Abstract
California mice (Peromyscus californicus) differ from most other mammals in that they are biparental, genetically monogamous, and (compared with other Peromyscus) relatively large. We evaluated effects of cold acclimation on metabolic rate, exercise performance, and morphology of pair-housed male California mice, as well as modulation of these effects by fatherhood. In Experiment 1, virgin males housed at 5° or 10 °C for approximately 25 days were compared with virgins housed at standard vivarium temperature of 22 °C. Measures included resting metabolic rate (RMR), maximal oxygen consumption (\(\dot{V}{\text{O}}_{2}\)max), grip strength, and sprint speed. In Experiment 2, virgin males housed at 22 °C were compared with three groups of males housed at 10 °C: virgins, breeding males (housed with a female and their pups), and non-breeding males (housed with an ovariectomized, estrogen- and progesterone-treated female) after long-term acclimation (mean 243 days). Measures in this experiment included basal metabolic rate (BMR), \(\dot{V}{\text{O}}_{2}\)max, maximal thermogenic capacity (\(\dot{V}{\text{O}}_{2}\)sum), and morphological traits. In Experiment 1, virgin males housed at 5° and 10 °C had higher RMR and \(\dot{V}{\text{O}}_{2}\)max than those at 22 °C. In Experiment 2, 10 °C-acclimated groups had shorter bodies; increased body, fat, and lean masses; higher BMR and \(\dot{V}{\text{O}}_{2}\)sum, and generally greater morphometric measures and organ masses than virgin males at 22 °C. Among the groups housed at 10 °C, breeding males had higher BMR and lower \(\dot{V}{\text{O}}_{2}\)max than non-breeding and/or virgin males. Overall, we found that effects of fatherhood during cold acclimation were inconsistent, and that several aspects of cold acclimation differ substantially between California mice and other small mammals.
Similar content being viewed by others
References
Achenbach GG, Snowdon CT (2002) Costs of caregiving: weight loss in captive adult male cotton-top tamarins (Saguinus oedipus) following the birth of infants. Int J Primatol 23:179–189
Andrew JR, Saltzman W, Chappell MA, Garland T Jr (2016) Consequences of fatherhood in the biparental California mouse (Peromyscus californicus): locomotor performance, metabolic rate, and organ masses. Physiol Biochem Zool 89:130–140
Bales KL, Saltzman W (2016) Fathering in rodents: neurobiological substrates and consequences for offspring. Horm Behav 77:249–259
Bedford NL, Hoekstra HE (2015) Peromyscus mice as a model for studying natural variation. Elife 4:e06813
Benjamini Y (2010) Discovering the false discovery rate. J R Stat Soc B 72:405–416
Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206:649–654
Biro PA, Garland T Jr, Beckmann C, Ujvari B, Thomas F, Post JR (2018) Metabolic scope as a proximate constraint on individual behavioral variation: effects on personality, plasticity, and predictability. Am Nat 192:142–154. https://doi.org/10.1086/697963
Braun K, Champagne FA (2014) Paternal influences on offspring development: behavioural and epigenetic pathways. J Neuroendocrinol 26:697–706
Brylski P, Harris J (1990) California’s wildlife volume III. California Department of Fish and Game, Sacramento
Brzęk P, Bielawska K, Książek A, Konarzewski M (2007) Anatomic and molecular correlates of divergent selection for basal metabolic rate in laboratory mice. Physiol Biochem Zool 80:491–499
Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359
Cantoni D, Brown RE (1997) Paternal investment and reproductive success in the California mouse, Peromyscus californicus. Anim Behav 54:377–386
Chappell MA, Rezende EL, Hammond KA (2003) Age and aerobic performance in deer mice. J Exp Biol 206:1221–1231
Chappell MA, Garland T Jr, Robertson GF, Saltzman W (2007) Relationships among running performance, aerobic physiology and organ mass in male Mongolian gerbils. J Exp Bio 210:4179–4197
Chauke M, Malisch JL, Robinson C, de Jong TR, Saltzman W (2011) Effects of reproductive status on behavioral and endocrine responses to acute stress in a biparental rodent, the California mouse (Peromyscus californicus). Horm Behav 60:128–138
Dawson TJ, Olson JMM (1988) Thermogenic capabilities of the opossum Monodelphis domestica when warm and cold acclimated: similarities between American and Australian marsupials. Comp Biochem Physiol 89:85–91
Derting TL, Austin MW (1998) Changes in gut capacity with lactation and cold exposure in a species with low rates of energy use, the pine vole (Microtus pinetorum). Physiol Zool 71:611–623
Deveci D, Stone PC, Egginton S (2001) Differential effect of cold acclimation on blood composition in rats and hamsters. J Comp Physiol B 171:135–143
Djawdan M, Garland T Jr (1988) Maximal running speeds of bipedal and quadrupedal rodents. J Mamm 69:765–772
Dlugosz EM, Harris BN, Saltzman W, Chappell MA (2012) Glucocorticoids, aerobic physiology, and locomotor behavior in California mice. Physiol Biochem Zool 85:671–683
Dudley D (1974) Paternal behavior in the California mouse, Peromyscus californicus. Behav Bio 11:247–252
Feist DD, White RG (1989) Terrestrial mammals in cold. In: Wang LCH (ed) Advances in comparative and environmental physiology 4. Academic Press, London, pp 328–354
Gammie SC, Hasen NS, Rhodes JS, Girard I, Garland T Jr (2003) Predatory aggression, but not maternal or intermale aggression, is associated with high voluntary wheel-running behavior in mice. Horm Behav 44:209–221
Gilbert G, McCafferty D, Le Maho Y, Martrette J-M, Giroud S, Blanc S, Ancel A (2010) One for all and all for one: the energetic benefits of huddling in endotherms. Biol Rev 85:545–569
Gittleman JL, Thompson SD (1988) Energy allocation in mammalian reproduction. Am Zool 28:863–875
Gubernick DJ (1988) Reproduction in the California mouse, Peromyscus californicus. J Mammal 69:857–860
Gubernick DJ, Alberts JR (1987a) The biparental care system of the California mouse, Peromyscus californicus. J Comp Psych 101:169–177
Gubernick DJ, Alberts JR (1987b) “Resource” exchange in the biparental California mouse (Peromyscus californicus): water transfer from pups to parents. J Comp Psych 101:328–334
Gubernick DJ, Teferi T (2000) Adaptive significance of male parental care in a monogamous mammal. Proc R Soc 267:147–150
Gubernick DJ, Wright SL, Brown RE (1993) The significance of father’s presence for offspring survival in the monogamous California mouse, Peromyscus californicus. Anim Behav 46:539–546
Hall ER (1981) The mammals of North America. Wiley, New York
Hammond KA (1997) Adaptation of the maternal intestine during lactation. J Mammary Gland Biol Neoplasia 2:243–252
Hammond KA, Kristan DM (2000) Responses to lactation and cold exposure by deer mice (Peromyscus maniculatus). Physiol Biochem Zool 73:547–556
Hammond KA, Wunder BA (1995) Effect of cold temperatures on the morphology of gastrointestinal tracts of two microtine rodents. J Mammal 76:232–239
Harris BN, Perea-Rodriguez JP, Saltzman W (2011) Acute effects of corticosterone injection on paternal behavior in California mouse (Peromyscus californicus) fathers. Horm Behav 60:666–675
Hart JS (1957) Climatic and temperature induced changes in the energetics of homeotherms. Rev Can Biol 16:166–174
Hart JS (1971) Rodents. In: Whittow GC (ed) Comparative physiology of thermoregulation. Academic Press, New York, pp 1–149
Hayes JP (1989a) Altitudinal and seasonal effects on aerobic metabolism of deer mice. J Comp Physiol B 159:453–459
Hayes JP (1989b) Field and maximal metabolic rates of deer mice (Peromyscus maniculatus) at low and high altitudes. Physiol Zool 62:732–744
Hayes JP, Chappell MA (1986) Effects of cold acclimation on maximum oxygen consumption during cold exposure and treadmill exercise in deer mice, Peromyscus maniculatus. Physiol Zool 59:473–481
Hayes JP, Chappell MA (1990) Individual consistency of maximal oxygen consumption in deer mice. Funct Ecol 4:495–503
Hayes JP, O’Connor CS (1999) Natural selection on thermogenic capacity of high-altitude deer mice. Int J Biometeorol 22:129–134
Hayward JS (1965) Metabolic rate and its temperature-adaptive significance in six geographic races of Peromyscus. Can J Zool 43:309–323
Heimer W, Morrison P (1978) Effects of chronic and intermittent cold exposure on metabolic capacity of Peromyscus and Microtus. Int J Biometeorol 22:129–134
Heldmaier G, Steinlechner S, Rafael J (1982) Nonshivering thermogenesis and cold resistance during seasonal acclimatization in the Djungarian hamster. J Comp Physiol B 149:1–9
Heldmaier G, Klaus S, Wiesinger H, Fredrichs U, Wenzel M (1989) Cold acclimation and thermogenesis. In: Malan A, Canguilhem B (eds) Living in the cold II. John Libby Eurotext, London, pp 347–358
Hill RW (1983) Thermal physiology and energetics of Peromyscus; ontogeny, body temperature, metabolism, insulation, and microclimatology. J Mammal 64:19–37
Hulbert AJ, Else PL (2004) Basal metabolic rate: history, composition, regulation, and usefulness. Physiol Biochem Zool 77:869–876
King JA (1968) Biology of Peromyscus (Rodentia). The American Society of Mammalogists, Pittsburgh
Konarzewski M, Diamond J (1994) Peak sustained metabolic rate and its individual variation in cold-stressed mice. Physiol Zool 67:1186–1212
Lee AW, Brown RE (2002) The presence of the male facilitates parturition in California mice (Peromyscus californicus). Can J Zool 80:926–933
Lynch GR (1973) Seasonal changes in thermogenesis, organ weights, and body composition in the white-footed mouse, Peromyscus leucopus. Oecologia 13:363–376
Maurissen JPJ, Marable BR, Andrus AK, Stebbins KE (2003) Factors affecting grip strength testing. Neurotoxicol Teratol 25:543–553
McNab BK, Morrison P (1963) Body temperature and metabolism in subspecies of Peromyscus from arid and mesic environments. Ecol Mono 33:63–82
Merritt JF (1974) Factors influencing the local distribution of Peromyscus californicus in northern California. J Mammal 55:102–114
Meyer OA, Tilson HA, Byrd WC, Riley MT (1979) A method for the routine assessment of fore-and hindlimb grip strength of rats and mice. Neurobehav Toxicol 1:233
Nespolo RF, Opazo JC, Rosenmann M, Bozinovic F (1999) Thermal acclimation, maximum metabolic rate, and nonshivering thermogenesis of Phyllotis xanthopygus (Rodentia) in the Andes mountains. J Mammol 80:742–748
Nespolo RF, Bacigalupe LD, Rezende EL, Bozinovic F (2001) When nonshivering thermogenesis equals maximum metabolic rate: thermal acclimation and phenotypic plasticity of fossorial Spalacopus cyanus (Rodentia). Physiol Biochem Zool 74:325–332
Reid REB, Greenwald EN, Wang Y, Wilmers CC (2013) Dietary niche partitioning by sympatric Peromyscus boylii and P. californicus in a mixed evergreen forest. J Mammal 94:1248–1257
Rezende EL, Bozinovic F, Garland T Jr (2004a) Climatic adaptation and the evolution of basal and maximum rates of metabolism in rodents. Evolution 58:1361–1374
Rezende EL, Chappell MA, Hammond KA (2004b) Cold-acclimation in Peromyscus: temporal effects and individual variation in maximum metabolism and ventilatory traits. J Exp Bio 207:295–305
Rezende EL, Hammond KA, Chappell MA (2009) Cold acclimation in Peromyscus: individual variation and sex effects in maximum and daily metabolism, organ mass and body composition. J Exp Bio 212:2795–2802
Ribble DO (1991) The monogamous mating system of Peromyscus californicus as revealed by DNA fingerprinting. Behav Ecol Sociobiol 29:161–166
Ribble DO (1992) Lifetime reproductive success and its correlates in the monogamous rodent, Peromyscus californicus. J Anim Ecol 61:457–468
Ribble DO, Salvioni M (1990) Social organization and nest co-occupancy in Peromyscus californicus, a monogamous rodent. Behav Ecol Sociobiol 26:9–15
Ricklefs RE, Konarzewski M, Daan S (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147:1047–1071
Rosenmann M, Morrison P (1974) Maximum oxygen consumption and heat loss facilitation in small homeotherms by He-O2. Am J Physiol 226:490–495
Russell GA, Chappell MA (2007) Is BMR repeatable in deer mice? Organ mass correlates and the effects of cold acclimation and natal altitude. J Comp Physiol B 177:75–87
Saltzman W, Ziegler TE (2014) Functional significance of hormonal changes in mammalian fathers. J Neuroendocrinol 26:685–696
Saltzman W, Harris BN, de Jong TR, Nguyen PP, Cho JT, Hernandez M, Perea-Rodriguez JP (2015) Effects of parental status on male body mass in the monogamous, biparental California mouse. J Zool 296:23–29
Smith RE, Horwitz BA (1969) Brown fat and thermogenesis. Physiol Rev 49:330–408
Speakman JR (2008) The physiological costs of reproduction in small mammals. Proc R Soc B 363:375–398
Vaanholt LM, Daan S, Schubert KA, Visser GH (2009) Metabolism and aging: effects of cold exposure on metabolic rate, body composition, and longevity in mice. Physiol Biochem Zool 82:314–324
Wickler SJ (1980) Maximal thermogenic capacity and body temperatures of white-footed mice (Peromyscus) in summer and winter. Physiol Zool 53:338–346
Zhao M, Garland T Jr, Chappell MA, Andrew JR, Saltzman W (2017) Metabolic and affective consequences of fatherhood in male California mice. Physiol Behav 177:57–67
Zhao M, Garland T Jr, Chappell MA, Andrew JR, Harris BN, Saltzman W (2018) Effects of a physical and energetic challenge on male California mice (Peromyscus californicus): modulation by reproductive condition. J Exp Bio 1:jeb168559
Ziegler TE, Prudom SL, Schultz-Darken NJ, Kurian AV, Snowdon CT (2006) Pregnancy weight gain: marmoset and tamarin dads show it too. Biol Lett 2:181–183
Zub K (2014) Lower body mass and higher metabolic rate enhance winter survival in root voles, Microtus oeconomus. Biol J Linn Soc 113:297–309
Acknowledgements
The authors would like to thank Joel Raqueno, Anthony Atalla, Allison Ibarra, Lorraine Horwitz, Felicia Gu, and Ashley Wong for assistance with data collection, Nathan Horrell and Dr. Juan Pablo Perea-Rodriguez for assistance with training and discussion of the study, the animal care staff of the UCR Spieth vivarium for maintenance of animals, and two anonymous reviewers for constructive comments on an earlier draft of the manuscript. This research was supported by NSF Grant IOS 1256572 and NIH Grant R21HD075021.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by F. Geiser.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Andrew, J.R., Garland, T., Chappell, M.A. et al. Effects of short- and long-term cold acclimation on morphology, physiology, and exercise performance of California mice (Peromyscus californicus): potential modulation by fatherhood. J Comp Physiol B 189, 471–487 (2019). https://doi.org/10.1007/s00360-019-01219-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-019-01219-7