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The role of steroid hormones and individual traits in food intake in the wood mouse (Apodemus sylvaticus)

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Abstract

Availability of food resources affects animal survival and reproduction. Thus, coping with changes in food availability is one of the most crucial behavioural and physiological processes in wildlife. Food intake is a key concept in animal ecology that is directly conditioned by food quality and abundance or diet choice, but may also vary according to individual-related factors (e.g. foraging behaviours, social rank or energy-demanding periods) and the influence of the endocrine system on energy metabolism. Here, we studied food intake in relation to individual characteristics (sex, breeding condition and age) and whether steroid hormones (testosterone and corticosterone metabolites) mediate food intake in wild wood mouse (Apodemus sylvaticus). Field work was carried out in February–March 2014 in Monte de Valdelatas (Madrid, Spain). Wood mice were live-trapped for 10 consecutive days in four independent plots. Traps were baited with 4 g of toasted corn and food intake was calculated by subtracting the remaining bait found inside traps. Fresh faecal samples from 130 different wood mice were collected and faecal testosterone and corticosterone metabolites (FTM and FCM, respectively) were analysed by enzyme immunoassays. Food intake was higher in females than males, probably due to greater energy requirements. Non-breeders and young individuals also showed a higher food intake. These individuals usually hold a lower social rank which is associated to limited food resources because of dominants; thus, increased food intake may be a result of freely exploit food bait inside traps while avoiding risky competition. In addition, food intake negatively correlated with FTM levels and positively with FCM levels indicating that both hormones have an active role mediating food intake in the wood mouse. Our data suggest that food intake is a function of both individual traits and the endocrine system that accordingly respond throughout different energy-demanding periods.

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References

  • Abelson KS, Kalliokoski O, Teilmann AC, Hau J (2016) Applicability of commercially available ELISA kits for the quantification of faecal immunoreactive corticosterone metabolites in mice. In Vivo 30:739–744

    Article  CAS  Google Scholar 

  • Alcántara M, Díaz M (1996) Patterns of body weight, body size, and body condition in the wood mouse Apodemus sylvaticus L.: effects of sex and habitat quality. Proceedings of the I European Congress of Mammalogy, pp 141–149

  • Bacigalupe LD, Bozinovic F (2002) Design, limitations and sustained metabolic rate: lessons from small mammals. J Exp Biol 205:2963–2970

    PubMed  Google Scholar 

  • Barboza PS, Parker KL, Hume ID (2009) Integrative wildlife nutrition. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Book AS, Starzyk KB, Quinsey VL (2001) The relationship between testosterone and aggression: a meta-analysis. Aggress Violent Behav 6:579–599

    Article  Google Scholar 

  • Briganti F, Della Seta D, Fontani G, Lodi L, Lupo C (2003) Behavioral effects of testosterone in relation to social rank in the male rabbit. Aggress Behav 29:269–278

    Article  CAS  Google Scholar 

  • Chen X, Wang L, Loh DH, Colwell CS, Taché Y, Reue K, Arnold A (2015) Sex differences in diurnal rhythms of food intake in mice caused by gonadal hormones and complement of sex chromosomes. Horm Behav 75:55–63

    Article  CAS  Google Scholar 

  • Dantzer B, McAdam AG, Palme R, Fletcher QE, Boutin S, Humphries MM, Boonstra R (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

    Article  CAS  Google Scholar 

  • Díaz M, Alonso CL (2003) Wood mouse Apodemus sylvaticus winter food supply: density, condition, breeding, and parasites. Ecology 84:2680–2691

    Article  Google Scholar 

  • Díaz M, Torre I, Arrizabalaga A (2010) Relative roles of density and rainfall on the short-term regulation of Mediterranean wood mouse Apodemus sylvaticus populations. Acta Theriol 55:251–260

    Article  Google Scholar 

  • Ebner K, Wotjak CT, Landgraf R, Engelmann M (2005) Neuroendocrine and behavioral response to social confrontation: residents versus intruders, active versus passive coping styles. Horm Behav 47:14–21

    Article  CAS  Google Scholar 

  • Gesquiere LR, Learn NH, Simao MC, Onyango PO, Alberts SC, Altmann J (2011) Life at the top: rank and stress in wild male baboons. Science 333:357–360

    Article  CAS  Google Scholar 

  • Godsall B, Coulson T, Malo AF (2014) From physiology to space use: energy reserves and androgenization explain home-range size variation in a woodland rodent. J Anim Ecol 83:126–135

    Article  Google Scholar 

  • Goymann W, Möstl E, Van't Hof T, East ML, Hofer H (1999) Noninvasive fecal monitoring of glucocorticoids in spotted hyenas, Crocuta crocuta. Gen Comp Endocrinol 114:340–348

    Article  CAS  Google Scholar 

  • Gurnell J, Flowerdew JR (2006) Live trapping small mammals. Mammal Society, London

    Google Scholar 

  • Handa RJ, Burgess LH, Kerr JE, O’Keefe JA (1994) Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm Behav 28:464–476

    Article  CAS  Google Scholar 

  • Hernández MC, Navarro-Castilla Á, Piñeiro A, Barja I (2018a) Wood mice aggressiveness and flight response to human handling: effect of individual and environmental factors. Ethology 124:559–569

    Article  Google Scholar 

  • Hernández MC, Navarro-Castilla Á, Planillo A, Sánchez-González B, Barja I (2018b) 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

    Article  Google Scholar 

  • Hiadlovská Z, Mikula O, Macholán M, Hamplová P, Bímová BV, Daniszová K (2015) Shaking the myth: body mass, aggression, steroid hormones, and social dominance in wild house mouse. Gen Comp Endocrinol 223:16–26

    Article  Google Scholar 

  • Hirschenhauser K, Oliveira RF (2006) Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis. Anim Behav 71:265–277

    Article  Google Scholar 

  • Hughes VL, Randolph SE (2001) Testosterone increases the transmission potential of tick-borne parasites. Parasitology 123:365–371

    Article  CAS  Google Scholar 

  • Kenagy GJ, Stevenson RD, Masman D (1989) Energy requirements for lactation and postnatal growth in captive golden-mantled ground squirrels. Physiol Zool 62:470–487

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Li Z, Wang Y, Sun KK, Wang K, Sun ZS, Zhao M, Wang J (2015) Sex-related difference in food-anticipatory activity of mice. Horm Behav 70:38–46

    Article  CAS  Google Scholar 

  • Lutermann H, Young AJ, Bennett NC (2013) Reproductive status and testosterone among females in cooperative mole-rat societies. Gen Comp Endocrinol 187:60–65

    Article  CAS  Google Scholar 

  • Malo AF, Godsall B, Prebble C, Grange Z, McCandless S, Taylor A, Coulson T (2013) Positive effects of an invasive shrub on aggregation and abundance of a native small rodent. Behav Ecol 24:759–767

    Article  Google Scholar 

  • Martineau J, Pothier D, Fortin D (2016) Processes driving short-term temporal dynamics of small mammal distribution in human-disturbed environments. Oecologia 181:831–840

    Article  Google Scholar 

  • Mills SC, Grapputo A, Jokinen I, Koskela E, Mappes T, Oksanen TA, Poikonen T (2009) Testosterone-mediated effects on fitness-related phenotypic traits and fitness. Am Nat 173:475–487

    Article  Google Scholar 

  • Monarca RI, da Luz Mathias M, Speakman JR (2015) Behavioural and physiological responses of wood mice (Apodemus sylvaticus) to experimental manipulations of predation and starvation risk. Physiol Behav 149:331–339

    Article  CAS  Google Scholar 

  • Montgomery SSJ, Montgomery WI (1990) Intrapopulation variation in the diet of the wood mouse Apodemus sylvaticus. J Zool 222:641–651

    Article  Google Scholar 

  • Montgomery WI, Wilson WL, Hamilton R, McCartney P (1991) Dispersion in the wood mouse, Apodemus sylvaticus: variable resources in time and space. J Anim Ecol 60:179–192

    Article  Google Scholar 

  • Morris DW (2003) Toward an ecological synthesis: a case for habitat selection. Oecologia 136:1–13

    Article  Google Scholar 

  • Muir C, Vella E, Pisani N (2001) Enzyme immunoassay of 17β-estradiol, estrone conjugates, and testosterone in urinary and fecal samples from male and female mice. Horm Metab Res 33:653–658

    Article  CAS  Google Scholar 

  • Navarro-Castilla Á, Barja I (2014a) Antipredatory response and food intake in wood mice (Apodemus sylvaticus) under simulated predation risk by resident and novel carnivorous predators. Ethology 120:90–98

    Article  Google Scholar 

  • Navarro-Castilla Á, Barja I (2014b) Does predation risk, through moon phase and predator cues, modulate food intake, antipredatory and physiological responses in wood mice (Apodemus sylvaticus)? Behav Ecol Sociobiol 68:1505–1512

    Article  Google Scholar 

  • Navarro-Castilla Á, Barja I (2019) Stressful living in lower-quality habitats? Body mass, feeding behaviour and physiological stress levels in wild wood mouse populations. Integr Zool 14:114–126

    Article  Google Scholar 

  • Navarro-Castilla Á, Díaz M, Barja I (2017) Does ungulate disturbance mediate behavioural and physiological stress responses in Algerian mouse (Mus spretus)? A wild exclosure experiment. Hystrix, Ital J Mammal 28:165–172

    Google Scholar 

  • Navarro-Castilla Á, Barja I, Díaz M (2018) Foraging, feeding, and physiological stress responses of wild wood mice to increased illumination and common genet cues. Curr Zool 64:409–417

    Article  Google Scholar 

  • Navarro-Castilla Á, Sánchez-González S, Barja I (2019) Latrine behaviour and faecal corticosterone metabolites as indicators of habitat-related responses of wild rabbits to predation risk. Ecol Indic 97:175–182

    Article  Google Scholar 

  • Neuman-Lee LA, Bobby Fokidis H, Spence AR, Van der Walt M, Smith GD, Durham S, French SS (2015) Food restriction and chronic stress alter energy use and affect immunity in an infrequent feeder. Funct Ecol 29:1453–1462

    Article  Google Scholar 

  • Oyegbile TO, Marler CA (2006) Weak winner effect in a less aggressive mammal: correlations with corticosterone but not testosterone. Physiol Behav 89:171–179

    Article  CAS  Google Scholar 

  • Penn DJ, Smith KR (2007) Differential fitness costs of reproduction between the sexes. Proc Natl Acad Sci 104:553–558

    Article  CAS  Google Scholar 

  • Raynaud J, Müller K, Schradin C (2012) Experimental increase of testosterone levels in free-ranging juvenile male African striped mice (Rhabdomys pumilio) induces physiological, morphological, and behavioral changes. Gen Comp Endocrinol 178:108–115

    Article  CAS  Google Scholar 

  • Reue K (2017) Sex differences in obesity: X chromosome dosage as a risk factor for increased food intake, adiposity and co-morbidities. Physiol Behav 176:174–182

    Article  CAS  Google Scholar 

  • Rimbach R, Willigenburg R, Schoepf I, Yuen CH, Pillay N, Schradin C (2016) Young but not old adult African striped mice reduce their activity in the dry season when food availability is low. Ethology 122:828–840

    Article  Google Scholar 

  • Rogovin K, Randall JA, Kolosova I, Moshkin M (2003) Social correlates of stress in adult males of the great gerbil, Rhombomys opimus, in years of high and low population densities. Horm Behav 43:132–139

    Article  Google Scholar 

  • Sánchez-González B, Barja I, Navarro-Castilla Á (2017) Wood mice modify food intake under different degrees of predation risk: influence of acquired experience and degradation of predator’s faecal volatile compounds. Chemoecology 27:115–122

    Article  Google Scholar 

  • Sánchez-González B, Planillo A, Navarro-Castilla Á, Barja I (2018) The concentration of fear: mice’s behavioural and physiological stress responses to different degrees of predation risk. Sci Nat 105:16

    Article  Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89

    CAS  Google Scholar 

  • Scantlebury M, Waterman JM, Bennett NC (2008) Alternative reproductive tactics in male Cape ground squirrels Xerus inauris. Physiol Behav 94:359–367

    Article  CAS  Google Scholar 

  • Schradin C, Pillay N, Kondratyeva A, Yuen C, Schoepf I, Krackow S (2015) Basal blood glucose concentration in free-living striped mice is influenced by food availability, ambient temperature and social tactic. Biol Lett 11:20150208

    Article  Google Scholar 

  • Speakman JR (2008) The physiological costs of reproduction in small mammals. Philos Trans R Soc Lond Ser B Biol Sci 363:375–398

    Article  Google Scholar 

  • Torre I, Arrizabalaga A, Díaz M (2002) Ratón de campo Apodemus sylvaticus. Galemys 14:1–26

    Google Scholar 

  • Touma C, Sachser N, Möstl E, Palme R (2003) Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen Comp Endocrinol 130:267–278

    Article  CAS  Google Scholar 

  • Trainor BC, Bird IM, Marler CA (2004) Opposing hormonal mechanisms of aggression revealed through short-lived testosterone manipulations and multiple winning experiences. Horm Behav 45:115–121

    Article  CAS  Google Scholar 

  • Wan-long Z, Zheng-kun W (2016) Effects of random food deprivation and refeeding on energy metabolism, behavior and hypothalamic neuropeptide expression in Apodemus chevrieri. Comp Biochem Physiol A Mol Integr Physiol 201:71–78

    Article  Google Scholar 

  • Williamson CM, Romeo RD, Curley JP (2017a) Dynamic changes in social dominance and mPOA GnRH expression in male mice following social opportunity. Horm Behav 87:80–88

    Article  CAS  Google Scholar 

  • Williamson CM, Lee W, Romeo RD, Curley JP (2017b) Social context-dependent relationships between mouse dominance rank and plasma hormone levels. Physiol Behav 171:110–119

    Article  CAS  Google Scholar 

  • Wingfield JC, Romero LM (2001) Adrenocortical responses to stress and their modulation in free-living vertebrates. In: McEwen BS, Goodman HM (eds) Handbook of Physiology – Coping with the Environment: Neural and Endocrine Mechanisms. Oxford University Press, New York, pp 211–234

    Google Scholar 

  • Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone—behavior interactions: the “emergency life history stage”. Am Zool 38:191–206

    Article  CAS  Google Scholar 

  • Wróbel A, Bogdziewicz M (2015) It is raining mice and voles: which weather conditions influence the activity of Apodemus flavicollis and Myodes glareolus? Eur J Wildl Res 61:475–478

    Article  Google Scholar 

  • Yang T, Xu W, York H, Liang N (2017) Diet choice patterns in rodents depend on novelty of the diet, exercise, species, and sex. Physiol Behav 176:149–158

    Article  CAS  Google Scholar 

  • Young KM, Walker SL, Lanthier C, Waddell WT, Monfort SL, Brown JL (2004) Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. Gen Comp Endocrinol 137:148–165

    Article  CAS  Google Scholar 

  • Zhao Z, Wang D (2007) Effects of diet quality on energy budgets and thermogenesis in Brandt's voles. Comp Biochem Physiol A Mol Integr Physiol 148:168–177

    Article  Google Scholar 

  • Zohdy S, Bisanzio D, Tecot S, Wright PC, Jernvall J (2017) Aggression and hormones are associated with heterogeneity in parasitism and parasite dynamics in the brown mouse lemur. Anim Behav 132:109–119

    Article  Google Scholar 

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Acknowledgements

We thank to the Comunidad Autónoma of Madrid (Spain) for providing the permits required to conduct this study and to the Universidad Autónoma de Madrid (Spain) for allowing us to carry out this project. We also thank Juan Malo and Cristina Mata for the logistical support.

Funding

ANC was supported by a FPU scholarship from the Spanish Ministry of Education and Science (grant number AP2008-03430).

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Correspondence to Álvaro Navarro-Castilla.

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This research complies with the regulations on the protection of animals used for scientific purposes: Directive 2010/63/EU of the European Parliament and of the Council, and the Spanish legislation (Royal Decree 53/2013). The study had the approval of the Autonomous Community of Madrid (reference number 10/211643.9/13) and favourable reports from both the Ethics Committee of the Autonomous University of Madrid and the Body Enabled (CIS 50-940-A007).

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Communicated by: Matthias Waltert

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Navarro-Castilla, Á., Sánchez-González, B. & Barja, I. The role of steroid hormones and individual traits in food intake in the wood mouse (Apodemus sylvaticus). Sci Nat 106, 36 (2019). https://doi.org/10.1007/s00114-019-1628-7

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