Assessing the impact of live-capture, confinement, and translocation on stress and fate in eastern gray squirrels

Abstract Live-capture and translocation are methods to deal with nuisance eastern gray squirrels in North America, but it is unknown how these methods affect squirrel physiology or survival. In this study we validated an enzyme immunoassay (EIA) to measure fecal cortisol metabolites (FCMs) in gray squirrels; assessed their stress response relative to the positioning of the live trap (sun, shade, or control); and assessed the impact of translocation on their long-term stress, movement patterns, and survival using FCM levels, body mass changes, and radiotelemetry. We found that a 5α-pregnane-3β,11β,21-triol-20-one EIA reliably detected acute stress in gray squirrel feces 12–24 h after the stressor; live traps positioned in the sun resulted in higher peak FCM levels compared with traps positioned in the shade; translocated squirrels experienced a 10% mortality rate, compared with no mortality in the controls, although overall fates were the same; translocated squirrels initially explored more and dispersed farther than controls, but after 2 weeks made similar movements; and after controlling for the effect of season, translocation did not affect long-term FCM levels or body mass; this conclusion must be tempered by the low number of recaptures. Our study demonstrates the utility of the FCM assay; that gray squirrels are extremely sensitive to capture, handling, and confinement; and that live-capture must be done in a way that minimizes exposure to additive environmental stressors.

[1]  R. Boonstra Reality as the leading cause of stress: rethinking the impact of chronic stress in nature , 2013 .

[2]  R. Boonstra,et al.  The impact of live trapping and trap model on the stress profiles of North American red squirrels , 2012 .

[3]  R. Palme,et al.  Hair cortisol: a parameter of chronic stress? Insights from a radiometabolism study in guinea pigs , 2012, Journal of Comparative Physiology B.

[4]  C. Krebs,et al.  Mountain‐top and valley‐bottom experiences: the stress axis as an integrator of environmental variability in arctic ground squirrel populations , 2012 .

[5]  D. Réale,et al.  Noninvasive monitoring of fecal cortisol metabolites in the eastern chipmunk (Tamias striatus): validation and comparison of two enzyme immunoassays. , 2012, Physiological and biochemical zoology : PBZ.

[6]  Jessica B. Turner,et al.  Glucocorticoid response to changes in enclosure size and human proximity in the Persian onager (Equus hemionus onager) , 2012, Stress.

[7]  Maria Toledo-Rodriguez,et al.  Stress during Adolescence Increases Novelty Seeking and Risk-Taking Behavior in Male and Female Rats , 2011, Front. Behav. Neurosci..

[8]  R. Boonstra,et al.  Measuring stress in wildlife: techniques for quantifying glucocorticoids , 2011, Oecologia.

[9]  Patrick O. McGowan,et al.  The Neurological Ecology of Fear: Insights Neuroscientists and Ecologists Have to Offer one Another , 2011, Front. Behav. Neurosci..

[10]  R. Chavira,et al.  Preliminary evidence of accumulation of stress during translocation in mantled howlers , 2010, American journal of primatology.

[11]  R. Palme,et al.  Faecal glucocorticoid metabolites: How to express yourself – comparison of absolute amounts versus concentrations in samples from a study in laboratory rats , 2010, Laboratory animals.

[12]  L. Romero,et al.  Stress: An inevitable component of animal translocation , 2010 .

[13]  M. Humphries,et al.  Fecal cortisol metabolite levels in free-ranging North American red squirrels: Assay validation and the effects of reproductive condition. , 2010, General and comparative endocrinology.

[14]  R. Palme,et al.  Sex differences in the excretion of fecal glucocorticoid metabolites in the Syrian hamster , 2010, Journal of Comparative Physiology B.

[15]  R. Palme,et al.  A non-invasive method for measuring glucocorticoid metabolites (GCM) in Mountain hares (Lepus timidus) , 2009, European Journal of Wildlife Research.

[16]  Joseph E LeDoux,et al.  The influence of stress hormones on fear circuitry. , 2009, Annual review of neuroscience.

[17]  L. Michael Romero,et al.  Stress and translocation: alterations in the stress physiology of translocated birds , 2009, Proceedings of the Royal Society B: Biological Sciences.

[18]  R. Boonstra,et al.  Assessment of the Stress Response in Columbian Ground Squirrels: Laboratory and Field Validation of an Enzyme Immunoassay for Fecal Cortisol Metabolites , 2009, Physiological and Biochemical Zoology.

[19]  Mollie E. Brooks,et al.  Generalized linear mixed models: a practical guide for ecology and evolution. , 2009, Trends in ecology & evolution.

[20]  C. Krebs,et al.  A non-invasive technique for analyzing fecal cortisol metabolites in snowshoe hares (Lepus americanus) , 2009, Journal of Comparative Physiology B.

[21]  R. Sanderson,et al.  Predicting the spread of the American grey squirrel (Sciurus carolinensis) in Europe: A call for a co-ordinated European approach , 2008 .

[22]  D. Rubenstein,et al.  Fecal glucocorticoid metabolite analysis as an indicator of stress during translocation and acclimation in an endangered large mammal, the Grevy's zebra , 2008 .

[23]  F. Palomares,et al.  Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits , 2008, Oecologia.

[24]  R. Palme,et al.  Non-invasive measurement of adrenocortical activity in male and female rats , 2007, Laboratory animals.

[25]  R. Sikes,et al.  Guidelines of the American Society of Mammalogists for the Use of Wild Mammals in Research , 2007 .

[26]  M. Mendl,et al.  Revisiting translocation and reintroduction programmes: the importance of considering stress , 2007, Animal Behaviour.

[27]  D. Preatoni,et al.  Modelling the Expansion of a Grey Squirrel population: Implications for Squirrel Control , 2006, Biological Invasions.

[28]  Heiko G. Rödel,et al.  Non-invasive measurement of the physiological stress response of wild rabbits to the odour of a predator , 2006, CHEMOECOLOGY.

[29]  R. Palme,et al.  Measuring Fecal Glucocorticoid Metabolites in Mammals and Birds: The Importance of Validation , 2005, Annals of the New York Academy of Sciences.

[30]  D. Reeder,et al.  STRESS IN FREE-RANGING MAMMALS: INTEGRATING PHYSIOLOGY, ECOLOGY, AND NATURAL HISTORY , 2005 .

[31]  R. Palme,et al.  Stress Hormones in Mammals and Birds: Comparative Aspects Regarding Metabolism, Excretion, and Noninvasive Measurement in Fecal Samples , 2005, Annals of the New York Academy of Sciences.

[32]  G. H. Olsen,et al.  Fecal corticoid monitoring in whooping cranes (Grus americana) undergoing reintroduction , 2005 .

[33]  C. Calvete,et al.  Short-term survival and dispersal of translocated European wild rabbits. Improving the release protocol , 2004 .

[34]  L. Adams,et al.  Movement and mortality of translocated urban-suburban grey squirrels , 2004, Animal Welfare.

[35]  S. Lowe,et al.  100 of the world's worst invasive alien species. A selection from the global invasive species database , 2004 .

[36]  P. Genovesi,et al.  Spread and attempted eradication of the grey squirrel (Sciurus carolinensis) in Italy, and consequences for the red squirrel (Sciurus vulgaris) in Eurasia , 2003 .

[37]  R. Palme,et al.  Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. , 2003, General and comparative endocrinology.

[38]  L. Romero Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. , 2002, General and comparative endocrinology.

[39]  R. Sapolsky Endocrinology of the stress-response. , 2002 .

[40]  David B. Lindenmayer,et al.  An assessment of the published results of animal relocations , 2000 .

[41]  S. Murphy,et al.  Comparative Morphology of the Gastrointestinal Tract in the Feeding Specialist Sciurus aberti and Several Generalist Congeners , 1999 .

[42]  R. Kenward,et al.  Red squirrels ( Sciurus vulgaris ) released in conifer woodland: the effects of source habitat, predation and interactions with grey squirrels ( Sciurus carolinensis ) , 1998 .

[43]  R. Dantzer,et al.  Stress in farm animals: a need for reevaluation. , 1983, Journal of animal science.

[44]  M. K. Younoszai,et al.  Dietary components and gastrointestinal growth in rats. , 1978, The Journal of nutrition.

[45]  C. J. Cowles,et al.  Characteristics of Captive Gray Squirrels Exposed to Cold and Food Deprivation , 1978 .

[46]  H. G. Lloyd,et al.  Movements of the Grey Squirrel as Revealed by Trapping , 1971 .

[47]  P. Siegel,et al.  Influence of Social Hierarchy on Gray Squirrel Behavior , 1967 .

[48]  J. C. Osborne,et al.  Physiological Changes Associated with Shock in Confined Gray Squirrels , 1967 .

[49]  K. E. Hungerford,et al.  Observations on the Homing Behavior of the Gray Squirrel (Sciurus carolinensis) , 1941 .