurus oculatus. En G. Ceballos, & G. Oliva (Eds.), Los mamíferos silvestres de México (pp. 556–557). México D.F.: Fondo de Cultura Económica.

Vander Haegen, W. M., Orth, G. R., & Linders, M. J. (2013). Survival and causes of mortality in a northern population of western gray squirrels. The Journal of Wildlife Management, 77, 1249–1257. https://doi.org/10.1002/jwmg.567

Van Der Merwe, M., Brown, J. S., & Jackson, W. M. (2005). The coexistence of fox (Sciurus niger) and gray (S. carolinensis) squirrels in the Chicago metropolitan area. Urban Ecosystems, 8, 335–347. https://doi.org/10.1007/s11252-005-4865-9

Welbourne, D. J., MacGregor, C., Paull, D., & Lindenmayer, D. B. (2015). The effectiveness and cost of camera traps for surveying small reptiles and critical weight range mammals, a comparison with labour-intensive complementary methods. Wildlife Research, 42, 414–425. https://doi.org/10.1071/WR15054


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