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Does predation risk, through moon phase and predator cues, modulate food intake, antipredatory and physiological responses in wood mice (Apodemus sylvaticus)?

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Abstract

Predation influences the ecology and behaviour of prey species and it is well known that the risk of predation affects prey’s decision making. We investigated whether predation risk through moon phase and exposure to the faecal odour of a natural predator, the red fox Vulpes vulpes, affect feeding behaviour and physiological response in wood mice (Apodemus sylvaticus). Antipredatory response was studied by live trapping under new and full moon in odourless control areas and areas experimentally manipulated with red fox fresh faeces. Food intake by individuals was determined as the amount of bait remaining in each trap and the physiological response was measured non-invasively analysing faecal corticosterone metabolites (FCM). Traps treated with faeces of red fox were the most avoided, and this avoidance was more significant during full moon. Food intake by wood mice varied according to the moon phase being significantly lower under full moon nights. We found sex, breeding condition and weight of individuals explaining the variation found in FCM concentrations, but no changes in FCM levels due to moon phase or exposure to red fox faeces were detected. These results indicate that wood mice avoid red fox faecal odour and this antipredatory response as well as feeding behaviour are significantly influenced by moon phase. However, no physiological response was found due to predation risk suggesting that wood mice do not take these predation cues enough reliable to experience physiological changes.

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References

  • Abrahams MV, Dill LM (1989) A determination of the energetic equivalence of the risk of predation. Ecology 70:999–1007

    Article  Google Scholar 

  • Abrams PA (1986) Is predator–prey coevolution an arms race? Trends Ecol Evol 1:108–110

    Article  CAS  PubMed  Google Scholar 

  • Andreolini F, Jemiolo B, Novotny M (1987) Dynamics of excretion of urinary chemosignals in the house mouse (Mus musculus) during the natural estrous cycle. Experientia 43:998–1002

    Article  CAS  PubMed  Google Scholar 

  • Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav R 29:1123–1144

    Article  Google Scholar 

  • Barja I (2009) Decision making in plant selection during the faecal-marking behaviour of wild wolves. Anim Behav 77:489–493

    Article  Google Scholar 

  • Barja I, de Miguel FJ, Bárcena F (2005) Faecal marking behaviour of Iberian wolf in different zones of their territory. Folia Zool 54:21–29

    Google Scholar 

  • Barja I, Silván G, Rosellini S, Piñeiro A, González-Gil A, Camacho L, Illera JC (2007) Stress physiological responses to tourist pressure in a wild population of European pine marten. J Steroid Biochem 104:136–142

    Article  CAS  Google Scholar 

  • Barja I, Escribano G, Lara C, Virgós E, Benito J, Rafart E (2012) Non-invasive monitoring of adrenocortical activity in European badgers (Meles meles) and effects of sample collection and storage on faecal cortisol metabolite concentrations. Anim Biol 62:419–432

    Article  Google Scholar 

  • Barreto GR, Macdonald DW (1999) The response of water voles, Arvicola terrestris, to the odours of predators. Anim Behav 57:1107–1112

    Article  PubMed  Google Scholar 

  • Bauman DE (2000) Regulation of nutrient partitioning during lactation: homeostasis and homeorhesis revisited. In: Cronjé PB (ed) Ruminant physiology: digestion, metabolism, growth and reproduction. CAB, New York, pp 311–327

    Google Scholar 

  • Bednekoff PA, Lima SL (2004) Risk allocation and competition in foraging groups: reversed effects of competition if group size varies under risk of predation. Proc R Soc Lond B 271:1491–1496

    Article  Google Scholar 

  • Boonstra R, Hik D, Singleton GR, Tinnikov A (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecol Monogr 79:371–394

    Article  Google Scholar 

  • Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014

    Article  Google Scholar 

  • Brown JS, Laundré JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399

    Article  Google Scholar 

  • Calder CJ, Gorman ML (1991) The effects of red fox Vulpes vulpes faecal odours on the feeding behaviour of Orkney voles Microtus arvalis. J Zool 224:599–606

    Article  Google Scholar 

  • Daly M, Behrends PR, Wilson MI, Jacobs LF (1992) Behavioural modulation of predation risk: moonlight avoidance and crepuscular compensation in a nocturnal desert rodent, Dipodomys merriami. Anim Behav 44:1–9

    Article  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  PubMed  Google Scholar 

  • Díaz M (1992) Rodent seed predation in cereal crop areas of central Spain: effects of physiognomy, food availability, and predation risk. Ecography 15:77–85

    Article  Google Scholar 

  • Díaz M, Torre I, Peris A, Tena L (2005) Foraging behavior of wood mice as related to presence and activity of genets. J Mammal 86:1178–1185

    Article  Google Scholar 

  • Dickman CR, Doncaster CP (1984) Responses of small mammals to red fox (Vulpes vulpes) odour. J Zool 204:521–531

    Article  Google Scholar 

  • Eilam D (2004) Locomotor activity in common spiny mice (Acomys cahirinuse): the effect of light and environmental complexity. BMC Ecology 4:16

    Article  PubMed Central  PubMed  Google Scholar 

  • Eilam D, Dayan T, Ben-Eliyahu S, Schulman I, Shefer G, Hendrie CA (1999) Differential behavioural and hormonal responses of voles and spiny mice to owl calls. Anim Behav 58:1085–1093

    Article  PubMed  Google Scholar 

  • Epple G, Belcher AM, Kuderling I, Zeller U, Scolnick L, Greenfield KL, Smith ABI (1993) Making sense out of scents: species differences in scent glands, scent-marking behaviour, and scent-mark composition in the Callitrichidae. In: Rylands AB (ed) Marmosets and tamarins: systematics, behaviour, and ecology. Oxford University Press, New York, pp 123–151

    Google Scholar 

  • Fletcher QE, Boonstra R (2006) Do captive male meadow voles experience acute stress in response to weasel odour? Can J Zool 84:583–588

    Article  CAS  Google Scholar 

  • Gurnell J, Flowerdew JR (1994) Live trapping small mammals. A practical guide. The Mammal Society, London

    Google Scholar 

  • Hauger R, Thrivikraman K, Plotsky P (1994) Age-related alterations of hypothalamic–pituitary–adrenal axis function in male Fischer 344 rats. Endocrinology 134:1528–1536

    CAS  PubMed  Google Scholar 

  • Hayes RA, Morelli TL, Wright PC (2006) Volatile components of lemur scent secretions vary throughout the year. Am J Primatol 68:1202–1207

    Article  CAS  PubMed  Google Scholar 

  • Hirschenhauser K, Möstl E, Wallner B, Dittami J, Kotrschal K (2000) Endocrine and behavioural responses of male greylag geese (Anser anser) to pairbond challenges during the reproductive season. Ethology 106:63–77

    Article  Google Scholar 

  • Hutchings MR, White PCL (2000) Mustelid scent–marking in managed ecosystems: implications for population management. Mamm Rev 30:157–169

    Article  Google Scholar 

  • Jedrzejewski W, Rychlik L, Jedrzejewska B (1993) Responses of bank voles to odours of seven species of predators: experimental data and their relevance to natural predator–vole relationships. Oikos 68:251–257

    Article  Google Scholar 

  • Jemiolo B, Xie TM, Andreolini F, Baker AEM, Novotny M (1991) The t complex of the mouse: chemical characterization by urinary volatile profiles. J Chem Ecol 17:353–367

    Article  CAS  PubMed  Google Scholar 

  • Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394

    Google Scholar 

  • Kaufman DW, Kaufman GA (1982) Effect of moonlight on activity and microhabitat use by Ord's kangaroo rat (Dipodomys ordii). J Mammal 63:309–312

    Article  Google Scholar 

  • Korte SM (2001) Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci Biobehav R 25:117–142

    Article  CAS  Google Scholar 

  • Kotler BP, Brown JS, Hasson O (1991) Owl predation on gerbils: the role of body size, illumination, and habitat structure on rates of predation. Ecology 72:2249–2260

    Article  Google Scholar 

  • Kotler BP, Brown J, Mukherjee S, Berger-Tal O, Bouskila A (2010) Moonlight avoidance in gerbils reveals a sophisticated interplay among time allocation, vigilance and state-dependent foraging. Proc R Soc Lond B 277:1469–1474

    Article  Google Scholar 

  • Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv Stud Behav 27:215–290

    Article  Google Scholar 

  • Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Lima SL, Valone TJ (1986) Influence of predation risk on diet selection: a simple example in the grey squirrel. Anim Behav 34:536–544

    Article  Google Scholar 

  • Liu J, Chen Y, Guo L, Gu B, Liu H, Hou A, Liu X, Sun L, Liu D (2006) Stereotypic behavior and fecal cortisol level in captive giant pandas in relation to environmental enrichment. Zoo Biol 25:445–459

    Article  CAS  Google Scholar 

  • Longland WS, Price MV (1991) Direct observations of owls and heteromyid rodents: can predation risk explain microhabitat use? Ecology 72:2261–2273

    Article  Google Scholar 

  • Martín J, Barja I, López P (2010) Chemical scent constituents in feces of wild Iberian wolves (Canis lupus signatus). Biochem Syst Ecol 38:1096–1102

    Article  Google Scholar 

  • Millspaugh JJ, Washburn BE (2003) Within-sample variation of fecal glucocorticoid measurements. Gen Comp Endocrinol 132:21–26

    Article  CAS  PubMed  Google Scholar 

  • Monclús R, Rödel HG, Palme R, Von Holst D, de Miguel J (2006) Non-invasive measurement of the physiological stress response of wild rabbits to the odour of a predator. Chemoecology 16:25–29

    Article  Google Scholar 

  • Monclús R, Palomares F, Tablado Z, Martínez-Fontúrbel A, Palme R (2009) Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits. Oecologia 158:615–623

    Article  PubMed  Google Scholar 

  • Möstl E, Palme R (2002) Hormones as indicators of stress. Domest Anim Endocrin 23:67–74

    Article  Google Scholar 

  • Möstl E, Rettenbacher S, Palme R (2005) Measurement of corticosterone metabolites in birds' droppings: an analytical approach. Ann NY Acad Sci 1046:17–34

    Article  PubMed  Google Scholar 

  • Navarro–Castilla Á, Barja I (2014) 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, Olea PP, Piñeiro A, Mateo-Tomás P, Silván G, Illera JC (2014) Are degraded habitats from agricultural crops associated with elevated faecal glucocorticoids in a wild population of common vole (Microtus arvalis)? Mamm Biol 79:36–43

    Article  Google Scholar 

  • Navarro–Castilla Á, Mata C, Ruiz-Capillas P, Palme R, Malo JE, Barja I (2014) Are motorways potential stressors of roadside wood mice (Apodemus sylvaticus) populations? PLoS One 9:e91942

    Article  PubMed Central  PubMed  Google Scholar 

  • Newman JA, Recer GM, Zwicker SM, Caraco T (1988) Effects of predation hazard on foraging "constraints": patch-use strategies in grey squirrels. Oikos 53:93–97

    Article  Google Scholar 

  • Orrock JL, Danielson BJ, Brinkerhoff RJ (2004) Rodent foraging is affected by indirect, but not by direct, cues of predation risk. Behav Ecol 15:433–437

    Article  Google Scholar 

  • Padial JM, Ávila E, Sanchez JM (2002) Feeding habits and overlap among red fox (Vulpes vulpes) and stone marten (Martes foina) in two Mediterranean mountain habitats. Mamm Biol 67:137–146

    Article  Google Scholar 

  • Palme R, Touma C, Arias N, Dominchin MF, Lepschy M (2013) Steroid extraction: get the best out of faecal samples. Wien Tierärztl Monat 100:238–246

    Google Scholar 

  • Penteriani V, Kuparinen A, del Mar Delgado M, Palomares F, López-Bao JV, Fedriani JM, Calzada J, Moreno S, Villafuerte R, Campioni L (2013) Responses of a top and a meso predator and their prey to moon phases. Oecologia 173:753–766

    Article  PubMed  Google Scholar 

  • Piñeiro A, Barja I, Silván G, Illera JC (2012) Effects of tourist pressure and reproduction on physiological stress response in wildcats: management implications for species conservation. Wildlife Res 39:532–539

    Article  Google Scholar 

  • Raymer J, Wiesler D, Novotny M, Asa C, Seal US, Mech LD (1984) Volatile constituents of wolf (Canis lupus) urine as related to gender and season. Experientia 40:707–709

    Article  CAS  PubMed  Google Scholar 

  • Reeder DM, Kramer KM (2005) Stress in free-ranging mammals: integrating physiology, ecology, and natural history. J Mammal 86:225–235

    Article  Google Scholar 

  • Scordato ES, Dubay G, Drea CM (2007) Chemical composition of scent marks in the ringtailed lemur (Lemur catta): glandular differences, seasonal variation, and individual signatures. Chem Senses 32:493–504

    Article  CAS  PubMed  Google Scholar 

  • Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166:869–887

    Article  PubMed  Google Scholar 

  • Stoddart DM (1982) Demonstration of olfactory discrimination by the short-tailed vole, Microtus agrestis L. Anim Behav 30:293–294

    Article  Google Scholar 

  • Strier KB, Lynch JW, Ziegler TE (2003) Hormonal changes during the mating and conception seasons of wild northern muriquis (Brachyteles arachnoides hypoxanthus). Am J Primatol 61:85–99

    Article  CAS  PubMed  Google Scholar 

  • Sundell J, Dudek D, Klemme I, Koivisto E, Pusenius J, Ylönen H (2004) Temporal variation of fear and vole behaviour: an experimental field test of the predation risk allocation hypothesis. Oecologia 139:157–162

    Article  PubMed  Google Scholar 

  • Tataranni PA, Larson DE, Snitker S, Young JB, Flatt JP, Ravussin E (1996) Effects of glucocorticoids on energy metabolism and food intake in humans. Am J Physiol-Endoc M 271:317–325

    Google Scholar 

  • Touma C, Palme R (2005) Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann NY Acad Sci 1046:54–74

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Touma C, Palme R, Sachser N (2004) Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Horm Behav 45:10–22

    Article  CAS  PubMed  Google Scholar 

  • Wingfield JC, Hunt K, Breuner C, Dunlap K, Fowler GS, Freed L, Lepson J (1997) Environmental stress, field endocrinology, and conservation biology. In: Clemmons JR, Buchholds R (eds) Behavioral approaches to conservation in the wild. Cambridge University Press, Cambridge, UK, pp 95–131

    Google Scholar 

  • Wolfe JL, Summerlin CT (1989) The influence of lunar light on nocturnal activity of the old-field mouse. Anim Behav 37:410–414

    Article  Google Scholar 

  • Ylönen H, Eccard JA, Jokinen I, Sundell J (2006) Is the antipredatory response in behaviour reflected in stress measured in faecal corticosteroids in a small rodent? Behav Ecol Sociobiol 60:350–358

    Article  Google Scholar 

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Acknowledgments

The authors wish to thank the Comunidad Autónoma of Madrid (Spain) for providing the permits required to conduct this study. We are grateful to Itziar Cabrero for her help in the field, to Cañada Real Open Center, especially to José España, for supplying the red fox faecal material needed to carry out the experiments. We thank Rupert Palme for performing the EIA in the Biochemistry lab at the Vetmeduni Vienna and for his generous revision of this manuscript and making useful comments to improve it. We would also like to thank Edith Klobetz-Rassam and Nino Arias for excellent help with the laboratory analysis. In addition, we would like to thank Dr. Vincenzo Penteriani and an anonymous referee for their useful comments and suggestions to improve this manuscript. Á. Navarro-Castilla was supported by a FPU scholarship from the Ministerio de Educación y Ciencia of Spain.

Ethical standards

In this research, we fulfilled all the regulations concerning to handling and treatment of animals in accordance with the European Communities Council Directives of 24 November 1986 (86/609/EEC) for animal experiments. Manipulations of animals were done under the permit of the Comunidad Autónoma de Madrid (Spain) reference number 10/422505.

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  1. Departamento de Biología, Unidad de Zoología, Facultad de Ciencias, Universidad Autónoma de Madrid, 28049, Madrid, Spain

    Álvaro Navarro-Castilla & Isabel Barja

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  1. Álvaro Navarro-Castilla
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Correspondence to Álvaro Navarro-Castilla.

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Communicated by E. Korpimäki

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Navarro-Castilla, Á., Barja, I. 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 (2014). https://doi.org/10.1007/s00265-014-1759-y

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