Heterothermy as a mechanism to offset energetic costs of environmental and homeostatic perturbations
1.Wingfield, J. C., Vleck, C. M. & Moore, M. C. Seasonal changes of the adrenocortical response to stress in birds of the Sonoran Desert. J. Exp. Zool. 264, 419–428 (1992).CAS
PubMed
Article
Google Scholar
2.Boonstra, R. Coping with changing northern environments: The role of the stress axis in birds and mammals. Integr. Comp. Biol. 44, 95–108 (2004).PubMed
Article
Google Scholar
3.Lind, J. & Cresswell, W. Determining the fitness consequences of antipredation behavior. Behav. Ecol. 16, 945–956 (2005).Article
Google Scholar
4.Boyles, J. G., Smit, B. & McKechnie, A. E. A new comparative metric for estimating heterothermy in endotherms. Physiol. Biochem. Zool. 84, 115–123 (2011).PubMed
Article
Google Scholar
5.Boyles, J. G. et al. A global heterothermic continuum in mammals. Glob. Ecol. Biogeogr. 22, 1029–1039 (2013).Article
Google Scholar
6.Canale, C. I., Levesque, D. L. & Lovegrove, B. G. Tropical heterothermy: Does the exception prove the rule or force a re-definition? In Living in a Seasonal World: Thermoregulatory and Metabolic adaptations (eds Ruf, T. et al.) 29–40 (Springer, Berlin, 2012).Chapter
Google Scholar
7.Dammhahn, M., Landry-Cuerrier, M., Réale, D., Garant, D. & Humphries, M. M. Individual variation in energy-saving heterothermy affects survival and reproductive success. Funct. Ecol. 31, 866–875 (2017).Article
Google Scholar
8.McGuire, L. P., Jonasson, K. A. & Guglielmo, C. G. Bats on a budget: Torpor-assisted migration saves time and energy. PLoS ONE 9, e115724 (2014).ADS
PubMed
PubMed Central
Article
CAS
Google Scholar
9.Glazier, D. S. Metabolic level and size scaling of rates of respiration and growth in unicellular organisms. Funct. Ecol. 23, 963–968 (2009).Article
Google Scholar
10.Turbill, C. & Stojanovski, L. Torpor reduces predation risk by compensating for the energetic cost of antipredator foraging behaviours. Proc. R. Soc. B Biol. Sci. 285, 1–9 (2018).
Google Scholar
11.Angilletta, M. J., Cooper, B. S., Schuler, M. S. & Boyles, J. G. The evolution of thermal physiology in endotherms. Front. Biosci. 2, 861–881 (2010).
Google Scholar
12.Angilletta, M. J. Thermal Adaptation: A Theoretical and Empirical Synthesis (Oxford University Press, Oxford, 2009).Book
Google Scholar
13.Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).ADS
CAS
Article
Google Scholar
14.Menzies, A. K. et al. Body temperature, heart rate, and activity patterns of two boreal homeotherms in winter: Homeostasis, allostasis, and ecological coexistence. Funct. Ecol. 34, 2292–2301 (2020).Article
Google Scholar
15.Humphries, M. M. & Careau, V. Heat for nothing or activity for free? Evidence and implications of activity-thermoregulatory heat substitution. Integr. Comp. Biol. 51, 419–431 (2011).PubMed
Article
PubMed Central
Google Scholar
16.Daly, M., Behrends, P. R., Wilson, M. I. & Jacobs, L. F. Behavioural modulation of predation risk: Moonlight avoidance and crepuscular compensation in a nocturnal desert rodent, Dipodomys merriami. Anim. Behav. 44, 1–9 (1992).Article
Google Scholar
17.Price, M. V., Waser, N. M. & Bass, T. A. Effects of moonlight on microhabitat use by desert rodents. J. Mammal. 65, 353–356 (1984).Article
Google Scholar
18.Roschlau, C. & Scheibler, E. Foraging behaviour of a desert rodent community: Habitat or moon—Which is more influential?. Ethol. Ecol. Evol. 28, 394–413 (2016).Article
Google Scholar
19.Mandelik, Y., Jones, M. & Dayan, T. Structurally complex habitat and sensory adaptations mediate the behavioural responses of a desert rodent to an indirect cue for increased predation risk. Evol. Ecol. Res. 5, 501–515 (2003).
Google Scholar
20.Gutman, R., Dayan, T., Levy, O., Schubert, I. & Kronfeld-Schor, N. The effect of the lunar cycle on fecal cortisol metabolite levels and foraging ecology of nocturnally and diurnally active spiny mice. PLoS ONE 6, 35–38 (2011).Article
CAS
Google Scholar
21.Upham, N. S. & Hafner, J. C. Do nocturnal rodents in the great basin desert avoid moonlight?. J. Mammal. 94, 59–72 (2013).Article
Google Scholar
22.Price, M. V. Structure of desert rodent communities: A critical review of questions and approaches. Integr. Comp. Biol. 26, 39–49 (1986).
Google Scholar
23.Bennett, A. M. et al. Acute changes in whole body corticosterone in response to perceived predation risk: A mechanism for anti-predator behavior in anurans? Gen. Comp. Endocrinol. 229, 62–66 (2016).CAS
PubMed
Article
PubMed Central
Google Scholar
24.Hernández, M. C., Navarro-Castilla, Á., Planillo, A., Sánchez-González, B. & Barja, I. The landscape of fear: Why some free-ranging rodents choose repeated live-trapping over predation risk and how it is associated with the physiological stress response. Behav. Process. 157, 125–132 (2018).Article
Google Scholar
25.Thaker, M., Lima, S. L. & Hews, D. K. Acute corticosterone elevation enhances antipredator behaviors in male tree lizard morphs. Horm. Behav. 56, 51–57 (2009).CAS
PubMed
Article
PubMed Central
Google Scholar
26.Sapolsky, R. M., Romero, L. M. & Munck, A. U. How do glucocorticoids influence stress responses? Preparative actions. Endocr. Rev. 21, 55–89 (2000).CAS
PubMed
PubMed Central
Google Scholar
27.Mitra, R. & Sapolsky, R. M. Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc. Natl. Acad. Sci. 105, 5573–5578 (2008).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
28.Schroder, G. D. Foraging behavior and home range utilization of the bannertial kangaroo rat (Dipodomys spectabilis). Ecology 60, 657–665 (1979).ADS
Article
Google Scholar
29.Andersen, M. C. & Kay, F. R. Banner-tailed kangaroo rat burrow mounds and desert grassland habitats. J. Arid Environ. 41, 147–160 (1999).ADS
Article
Google Scholar
30.Harris, J. H. An experimental analysis of desert rodent foraging ecology. Ecology 65, 1579–1584 (1984).Article
Google Scholar
31.Lockard, R. B. Seasonal change in the activity pattern of Dipodomys spectabilis. J. Mammal. 59, 563–568 (1978).Article
Google Scholar
32.Lockard, R. B. & Owings, D. H. Seasonal variation in moonlight avoidance by bannertail kangaroo rats. J. Mammal. 55, 189–193 (1974).CAS
PubMed
Article
Google Scholar
33.Dawson, W. R. The relaxation of oxygen consumption to temperature in desert rodents. J. Mammal. 36, 543–553 (1955).Article
Google Scholar
34.Hart, J. S. Rodents. In Mammals. 1–149 (Academic Press, 1971).35.Quispe, R., Trappschuh, M., Gahr, M. & Goymann, W. Towards more physiological manipulations of hormones in field studies: Comparing the release dynamics of three kinds of testosterone implants, silastic tubing, time-release pellets and beeswax. Gen. Comp. Endocrinol. 212, 100–105 (2015).CAS
PubMed
Article
Google Scholar
36.Sahores, A. et al. Novel, low cost, highly effective, handmade steroid pellets for experimental studies. PLoS ONE 8, e64049 (2013).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
37.Sopinka, N. M. et al. Manipulating glucocorticoids in wild animals: Basic and applied perspectives. Conserv. Physiol. 3, cov031 (2015).PubMed
PubMed Central
Article
CAS
Google Scholar
38.Akana, S. F. et al. Feedback sensitivity of the rat hypothalamo-pituitary-adrenal axis and its capacity to adjust to exogenous corticosterone. Endocrinology 131, 585–594 (1992).CAS
PubMed
PubMed Central
Google Scholar
39.Bush, V. L., Middlemiss, D. N., Marsden, C. A. & Fone, K. C. F. Implantation of a slow release rorticosterone pellet induces long-term alterations in serotonergic neurochemistry in the rat brain. J. Neuroendocrinol. 15, 607–613 (2003).CAS
PubMed
Article
Google Scholar
40.Meyer, J. S., Micco, D. J., Stephenson, B. S., Krey, L. C. & McEwen, B. S. Subcutaneous implantation method for chronic glucocorticoid replacement therapy. Physiol. Behav. 22, 867–870 (1979).CAS
PubMed
Article
Google Scholar
41.Chang, C. C. & Kincl, F. A. Sustained release hormonal preparations: 3. Biological effectiveness of 6-methyl-1717α-acetoxypregna-4,6-diene-3,20-dione. Steroids 12, 689–696 (1968).CAS
PubMed
Article
Google Scholar
42.Kratochvíl, P., Benagiano, G. & Kincl, F. A. Sustained release hormonal preparations. 6. Permeability constant of various steroids. Steroids 15, 505–511 (1970).PubMed
Article
Google Scholar
43.Nash, H. A., Robertson, D. N., Moo Young, A. J. & Atkinson, L. E. Steroid release from silastic capsules and rods. Contraception 18, 367–394 (1978).CAS
PubMed
Article
Google Scholar
44.Borrow, A. P. et al. Chronic variable stress alters hypothalamic–pituitary–adrenal axis function in the female mouse. Physiol. Behav. 209, 112613 (2019).CAS
PubMed
PubMed Central
Article
Google Scholar
45.Lajud, N., Roque, A., Cajero, M., Gutiérrez-Ospina, G. & Torner, L. Periodic maternal separation decreases hippocampal neurogenesis without affecting basal corticosterone during the stress hyporesponsive period, but alters HPA axis and coping behavior in adulthood. Psychoneuroendocrinology 37, 410–420 (2012).CAS
PubMed
Article
Google Scholar
46.Mateo, J. M. & Cavigelli, S. A. A validation of extraction methods for noninvasive sampling of glucocorticoids in free-living ground squirrels. Physiol. Biochem. Zool. 78, 1069–1084 (2005).CAS
PubMed
PubMed Central
Article
Google Scholar
47.Touma, C., Palme, R. & Sachser, N. Analyzing corticosterone metabolites in fecal samples of mice: A noninvasive technique to monitor stress hormones. Horm. Behav. 45, 10–22 (2004).CAS
PubMed
Article
Google Scholar
48.Torres-Medina, F. et al. Corticosterone implants produce stress-hyporesponsive birds. J. Exp. Biol. 221, jeb173864 (2018).PubMed
Article
Google Scholar
49.Adzic, M. et al. Acute or chronic stress induce cell compartment-specific phosphorylation of glucocorticoid receptor and alter its transcriptional activity in Wistar rat brain. J. Endocrinol. 202, 87–97 (2009).CAS
PubMed
PubMed Central
Article
Google Scholar
50.Ellis, M. V. Development of a compact system for field euthanasia of small mammals. J. Mammal. 98, 1211–1214 (2017).Article
Google Scholar
51.Guglielmo, C. G., McGuire, L. P., Gerson, A. R. & Seewagen, C. L. Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance. J. Ornithol. 152, 75 (2011).Article
Google Scholar
52.McGuire, L. P. & Guglielmo, C. G. Quantitative magnetic resonance: A rapid, noninvasive body composition analysis technique for live and salvaged bats. J. Mammal. 91, 1375–1380 (2010).Article
Google Scholar
53.Warner, D. A., Johnson, M. S. & Nagy, T. R. Validation of body condition indices and quantitative magnetic resonance in estimating body composition in a small lizard. J. Exp. Zool. Part A Ecol. Genet. Physiol. 325, 588–597 (2016).CAS
Article
Google Scholar
54.Boyles, J. G. A brief introduction to methods for describing body temperature in endotherms. Physiol. Biochem. Zool. 92, 365–372 (2019).PubMed
Article
PubMed Central
Google Scholar
55.Monson, G. & Kessler, W. Life history notes on the banner-tailed kangaroo rat, Merriam’s kangaroo rat, and the white-throated wood rat in Arizona and New Mexico. J. Wildl. Manag. 4, 37–43 (1940).Article
Google Scholar
56.Smit, B., Boyles, J. G., Brigham, R. M. & Mckechnie, A. E. Torpor in dark times: patterns of heterothermy are associated with the lunar cycle in a nocturnal bird. J. Biol. Rhythms 26, 241–248 (2011).PubMed
Article
PubMed Central
Google Scholar
57.Kay, F. R. & Whitford, W. G. The burrow environment of the banner-tailed kangaroo rat, Dipodomys spectabilis, in southcentral New Mexico. Am. Midl. Nat. 99, 270–279 (1978).Article
Google Scholar
58.Randall, J. A. Territorial-defense interactions with neighbors and strangers in banner-tailed kangaroo rats. J. Mammal. 70, 308–315 (1989).Article
Google Scholar
59.Randall, J. A. Mating strategies of a nocturnal, desert rodent (Dipodomys spectabilis). Behav. Ecol. Sociobiol. 28, 215–220 (1991).Article
Google Scholar
60.Ward, D. W. & Randall, J. A. Territorial defense in the bannertail kangaroo rat (Dipodomys spectabilis): footdrumming and visual threats. Behav. Ecol. Sociobiol. 20, 323–328 (1987).Article
Google Scholar
61.Brown, J. S., Kotler, B. P., Smith, R. J. & Wirtz, W. O. The effects of owl predation on the foraging behavior of heteromyid rodents. Oecologia 76, 408–415 (1988).ADS
PubMed
Article
PubMed Central
Google Scholar
62.Navarro-Castilla, Á., Barja, I. & Díaz, M. Foraging, feeding, and physiological stress responses of wild wood mice to increased illumination and common genet cues. Curr. Zool. 64, 409–417 (2018).PubMed
Article
PubMed Central
Google Scholar
63.Sargunaraj, F., Kotler, B. P., Juliana, J. R. S. & Wielebnowski, N. Stress as an adaptation II: Does experimental cortisol supplementation affect predation risk assessment in foraging gerbils?. Evol. Ecol. Res. 18, 587–598 (2017).
Google Scholar
64.Voellmy, I. K., Goncalves, I. B., Barrette, M. F., Monfort, S. L. & Manser, M. B. Mean fecal glucocorticoid metabolites are associated with vigilance, whereas immediate cortisol levels better reflect acute anti-predator responses in meerkats. Horm. Behav. 66, 759–765 (2014).CAS
PubMed
Article
PubMed Central
Google Scholar
65.Kotler, B. P., Brown, J., Mukherjee, S., Berger-Tal, O. & Bouskila, A. Moonlight avoidance in gerbils reveals a sophisticated interplay among time allocation, vigilance and state-dependent foraging. Proc. R. Soc. B Biol. Sci. 277, 1469–1474 (2010).Article
Google Scholar
66.Pravosudov, V. V. Long-term moderate elevation of corticosterone facilitates avian food-caching behaviour and enhances spatial memory. Proc. R. Soc. B Biol. Sci. 270, 2599–2604 (2003).CAS
Article
Google Scholar
67.Speakman, J. R. & Król, E. Maximal heat dissipation capacity and hyperthermia risk: Neglected key factors in the ecology of endotherms. J. Anim. Ecol. 79, 726–746 (2010).PubMed
PubMed Central
Google Scholar
68.Humphries, M. M., Kramer, D. L. & Thomas, D. W. The role of energy availability in mammalian hibernation: An experimental test in free-ranging eastern chipmunks. Physiol. Biochem. Zool. 76, 165–179 (2003).PubMed
Article
PubMed Central
Google Scholar
69.Munro, D., Thomas, D. W. & Humphries, M. M. Torpor patterns of hibernating eastern chipmunks Tamias striatus vary in response to the size and fatty acid composition of food hoards. J. Anim. Ecol. 74, 692–700 (2005).Article
Google Scholar
70.Ernest, S. K. M. et al. Rodents, plants, and precipitation: Spatial and temporal dynamics of consumers and resources. Oikos 88, 470–482 (2017).Article
Google Scholar
71.Warne, R. W., Pershall, A. D. & Wolf, B. O. Linking precipitation and C3–C4 plant production to resource dynamics in higher-trophic-level consumers. Ecology 91, 1628–1638 (2010).PubMed
Article
Google Scholar
72.Warne, R. W., Baer, S. G. & Boyles, J. G. Community physiological ecology. Trends Ecol. Evol. 34, 510–518 (2019).PubMed
Article
Google Scholar More