Abstract
Seasonally breeding mammals must make constant adjustments in behavior and physiology to manage energetic trade-offs between survival and reproduction. Despite encountering high levels of climate and resource variability across the year, specialist Abert’s squirrels (Sciurus aberti), lack the capacity to express hibernation or pronounced morphological adaptations to seasonality. Using accelerometer and GPS devices, we assessed how abiotic environmental factors, reproduction, and resource abundance influenced levels of activity and daily range size in a rural and food-supplemented suburban population of squirrels. We also quantified fecal cortisol metabolites (FCM) in squirrels to assess patterns of glucocorticoid secretion. While changes in weather predicted activity levels in both populations, seasonal variation in activity levels were reduced in food-supplemented compared to rural squirrels. In contrast to activity, daily range size was not affected by weather but was a better predictor of sex-specific reproductive investment. Comparisons between populations suggest that food-supplemented squirrels forage more efficiently within smaller areas. Across both sexes and populations, squirrels showed no sexual dimorphism in body size, no major patterns of seasonal weight change, and no associations between body mass and FCM concentrations; however, FCMs were lower in the food-supplemented compared to rural population during late-spring. Taken together, activity levels and FCM concentrations appear primarily influenced by weather and seasonal fluctuations in food availability, whereas daily range size reflects sexual asymmetries in seasonal reproductive investment. Overall, squirrels appear to rely largely on behavioral adjustments to cope with novel environmental heterogeneity, rather than changes in morphology or GC secretion.
Similar content being viewed by others
Availability of data and material
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Allred S, Pogany G (1996) Early estrus in a female Abert squirrel (Sciurus aberti aberti). Southwest Nat 41:90–91
Angelier F, Clément-Chastel C, Gabrielsen GW, Chastel O (2007) Corticosterone and time-activity budget: an experiment with Black-legged kittiwakes. Horm Behav 52:482–491. https://doi.org/10.1016/j.yhbeh.2007.07.003
Angelier F, Clément-Chastel C, Welcker J et al (2009) How does corticosterone affect parental behaviour and reproductive success? A study of prolactin in black-legged kittiwakes. Funct Ecol 23:784–793. https://doi.org/10.1111/j.1365-2435.2009.01545.x
Astheimer LB, Buttemer WA, Wingfield JC (1992) Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scandin (scandin J Ornithol) 23:355–365. https://doi.org/10.2307/3676661
Beck CA, Bowen WD, Iverson SJ (2003) Sex differences in the seasonal patterns of energy storage and expenditure in a phocid seal. J Anim Ecol 72:280–291. https://doi.org/10.1046/j.1365-2656.2003.00704.x
Beehner JC, McCann C (2008) Seasonal and altitudinal effects on glucocorticoid metabolites in a wild primate (Theropithecus gelada). Physiol Behav 95:508–514. https://doi.org/10.1016/j.physbeh.2008.07.022
Boonstra R, Hik D, Singleton GR, Tinnikov A (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecol Monogr 68:371–394. https://doi.org/10.1890/0012-9615(1998)068[0371:TIOPIS]2.0.CO;2
Boswell T, Woods SC, Kenagy GJ (1994) Seasonal changes in body mass, insulin, and glucocorticoids of free-living golden-mantled ground squirrels. Gen Comp Endocrinol 96:339–346. https://doi.org/10.1006/gcen.1994.1189
Boutin S (1990) Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Can J Zool 68:203–220. https://doi.org/10.1139/z90-031
Breuner CW, Hahn TP (2003) Integrating stress physiology, environmental change, and behavior in free-living sparrows. Horm Behav 43:115–123. https://doi.org/10.1016/S0018-506X(02)00020-X
Brewer JH, O’Reilly KM, Buck CL (2008a) Effects of investigator disturbance on corticosterone concentrations of Black-legged Kittiwake chicks. J Field Ornithol 79:391–398. https://doi.org/10.1111/j.1557-9263.2008.00187.x
Brewer JH, O’Reilly KM, Dean Kildaw S, Loren Buck C (2008b) Interannual variation in the adrenal responsiveness of black-legged kittiwake chicks (Rissa tridactyla). Gen Comp Endocrinol 156:361–368. https://doi.org/10.1016/j.ygcen.2008.01.010
Buck CL, Barnes BM (1999) Annual cycle of body composition and hibernation in free-living arctic ground squirrels. J Mammal 80:430–442. https://doi.org/10.2307/1383291
Buck CL, Barnes BM (2000) Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. Am J Physiol Regul Integ Compar Physiol 279:R255–R262. https://doi.org/10.1152/ajpregu.2000.279.1.R255
Buck CL, Barnes BM (2003) Androgen in free-living arctic ground squirrels: seasonal changes and influence of staged male-male aggressive encounters. Horm Behav 43:318–326. https://doi.org/10.1016/S0018-506X(02)00050-8
Buck CL, O’Reilly KM, Kildaw SD (2007) Interannual variability of Black-legged Kittiwake productivity is reflected in baseline plasma corticosterone. Gen Comp Endocrinol 150:430–436. https://doi.org/10.1016/j.ygcen.2006.10.011
Calenge C (2019) Home range estimation in R: the adehabitatHR package. Office national de la classe et de la faune sauvage: Saint Benoist, Auffargis, France
Cash WB, Holberton RL (1999) Effects of exogenous corticosterone on locomotor activity in the red-eared slider turtle, Trachemys scripta elegans. J Exp Zool 284:637–644. https://doi.org/10.1002/(SICI)1097-010X(19991101)284:6%3c637::AID-JEZ5%3e3.0.CO;2-N
Chmura HE, Zhang VY, Wilbur SM et al (2020) Plasticity and repeatability of activity patterns in free-living Arctic ground squirrels. Anim Behav 169:81–91. https://doi.org/10.1016/j.anbehav.2020.09.007
Collin A, van Milgent J, Dividich JL (2001) Modelling the effect of high, constant temperature on food intake in young growing pigs. Anim Sci 72:519–527. https://doi.org/10.1017/S1357729800052048
Cork SJ, Kenagy GJ (1989) Nutritional value of hypogeous fungus for a forest-dwelling ground squirrel. Ecology 70:577–586. https://doi.org/10.2307/1940209
Corlatti L, Palme R, Frey-Roos F, Hackländer K (2011) Climatic cues and glucocorticoids in a free-ranging riparian population of red deer (Cervus elaphus). J Vertebrate Biol 60:176–180
Cox RM, Parker EU, Cheney DM et al (2010) Experimental evidence for physiological costs underlying the trade-off between reproduction and survival: Physiological costs of reproduction. Funct Ecol 24:1262–1269. https://doi.org/10.1111/j.1365-2435.2010.01756.x
Crespi EJ, Williams TD, Jessop TS, Delehanty B (2013) Life history and the ecology of stress: how do glucocorticoid hormones influence life-history variation in animals? Funct Ecol 27:93–106. https://doi.org/10.1111/1365-2435.12009
Dallman MF, Strack AM, Akana SF et al (1993) Feast and Famine: Critical Role of Glucocorticoids with Insulin in Daily Energy Flow. Front Neuroendocrinol 14:303–347. https://doi.org/10.1006/frne.1993.1010
Dallman MF, la Fleur SE, Pecoraro NC et al (2004) Minireview: glucocorticoids—food intake, abdominal obesity, and wealthy nations in 2004. Endocrinology 145:2633–2638
Dantzer B, McAdam AG, Palme R et al (2010) Fecal cortisol metabolite levels in free-ranging North American red squirrels: Assay validation and the effects of reproductive condition. Gen Comp Endocrinol 167:279–286. https://doi.org/10.1016/j.ygcen.2010.03.024
Dantzer B, Santicchia F, van Kesteren F et al (2016) Measurement of fecal glucocorticoid metabolite levels in Eurasian red squirrels ( Sciurus vulgaris ): effects of captivity, sex, reproductive condition, and season. JMAMMAL 97:1385–1398. https://doi.org/10.1093/jmammal/gyw095
Dausmann KH, Wein J, Turner JM, Glos J (2013) Absence of heterothermy in the European red squirrel (Sciurus vulgaris). Mamm Biol 78:332–335. https://doi.org/10.1016/j.mambio.2013.01.004
de Bruijn R, Romero LM (2018) The role of glucocorticoids in the vertebrate response to weather. Gen Comp Endocrinol 269:11–32. https://doi.org/10.1016/j.ygcen.2018.07.007
Dodd NL, States JS, Rosenstock SS (2003) Tassel-eared squirrel population, habitat condition, and dietary relationships in north-central arizona. J Wildl Manag 67:622. https://doi.org/10.2307/3802719
Dunn PO, Whittingham LA, Pitcher TE (2001) Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution 55:161–175. https://doi.org/10.1111/j.0014-3820.2001.tb01281.x
Edelman AJ, Koprowski JL (2006) Seasonal changes in home ranges of Abert’s squirrels: impact of mating season. Can J Zool 84:404–411. https://doi.org/10.1139/z06-009
Eleftheriou A, Palme R, Boonstra R (2020) Assessment of the stress response in north american deermice: laboratory and field validation of two enzyme immunoassays for fecal corticosterone metabolites. Animals 10:1120. https://doi.org/10.3390/ani10071120
Farentinos RC (1972a) Social dominance and mating activity in the tassel-eared squirrel (Sciurus aberti ferreus). Anim Behav 20:316–326. https://doi.org/10.1016/S0003-3472(72)80053-8
Farentinos RC (1972b) Observations on the Ecology of the Tassel-Eared Squirrel. J Wildl Manag 36:1234. https://doi.org/10.2307/3799253
Farentinos RC (1979) Seasonal changes in home range size of tassel-eared squirrels (Sciurus aberti). Southwest Nat 24:49. https://doi.org/10.2307/3670624
Fauteux D, Gauthier G, Berteaux D et al (2018) High Arctic lemmings remain reproductively active under predator-induced elevated stress. Oecologia 187:657–666. https://doi.org/10.1007/s00442-018-4140-4
Fernández Ajó AA, Hunt KE, Giese AC et al (2020) Retrospective analysis of the lifetime endocrine response of southern right whale calves to gull wounding and harassment: A baleen hormone approach. Gen Comp Endocrinol 296:113536. https://doi.org/10.1016/j.ygcen.2020.113536
Fletcher QE, Speakman JR, Boutin S et al (2012) Seasonal stage differences overwhelm environmental and individual factors as determinants of energy expenditure in free-ranging red squirrels: Cost of living in wild squirrels. Funct Ecol 26:677–687. https://doi.org/10.1111/j.1365-2435.2012.01975.x
Fokidis HB, Hurley L, Rogowski C et al (2011) Effects of captivity and body condition on plasma corticosterone, locomotor behavior, and plasma metabolites in curve-billed thrashers. Physiol Biochem Zool 84:595–606
Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274. https://doi.org/10.1146/annurev.physiol.66.032102.115105
Gilbert C, McCafferty D, Maho YL et al (2010) One for all and all for one: the energetic benefits of huddling in endotherms. Biol Rev 85:545–569. https://doi.org/10.1111/j.1469-185X.2009.00115.x
Gittleman JL, Thompson SD (1988) Energy allocation in mammalian reproduction. Am Zool 28:863–875. https://doi.org/10.1093/icb/28.3.863
Golightly RT, Ohmart RD (1978) Heterothermy in free-ranging abert’s squirrels (Sciurus Aberti). Ecology 59:897–909. https://doi.org/10.2307/1938542
Grotjan HE, Keel BA (1996) Data interpretation and quality control. In: Diamandis EP, Christopoulos TK (eds) Immunoassay. Academic Press, Dan Diego, CA, pp 51–95
Halloran ME, Bekoff M (2000) Home range use by abert squirrels: a comparative analysis. Southwest Nat 45:253. https://doi.org/10.2307/3672827
Halsey LG, Green JA, Wilson RP, Frappell PB (2009a) Accelerometry to estimate energy expenditure during activity: best practice with data loggers. Physiol Biochem Zool 82:396–404. https://doi.org/10.1086/589815
Halsey LG, Shepard ELC, Quintana F et al (2009b) The relationship between oxygen consumption and body acceleration in a range of species. Comp Biochem Physiol a: Mol Integr Physiol 152:197–202. https://doi.org/10.1016/j.cbpa.2008.09.021
Hamilton CL (1963) Interactions of food intake and temperature regulation in the rat. J Comp Physiol Psychol 56:476–488. https://doi.org/10.1037/h0046241
Harper JM, Austad SN (2001) Effect of capture and season on fecal glucocorticoid levels in deer mice (Peromyscus maniculatus) and red-backed voles (Clethrionomys gapperi). Gen Comp Endocrinol 123:337–344. https://doi.org/10.1006/gcen.2001.7682
Harshman LG, Zera AJ (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22:80–86. https://doi.org/10.1016/j.tree.2006.10.008
Hau M, Dominoni D, Casagrande S et al (2017) Timing as a sexually selected trait: the right mate at the right moment. Phil Trans R Soc B 372:20160249. https://doi.org/10.1098/rstb.2016.0249
Hayssen V, Lacy RC (1985) Basal metabolic rates in mammals: taxonomic differences in the allometry of BMR and body mass. Comp Biochem Physiol A Comp Physiol 81:741–754. https://doi.org/10.1016/0300-9629(85)90904-1
Healy JE, Burdett KA, Buck CL, Florant GL (2012) Sex differences in torpor patterns during natural hibernation in golden-mantled ground squirrels ( Callospermophilus lateralis ). J Mammal 93:751–758. https://doi.org/10.1644/11-MAMM-A-120.1
Heldmaier G, Steinlechner S, Ruf T et al (1989) Photoperiod and thermoregulation in vertebrates: body temperature rhythms and thermogenic acclimation. J Biol Rhythms 4:251–265
Heldmaier G, Klaus S, Wiesinger H (1990) Seasonal Adaptation of Thermoregulatory Heat Production in Small Mammals. In: Bligh J, Voigt K, Braun HA et al (eds) Thermoreception and Temperature Regulation. Springer, Berlin, Heidelberg, pp 235–243
Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Respir Physiol Neurobiol 141:317–329. https://doi.org/10.1016/j.resp.2004.03.014
Hennin HL, Wells-Berlin AM, Love OP (2016) Baseline glucocorticoids are drivers of body mass gain in a diving seabird. Ecol Evol 6:1702–1711
Henry M, Thomas DW, Vaudry R, Carrier M (2002) Foraging distances and home range of pregnant and lactating little brown bats (Myotis lucifugus). J Mammal 83:8
Hubbs AH, Boonstra R (1998) Effects of food and predators on the home-range sizes of Arctic ground squirrels (Spermophilus parryii). Can J Zool 76:592–596
Ironside KE, Mattson DJ, Arundel TR, Hansen JR (2017) Is GPS telemetry location error screening beneficial? Wildl Biol. https://doi.org/10.2981/wlb.00229
Johnson DDP, Kays R, Blackwell PG, Macdonald DW (2002) Does the resource dispersion hypothesis explain group living? Trends Ecol Evol 17:563–570. https://doi.org/10.1016/S0169-5347(02)02619-8
Kauffman AS, Cabrera A, Zucker I (2001) Energy intake and fur in summer- and winter-acclimated Siberian hamsters (Phodopus sungorus). Am J Physiol Regul Integr Comp Physiol 281:R519-527. https://doi.org/10.1152/ajpregu.2001.281.2.R519
Keith JO (1965) The abert squirrel and its dependence on ponderosa pine. Ecology 46:150–163. https://doi.org/10.2307/1935266
Keith JO (1956) The Abert squirrel (Sciurus aberti aberti) and its relationship to the forests of Arizona
Kenagy GJ, Place NJ (2000) Seasonal changes in plasma glucocorticosteroids of free-living female yellow-pine chipmunks: effects of reproduction and capture and handling. Gen Comp Endocrinol 117:189–199. https://doi.org/10.1006/gcen.1999.7397
Kenagy GJ, Sharbaugh SM, Nagy KA (1989a) Annual cycle of energy and time expenditure in a golden-mantled ground squirrel population. Oecologia 78:269–282
Kenagy GJ, Stevenson RD, Masman D (1989b) Energy requirements for lactation and postnatal growth in captive golden-mantled ground squirrels. Physiol Zool 62:470–487
Khonmee J, Vorawattanatham N, Pinyopummin A et al (2016) Assessment of faecal glucocorticoid metabolite excretion in captive female fishing cats (Prionailurus viverinus) in Thailand. Conserv Physiol. https://doi.org/10.1093/conphys/cow021
Kitaysky AS, Wingfield JC, Piatt JF (1999) Dynamics of food availability, body condition and physiological stress response in breeding Black-legged Kittiwakes. Funct Ecol 13:577–584. https://doi.org/10.1046/j.1365-2435.1999.00352.x
Klenner W, Krebs CJ (1991) Red squirrel population dynamics i. the effect of supplemental food on demography. J Anim Ecol 60:961–978. https://doi.org/10.2307/5425
Koch KA, Wingfield JC, Buntin JD (2002) Glucocorticoids and parental hyperphagia in ring doves (Streptopelia risoria). Horm Behav 41:9–21
Landys MM, Ramenofsky M, Wingfield JC (2006) Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen Comp Endocrinol 148:132–149. https://doi.org/10.1016/j.ygcen.2006.02.013
Lane JE, Boutin S, Speakman JR, Humphries MM (2010) Energetic costs of male reproduction in a scramble competition mating system. J Anim Ecol 79:27–34. https://doi.org/10.1111/j.1365-2656.2009.01592.x
Lepschy M, Touma C, Hruby R, Palme R (2007) Non-invasive measurement of adrenocortical activity in male and female rats. Lab Anim 41:372–387. https://doi.org/10.1258/002367707781282730
Lewis JS, Rachlow JL, Garton EO, Vierling LA (2007) Effects of habitat on GPS collar performance: using data screening to reduce location error: GPS collar performance. J Appl Ecol 44:663–671. https://doi.org/10.1111/j.1365-2664.2007.01286.x
Logan M, Sanson GD (2003) The effects of lactation on the feeding behaviour and activity patterns of free-ranging female koalas (Phascolarctos cinereus Goldfuss). Aust J Zool 51:415–428
Mateo JM, Cavigelli SA (2005) A Validation of extraction methods for noninvasive sampling of glucocorticoids in free-living ground squirrels. Physiol Biochem Zool 78:1069–1084. https://doi.org/10.1086/432855
McClintic LF, Taylor JD, Jones JC et al (2014) Effects of spatiotemporal resource heterogeneity on home range size of American beaver. J Zool 293:134–141. https://doi.org/10.1111/jzo.12128
McEwen BS, Wingfield JC (2010) What is in a name? Integrating homeostasis, allostasis and stress. Horm Behav 57:105–111. https://doi.org/10.1016/j.yhbeh.2009.09.011
Michel CL, Chastel O, Bonnet X (2011) Ambient temperature and pregnancy influence cortisol levels in female guinea pigs and entail long-term effects on the stress response of their offspring. Gen Comp Endocrinol 171:275–282. https://doi.org/10.1016/j.ygcen.2011.02.007
Millesi E, Huber S, Dittami J et al (1998) Parameters of mating effort and success in male european ground squirrels, Spermophilus citellus. Ethology 104:298–313. https://doi.org/10.1111/j.1439-0310.1998.tb00070.x
Monsarrat S, Benhamou S, Sarrazin F et al (2013) How predictability of feeding patches affects home range and foraging habitat selection in avian social scavengers? PLoS ONE 8:e53077. https://doi.org/10.1371/journal.pone.0053077
Montiglio P-O, Pelletier F, Palme R et al (2012) Noninvasive monitoring of fecal cortisol metabolites in the eastern chipmunk ( Tamias striatus ): validation and comparison of two enzyme immunoassays. Physiol Biochem Zool 85:183–193. https://doi.org/10.1086/664592
Murphy SM, Linhart YB (1999) Comparative morphology of the gastrointestinal tract in the feeding specialist sciurus aberti and several generalist congeners. J Mammal 80:1325–1330. https://doi.org/10.2307/1383182
Nash DJ, Seaman RN (1977) Sciurus aberti. Mammalian Species 1–5
Nunes S, Pelz KM, Muecke E-M et al (2006) Plasma glucocorticoid concentrations and body mass in ground squirrels: Seasonal variation and circannual organization. Gen Comp Endocrinol 146:136–143. https://doi.org/10.1016/j.ygcen.2005.10.013
Palme R (2019) Non-invasive measurement of glucocorticoids: Advances and problems. Physiol Behav 199:229–243. https://doi.org/10.1016/j.physbeh.2018.11.021
Patton DR, Hudak HG, Ratcliff TD (1976) Trapping, anesthetizing, and marking the Abert squirrel. US Department of Agriculture, Forest Service, Rocky Mountain Forest and
Paul MJ, Tuthill C, Kauffman AS, Zucker I (2010) Pelage insulation, litter size, and ambient temperature impact maternal energy intake and offspring development during lactation. Physiol Behav 100:128–134. https://doi.org/10.1016/j.physbeh.2010.02.012
Pederson JC, Farentinos RC, Littlefield VM (1987) Effects of logging on habitat quality and feeding patterns of Abert squirrels. Great Basin Natural 47:252–258
Pereira ME, Aines J, Scheckter JL (2002) Tactics of heterothermy in eastern gray squirrels (Sciurus Carolinensis). J Mammal 83:467–477. https://doi.org/10.1644/1545-1542(2002)083%3c0467:TOHIEG%3e2.0.CO;2
Pérez-Barbería FJ, Gordon IJ, Pagel M (2002) The origins of sexual dimorphism in body size in ungulates. Evolution 56:1276–1285. https://doi.org/10.1111/j.0014-3820.2002.tb01438.x
Piersma T, van Gils JA (2011) The flexible phenotype: a body-centred integration of ecology, physiology, and behaviour. Oxford University Press, Oxford
Pond CM (1978) Morphological aspects and the ecological and mechanical consequences of fat deposition in wild vertebrates. Annu Rev Ecol Syst 9:519–570. https://doi.org/10.1146/annurev.es.09.110178.002511
Powell RA, Leonard RD (1983) Sexual dimorphism and energy expenditure for reproduction in female fisher martes pennanti. Oikos 40:166. https://doi.org/10.2307/3544579
Reed A, Pigage JC, Pigage HK et al (2019) Comparative analysis of microbiota along the length of the gastrointestinal tract of two tree squirrel species (Sciurus aberti and S. niger) living in sympatry. Ecol Evol 9:13344–13358. https://doi.org/10.1002/ece3.5789
Reynolds JC (1985) Autumn-winter energetics of Holarctic tree squirrels:a review. Mammal Rev 15:137–150. https://doi.org/10.1111/j.1365-2907.1985.tb00395.x
Richter MM, Barnes BM, O’Reilly KM et al (2017) The influence of androgens on hibernation phenology of free-living male arctic ground squirrels. Horm Behav 89:92–97. https://doi.org/10.1016/j.yhbeh.2016.12.007
Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24. https://doi.org/10.1016/S0016-6480(02)00064-3
Romero LM, Wikelski M (2001) Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proc Natl Acad Sci 98:7366–7370. https://doi.org/10.1073/pnas.131091498
Romero LM, Wingfield JC (2016) Tempests, poxes, predators, and people: stress in wild animals and how they cope. Oxford University Press, New York
Romero LM, Meister CJ, Cyr NE et al (2008) Seasonal glucocorticoid responses to capture in wild free-living mammals. Am J Physiol Regul Integrat Compar Physiol 294:R614–R622. https://doi.org/10.1152/ajpregu.00752.2007
Sandi C, Venero C, Guaza C (1996) Novelty-related rapid locomotor effects of corticosterone in rats. Eur J Neurosci 8:794–800. https://doi.org/10.1111/j.1460-9568.1996.tb01264.x
Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses, Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Rev 21:35
Scantlebury M, Bennett NC, Speakman JR et al (2006a) Huddling in groups leads to daily energy savings in free-living African Four-Striped Grass Mice, Rhabdomys pumilio. Funct Ecol 20:166–173. https://doi.org/10.1111/j.1365-2435.2006.01074.x
Scantlebury M, Speakman JR, Bennett NC (2006b) The energy costs of sexual dimorphism in mole-rats are morphological not behavioural. Proc Royal Soc B Biol Sci 273:57–63. https://doi.org/10.1098/rspb.2005.3280
Shepard E, Wilson R, Halsey L et al (2008) Derivation of body motion via appropriate smoothing of acceleration data. Aquat Biol 4:235–241. https://doi.org/10.3354/ab00104
Sheriff MJ, Kenagy GJ, Richter M et al (2011) Phenological variation in annual timing of hibernation and breeding in nearby populations of Arctic ground squirrels. Proc R Soc B 278:2369–2375. https://doi.org/10.1098/rspb.2010.2482
Sheriff MJ, Wheeler H, Donker SA et al (2012) Mountain-top and valley-bottom experiences: the stress axis as an integrator of environmental variability in arctic ground squirrel populations: Life on a mountainside: coping with environmental variation. J Zool 287:65–75. https://doi.org/10.1111/j.1469-7998.2011.00888.x
Snyder MA (1992) Selective herbivory by abert’s squirrel mediated by chemical variability in ponderosa pine. Ecology 73:1730–1741. https://doi.org/10.2307/1940025
States JS, Wettstein PJ (1998) Food habits and evolutionary relationships of the tasseleared squirrel (Sciurus aberti). Virginia Museum of Natural History Martinsville, VA
States JS, Gaud WS, Allred WS, Austin WJ (1988) Foraging patterns of tassel-eared squirrels of selected ponderosa pine stands. General technical report RM-Rocky Mountain Forest and Range Experiment Station, US Department of Agriculture, Forest Service (USA)
States JS, Gaud WS (1997) Ecology of hypogeous fungi associated with ponderosa pine. I. Patterns of distribution and sporocarp production in some Arizona forests. Mycologia 89:712–721. https://doi.org/10.1080/00275514.1997.12026837
Stearns SC (1992) The Evolution of Life Histories. Oxford University Press, Oxford, New York
Stephenson RL (1975) Reproductive biology and food habits of Abert’s squirrels in central Arizona. PhD Thesis, Arizona State University
Strauss A, Mascher E, Palme R, Millesi E (2007) Sexually mature and immature yearling male European ground squirrels: A comparison of behavioral and physiological parameters. Horm Behav 52:646–652. https://doi.org/10.1016/j.yhbeh.2007.08.003
Studd EK, Menzies AK, Siracusa ER et al (2020) Optimisation of energetic and reproductive gains explains behavioural responses to environmental variation across seasons and years. Ecol Lett 23:841–850. https://doi.org/10.1111/ele.13494
Trombulak SC (1989) Running speed and body mass in Belding’s ground squirrels. J Mammal 70:194–197
Turner JM, Reher S, Warnecke L, Dausmann KH (2017) Eurasian red squirrels show little seasonal variation in metabolism in food-enriched habitat. Physiol Biochem Zool 90:655–662. https://doi.org/10.1086/694847
Vitousek MN, Jenkins BR, Safran RJ (2014) Stress and success: Individual differences in the glucocorticoid stress response predict behavior and reproductive success under high predation risk. Horm Behav 66:812–819. https://doi.org/10.1016/j.yhbeh.2014.11.004
Weingrill T, Gray DA, Barrett L, Henzi SP (2004) Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors. Horm Behav 45:259–269. https://doi.org/10.1016/j.yhbeh.2003.12.004
West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278
White CR, Seymour RS (2004) Does basal metabolic rate contain a useful signal? mammalian BMR allometry and correlations with a selection of physiological, ecological, and life-history variables. Physiol Biochem Zool 77:929–941. https://doi.org/10.1086/425186
Williams CT, Wilsterman K, Zhang V et al (2016) The secret life of ground squirrels: accelerometry reveals sex-dependent plasticity in above-ground activity. R Soc Open Sci 3:160404. https://doi.org/10.1098/rsos.160404
Williams CT, Buck CL, Sheriff MJ et al (2017a) Sex-dependent phenological plasticity in an arctic hibernator. Am Nat 190:854–859. https://doi.org/10.1086/694320
Williams CT, Klaassen M, Barnes BM et al (2017b) Seasonal reproductive tactics: annual timing and the capital-to-income breeder continuum. Phil Trans R Soc B 372:20160250. https://doi.org/10.1098/rstb.2016.0250
Wilson RP, White CR, Quintana F et al (2006) Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant: Activity-specific metabolic rate in free-living animals. J Anim Ecol 75:1081–1090. https://doi.org/10.1111/j.1365-2656.2006.01127.x
Wingfield JC (2005) The concept of allostasis: coping with a capricious environment. J Mammal 86:248–254. https://doi.org/10.1644/BHE-004.1
Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how: reproduction and resistance to stress. J Neuroendocrinol 15:711–724. https://doi.org/10.1046/j.1365-2826.2003.01033.x
Wingfield JC, Maney DL, Breuner CW et al (1998) Ecological bases of hormone—behavior interactions: the “emergency life history stage.” Am Zool 38:191–206. https://doi.org/10.1093/icb/38.1.191
Wolff JO, Sherman PW (2007) Rodent Societies: An Ecological and Evolutionary Perspective. University of Chicago Press, Chicago, USA
Wood SN (2017) Generalized additive models: an introduction with R, 2nd edn. CRC Press/Taylor & Francis Group, Boca Raton
Wright TF, Eberhard JR, Hobson EA et al (2010) Behavioral flexibility and species invasions: the adaptive flexibility hypothesis. Ethol Ecol Evol 22:393–404. https://doi.org/10.1080/03949370.2010.505580
Young RA (1976) Fat, Energy and Mammalian Survival. Am Zool 16:699–710. https://doi.org/10.1093/icb/16.4.699
Zhang VY, Williams CT, Theimer TC, Buck CL (2019) Reproductive and environmental drivers of time and activity budgets of striped skunks. Integrat Organ Biol. https://doi.org/10.1093/iob/obz013
Zhang VY, Williams CT, Palme R, Buck CL (2020) Glucocorticoids and activity in free-living arctic ground squirrels: Interrelationships between weather, body condition, and reproduction. Horm Behav 125:104818
Acknowledgements
We thank Danielle Dillon for her assistance in the lab and Noa Vallance, Harvey Castillo, David Lugo, Reid Cooper, and George Magula for their help in the field. We are grateful to John Fagan for granting access to his property to conduct this study.
Funding
Research reported in this publication was supported by grants from the National Science Foundation (NSF) to C. Loren Buck (IOS-1558056) and from the Arizona Board of Regents Technology Research Initiative Fund, administered by Northern Arizona University.
Author information
Authors and Affiliations
Contributions
VYZ and CLB contributed to the development of the concept. VYZ captured animals, collected field data, analyzed data, drafted figures, and wrote the initial manuscript with input from CLB. All authors contributed to revisions of the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare no competing interests.
Ethics approval
This study was conducted as per guidelines of the Northern Arizona University International Animal Care and Use Committee (IACUC no. 17–014). Work at our study sites were permitted by the Arizona Game and Fish Department (Scientific Collecting License #SP615275).
Additional information
Communicated by K.H. Dausmann.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, V.Y., Buck, C.L. Seasonal patterns in behavior and glucocorticoid secretion of a specialist Holarctic tree squirrel (Sciurus aberti). J Comp Physiol B 192, 541–559 (2022). https://doi.org/10.1007/s00360-022-01429-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-022-01429-6