Abstract
Measuring changes in species distribution and understanding factors influencing site occupancy are recurring goals in wildlife studies. Imperfect detection of species hinders such studies, resulting in the underestimation of the number of sites occupied by the species of interest. American red squirrels (Tamiasciurus hudsonicus) are sampled traditionally with live-traps that require substantial resources to deploy and monitor. Here, we assessed whether auditory methods yield similar detection probabilities. We compared the detection probability of American red squirrels in boreal forest using point counts, playback counts, and live-trapping. Over the summer of 2014, we conducted three trapping sessions in 60 sites within black spruce forests of northwestern Quebec, Canada. We also conducted 10 min point counts in the same sites, together with playback counts using recordings of American red squirrel alarm and territorial calls. Using dynamic occupancy models to analyse three primary periods, all composed of three secondary periods, we found that the detection probability of squirrels from point counts was as high as with live-trapping. Our results thus highlight the value of the point count method in measuring American red squirrel occupancy.
Similar content being viewed by others
References
Allard-Duchêne, A., Pothier, D., Dupuch, A., Fortin, D., 2014. Temporal changes in habitat use by snowshoe hares and red squirrels during post-fire and post-logging forest succession. For. Ecol. Manag. 313, 17–25.
Bayne, E.M., Hobson, K.A., 2000. Relative use of contiguous and fragmented boreal forest by red squirrels (Tamiasciurus hudsonicus). Can. J. Zool. 78, 359–365.
Bayne, E.M., Hobson, K.A., 2002. Effects of red squirrel (Tamiasciurus hudsonicus) removal on survival of artificial songbird nests in boreal forest fragments. Am. Midl. Nat. 147, 72–79.
Bergeron, Y., Gauthier, S., Flannigan, M., Kafka, V., 2004. Fire regimes at the transition between mixedwood and coniferous boreal forest in northwestern Quebec. Ecology 85, 1916–1932.
Blouin, J., Berger, J.P., 2002. Guide de reconnaissance des types écologiques-Région écologique 5a Plaines de l’Abitibi. Ministère des Ressources Naturelles et de la Faune, Direction des Inventaires Forestiers, Division de la classification écologique et productivité des stations, Québec. Rep. n° 2002–3072, Québec, Canada, pp. 1–180.
Bosson, CO., Islam, Z., Boonstra, R., 2012. The impact of live trapping and trap model on the stress profiles of North American red squirrels. J. Zool. 288, 159–169.
Boutin, S., Wauters, LA., McAdam, A.G., Humphries, M.M., Tosi, G., Dhondt, A.A., 2006. Anticipatory reproduction and population growth in seed predators. Science 314, 1928–1930.
Buchanan, J.B., Lundquist, R.W., Aubry, K.B., 1990. Winter populations of Douglas’ squirrels in different-aged Douglas-fir forests. J. Wildl. Manage. 54, 577–581.
Burke Da Silva, K., Kramer, D.L., Weary, D.M., 1994. Context-specific alarm calls of the eastern chipmunk, Tamias striatus. Can.J. Zool. 72, 1087–1092.
Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference: A Practical Information-theoretic Approach, 2nd ed. Springer-Verlag, New York.
Burton, A.C., Neilson, E., Moreira, D., Ladle, A., Steenweg, R., Fisher, J.T., Bayne, E., Boutin, S., 2015. Wildlife camera trapping. a reviewand recommendations for linking surveys to ecological processes. J. Appl. Ecol. 52, 675–685.
Callahan, J.R., 1993. Squirrels as predators. Great Basin Nat. 1, 137–144.
Carey, A.B., 2000. Effects of new forest management strategies on squirrel populations. Ecol. Appl. 10, 248–257.
Dantzer, B., Boutin, S., Humphries, M., McAdam, A.G., 2012. Behavioral responses of territorial red squirrels to natural and experimental variation in population density. Behav. Ecol. Sociobiol. 66, 865–878.
Darveau, M., Bélanger, L., Huot, J., Mélancon, E., DeBellefeuille, S., 1997. Forestry practices and the risk of bird nest predation in a boreal coniferous forest. Ecol. Appl. 7, 572–580.
Drapeau, P., Leduc, A., McNeil, R., 1999. Refiningthe use of point counts at the scale of individual points in studies of bird-habitat relationships. J. Avian Biol. 30, 367–382.
Elliot, L., Mack, T., 1994. Le Son De Nos Forêts. Centre de conservation de la faune ailée de Montréal, Canada.
Fenton, N.J., Bergeron, Y., 2006. Facilitative succession in a boreal bryophyte community driven by changes in available moisture and light. J. Veg. Sci. 17, 65–76.
Fisher, J.T., Boutin, S., Hannon, S.J., 2005. The protean relationship between boreal forest landscape structure and red squirrel distribution at multiple spatial scales. Land. Ecol. 20, 73–82.
Fiske, I., Chandler, R., 2011. Unmarked: an R package for the fitting hierarchical models ofwildlife occurrence and abundance. J. Stat. Softw. 43, 1–23.
Garden, J.G., McAlpine, C.A., Possingham, H.P., Jones, D.N., 2007. Using multiple survey methods to detect terrestrial reptiles and mammals: what are the most successful and cost-efficient combinations? Wildl. Res. 34, 218–227.
Gauthier, S., Vaillancourt, M.A., Leduc, A., De Grandpré, L., Kneeshaw, D., Morin, H., Drapeau, P., Bergeron, Y., 2008. L’aménagement écosystémique en forêt boréale, 1st ed. Presses de l’Université du Québec, Québec, Canada.
Getschow, C.M., Rivers, P., Sterman, S., Lumpkin, D.C., Tarvin, K.A., 2013. Does gray squirrel (Sciurus carolinensis) response to heterospecific alarm calls depend on familiarity oracoustic similarity? Ethology 119, 983–992.
Gompper, M.E., Kays, R.W., Ray, J.C., Lapoint, S.D., Bogan, DA., Cryan, J.R., 2006. A comparison of noninvasive techniques to survey carnivore communities in northeastern North America. Wildl. Soc. Bull. 34, 1142–1151.
Green, E., Meagher, T., 1998. Red squirrels, Tamiasciurus hudsonicus, produce predator-class specific alarm calls. Anim. Behav. 55, 511–518.
Gurnell, J., McDonald, R., Lurz, P.W.W., 2011. Making red squirrels more visible: the use of baited visual counts to monitor populations. Mammal Rev. 41, 244–250.
Haigh, A., Butler, F., O’Riordan, R.M., 2012. An investigation into the techniques for detecting hedgehogs in a rural landscape. J. Negat. Results 9, 15–26.
Harris, S., Cresswell, W.J., Forde, P.G., Trewhella, W.J., Woodlard, T., Wray, S., 1990. Home range analysis using radiotracking data - a review of problems and techniques particularly as appliedtothe study of mammals. Mammal Rev. 20, 97–123.
Hubbard, C.R., 2008. A Comparison of Invasive and Non-invasive Techniques for Measuring Fiddler Crab Density in a Salt Marsh. (M.Sc. Dissertation). Georgia Southern University, Statesboro, USA.
Imbeau, L., St-Laurent, M.H., Marzell, L., Brodeur, V., 2015. Current capacity to conduct ecologically sustainable forest management in northeastern Canada reveals challenges forconservation of biodiversity. Can. J. For. Res. 45, 567–578.
Kéry, M., Schmidt, B.R., 2008. Imperfect detection and its consequences for monitoring in conservation. Community Ecol. 9, 207–216.
Kellner, K.F., Swihart, R.K., 2014. Accounting for imperfect detection in ecology: a quantitative review. PLoS One 9, e111436.
Klenner, W., Charles, J., Krebs, C.J., 1991. Red squirrel population dynamics I. The effect of supplemental food ondemography. J. Anim. Ecol. 60, 961–978.
Larsen, K.W., Boutin, S., 1994. Movements, survival, and settlement of red squirrel (Tamiasciurus hudsonicus) offspring. Ecology 75, 214–223.
Larsen, K.W., Boutin, S., 1995. Exploring territory quality in the North American red squirrel through removal experiments. Can.J. Zool. 73, 1115–1122.
Larsen, K.W., 1993. Female Reproductive Success in the North American Red Squirrel (Tamiasciurus hudsonicus). Ph. D. Thesis. Department of Zoology, University of Alberta, Edmonton.
Lishak, R.S., 1984. Alarm vocalizations of adult gray squirrels. J. Mammal. 65, 681–684.
MacKenzie, D.I., Bailey, L.L., 2004. Assessing the fit of site-occupancy models. J. Agric. Biol. Environ. Stat. 9, 300–318.
MacKenzie, D.I., Nichols, J.D., Lachman, G.B., Droege, S., Andrew Royle, J.A., Langtimm, C.A., 2002. Estimating site occupancy rates when detection probabilities are less than one. Ecology 83, 2248–2255.
MacKenzie, D.I., Nichols, J.D., Hines, J.E., Knutson, M.G., Franklin, A.B., 2003. Estimating site occupancy, colonization and local extinction when a species is detected imperfectly. Ecology 84, 2200–2207.
MacKenzie, D.I., Nichols, J.D., Royle, J.A., Pollock, K.H., Bailey, L.L., Hines, J.E., 2006. Occupancy Estimation and Modelling. Academic Press Burlington, USA.
Martin, J.L., Joron, J., 2003. Nest predation in forest birds: influence of predator type and predator’s habitat quality. Oikos 102, 641–653.
Mazerolle, M.J., Bailey, L.L., Kendall, W.L., Royle, J.A., Converse, S.J., Nichols, J.D., 2007. Makinggreat leaps forward: accounting fordetectability in herpetological field studies. J. Herpetol. 41, 672–689.
Mazerolle, M.J., 2015. AICcmodavg: Model Selection and Multimodel Inference Based on (Q)AIC(c). R Package Version 2.0-3.
Mori, E., Ancillotto, L., Menchetti, M., Romeo, C., Ferrari, N., 2013. Italian red squirrels and introduced parakeets: victims or perpetrators? Hystrix 24, 195–196.
Mortelliti, A., Boitani, L., 2008. Inferring red squirrel (Sciurus vulgaris) absence with hair tubes surveys: a sampling protocol. Eur. J. Wildl. Res. 54, 353–356.
Newson, S.E., Rexstad, E.A., Baillie, S.R., Buckland, S.T., Aebischer, N.J., 2010. Population change of avian predators and grey squirrels in England: is there evidence foran impact on avian prey populations? J. Appl. Ecol. 47, 244–252.
Otto, C.R.V., Roloff, G.J., 2011. Using multiple methods to assess detection probabilities of forestfloorwildlife.J. Wildl. Manag. 75, 423–431.
Pacifici, K., Simons, T.R., Pollock, K.H., 2008. Effects of vegetation and background noise on the detection process in auditory avian point-count surveys. Auk 125, 600–607.
Patterson, J.E., Malcolm, J.R., 2010. Landscape structure and local habitat characteristics as correlates of Glaucomys sabrinus and Tamiasciurus hudsonicus occurrence. J. Mammal. 91, 642–653.
Pearce, J.L., Boyce, M.S., 2006. Modelling distribution and abundance with presence-only data. J. Appl. Ecol. 43, 405–412.
Petitot, M., Manceau, N., Geniez, P., Besnard, A., 2014. Optimizing occupancy surveys by maximizing detection probability: application to amphibian monitoring in the Mediterranean region. Ecol. Evol. 4, 3538–3549.
Pollock, K.H., Nichols, J.D., Simons, T.R., Farnworth, G.L., Bailey, L.L., Sauer, J.R., 2002. Large scale wildlife monitoring studies: statistical methods for design and analysis. Environmetrics 13, 1–15.
Pradel, R., 1996. Utilization of capture-mark-recapture forthe study of recruitment and population growth rate. Biometrics 52, 703–709.
Price, K., Boutin, S., Ydenberg, R., 1990. Intensity of territorial defense in red squirrels: an experimental test of the asymmetric warofattrition. Behav. Ecol. Sociobiol. 27, 217–222.
R Development Core Team, 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Ralph, C.J., Sauer, J.R., Droege, S., 1995. Monitoring bird populations by point counts. USDA Forest Service, Pacific Southwest Research Station. General Technical Report PSW-GTR-149, Albany, USA.
Randler, C., 2006. Red squirrels (Sciurus vulgaris) respond to alarm calls of Eurasian jays (Garrulus glandarius). Ethology 112, 411–416.
Reitsma, L.R., Holmes, R.T., Sherry, T.W., 1990. Effects of removal of red squirrels, Tamiasciurus hudsonicus, and Eastern chipmunks, Tamias striatus, on nest predation in a Northern hardwood forest: an artificial nest experiment. Oikos 57, 375–380.
Richards, D.G., 1981. Environmental acoustics and censuses of singing birds. Stud. Avian Biol. 6, 297–300.
Richmond, O.M.W., Hines, J.E., Beissinger, S.R., 2010. Two-species occupancy models: a new parameterization applied to co-occurrence of secretive rails. Ecol. Appl. 20, 2036–2046.
Russell, R.E., Lehmkuhl, J.F., Buckland, S.T., Saab, VA., 2010. Short-term responses of red squirrels to prescribed burning in the Interior Pacific Northwest, USA. J. Wildl. Manag. 74, 12–17.
Scott, J.M., Heglund, P.J., Morrison, M.L., Haufler, J.B., Raphael, M.G., Wall, WA., Samson, F.B., 2002. Predicting Species Occurences: Issues of Scale and Accuracy, 1st ed. Island Press, Washington, USA.
Selonen, V., Varjonen, R., Korpimäki, E., 2015. Immediate or lagged responses of a red squirrel population to pulsed resources. Oecologia 177, 401–411.
Shonfield, J., Taylor, R.W., Boutin, S., Humphries, M.M., McAdam, A.G., 2012. Territorial defence behaviour in red squirrels is influenced by local density. Behaviour 149, 369–390.
Siepielki, A.M., 2006. A possible role for red squirrels in structuring breeding bird communities in lodgepole pine forests. Condor 108, 232–238.
Sieving, K.E., Willson, M.F., 1998. Nest predation and avian species diversity in northwestern forest understory. Ecology 79, 2391–2402.
Sjögren-Gulve, P., Hanski, I., 2000. Metapopulation viability analysis using occupancy models. Ecol. Bull. 48, 53–71.
Smith, J.B., Jenks, A.J., Klaver, R.W., 2007. Evaluating detection probabilities for American marten in the Black Hill, South Dakota. J. Wildl. Manag. 71, 2412–2416.
Smith, C.C., 1978. Structure and function of the vocalizations of tree squirrels (Tamiasciurus). J. Mammal. 59, 793–808.
Snyder, D.P., 1982. Tamias striatus. Mamm. Species 168, 1–8.
Steele, MA., 1998. Tamiasciurus hudsonicus. Mamm. Species 586, 1–9.
Wauters, L., Dhondt, A.A., 1993. Immigration pattern and success in red squirrels. Behav. Ecol. Sociobiol. 33, 159–167.
Wheatley, M., Larsen, K.W., Boutin, S., 2002. Does density reflect habitat quality for North American red squirrels during a spruce-cone failure? J. Mammal. 83, 716–727.
Willson, M.F., De Santo, T.L., Sieving, K.E., 2003. Red squirrels and predation risk to bird nests in northern forests. Can.J. Zool. 81, 1202–1208.
Wilson, D.R., Goble, A.R., Boutin, S., Humphries, M.M., Coltman, D.W., Gorrell, J.C., Shonfield, J., McAdam, A.G., 2015. Red squirrels use territorial vocalizations for kin discrimination. Anim. Behav. 107, 79–85.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chavel, E.E., Mazerolle, M.J., Imbeau, L. et al. Comparative evaluation of three sampling methods to estimate detection probability of American red squirrels (Tamiasciurus hudsonicus). Mamm Biol 83, 1–09 (2017). https://doi.org/10.1016/j.mambio.2016.11.003
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1016/j.mambio.2016.11.003