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Alarm scent-marking during predatory attempts in the Cabrera vole (Microtus cabrerae Thomas, 1906)

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Ecological Research

Abstract

The alarm pheromones often released by animals under stressful situations seem to elicit behavioral changes in conspecifics, which in the appropriate context can be viewed as anti-predatory responses. However, the releasing of alarm pheromones associated with predatory events has not been demonstrated in mammals. In the current study with wild-caught Cabrera voles, we carried out experiments in the laboratory and in the field to assess the release of alarm pheromones in scent-marks during simulated predatory events and disclose their effects on conspecifics. We first conducted an assay wherein voles where let to scent-mark a clean substrate in the absence of disturbance (control) and under the simulation of predatory events. Contrarily to the control, no fecal boli were released and the area marked with urine was significantly larger during the predatory simulation. In a subsequent assay, we assessed the voles’ preference between urine-marks released under predatory simulation and in control conditions. Voles showed a significant preference by control substrates. Finally, a third assay was carried out in the vole’s habitat wherein the individual activity was monitored by radio-tracking before and after placement of urine-marks obtained during the conditions described above. The vole’s activity was only reduced near the urine-marks released during the simulated predatory events. The results suggest that: (1) during predatory attempts, Cabrera voles release an alarm pheromone in their urine-marks; (2) the putative alarm pheromone reduces the voles’ activity in the surroundings of the marked area; (3) the putative alarm pheromone persists in the field affecting conspecifics’ activity for several days.

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References

  • Abel EL (1991) Alarm substance emitted by rats in the forced-swim test is a low volatile pheromone. Physiol Behav 50:723–727. doi:10.1016/0031-9384(91)90009-d

    Article  PubMed  CAS  Google Scholar 

  • Abel EL (1993) Physiological-effects of alarm chemosignal emitted during the forced swim test. J Chem Ecol 19:2891–2901

    Article  CAS  Google Scholar 

  • Abel EL, Bilitzke PJ (1990) A possible alarm substance in the forced swimming test. Physiol Behav 48:233–239

    Article  PubMed  CAS  Google Scholar 

  • Ackerl K, Atzmueller M, Grammer K (2002) The scent of fear. Neuroendocrinol Lett 23:79–84

    PubMed  Google Scholar 

  • ASAB (2006) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 71:245–253

    Article  Google Scholar 

  • Ashton MC, Paunonen SV, Helmes E, Jackson DN (1998) Kin altruism, reciprocal altruism, and the big five personality factors. Evolut Human Behav 19:243–255. doi:10.1016/s1090-5138(98)00009-9

    Article  Google Scholar 

  • Blum MS (1969) Alarm pheromones. Annu Rev Entomol 14:57–80. doi:10.1146/annurev.en.14.010169.000421

    Article  CAS  Google Scholar 

  • Boissy A, Terlouw C, Le Neindre P (1998) Presence of cues from stressed conspecifics increases reactivity to aversive events in cattle: evidence for the existence of alarm substances in urine. Physiol Behav 63:489–495

    Article  PubMed  CAS  Google Scholar 

  • Brown JS, Laundré JW, Gurung M, Laundre JW (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399. doi:10.2307/1383287

    Article  Google Scholar 

  • Brown GE, Poirier J, Adrian JC (2004) Assessment of local predation risk: the role of subthreshold concentrations of chemical alarm cues. Behav Ecol 15:810–815. doi:10.1093/beheco/arh084

    Article  Google Scholar 

  • Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago

    Google Scholar 

  • Carr WJ, Martorano RD, Krames L (1970) Responses of mice to odors associated with stress. J Comp Physiol Psych 71:223–228. doi:10.1037/h0029164

    Article  CAS  Google Scholar 

  • Chen D, Katdare A, Lucas N (2006) Chemosignals of fear enhance cognitive performance in humans. Chem Senses 31:415–423. doi:10.1093/chemse/bjj046

    Article  PubMed  CAS  Google Scholar 

  • Cocke R, Moynihan JA, Cohen N, Grota LJ, Ader R (1993) Exposure to conspecific alarm chemosignals alters immune-responses in balb/c mice. Brain Behav Immun 7:36–46

    Article  PubMed  CAS  Google Scholar 

  • Creel S (1990) How to measure inclusive fitness. P R Soc London 241:229–231. doi:10.1098/rspb.1990.0090

    Article  CAS  Google Scholar 

  • Desjardins C, Maruniak JA, Bronson FH (1973) Social rank in house mice: differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182:939–941

    Article  PubMed  CAS  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 

  • Fernandez-Salvador R (1998) Topillo de cabrera, Microtus cabrerae Thomas, 1906. Galemys 10:5–18

    Google Scholar 

  • Fernandez-Salvador R, Garcia-Perea R, Ventura J (2001) Reproduction and postnatal growth of the cabrera vole, Microtus cabrerae, in captivity. Can J Zool 79:2080–2085

    Article  Google Scholar 

  • Fernandez-Salvador R, Garcia-Perea R, Ventura J (2005a) Effect of climatic fluctuations on body mass of a Mediterranean vole, Microtus cabrerae. Mamm Biol 70:73–83

    Google Scholar 

  • Fernandez-Salvador R, Ventura J, Garcia-Perea R (2005b) Breeding patterns and demography of a population of the cabrera vole, Microtus cabrerae. Anim Biol 55:147–161

    Article  Google Scholar 

  • Figueiredo HF, Bodie BL, Tauchi M, Dolgas CM, Herman JP (2003) Stress integration after acute and chronic predator stress: differential activation of central stress circuitry and sensitization of the hypothalamo-pituitary-adrenocortical axis. Endocrinology 144:5249–5258

    Article  PubMed  CAS  Google Scholar 

  • Gannon WL, Sikes RS, Mammalogists ACaUCotASo (2007) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 88:809–823

    Article  Google Scholar 

  • Gray SJ, Hurst JL, Stidworthy R, Smith J, Preston R, MacDougall R (1998) Microhabitat and spatial dispersion of the grassland mouse (Mus spretus Lataste). J Zool 246:299–308

    Article  Google Scholar 

  • Gutierrez-Garcia AG, Contreras CM, Mendoza-Lopez MR, Garcia-Barradas O, Cruz-Sanchez S (2007) Urine from stressed rats increases immobility in receptor rats forced to swim: role of 2-heptanone. Physiol Behav 91:166–172

    Article  PubMed  CAS  Google Scholar 

  • Halpern M (1992) Nasal chemical senses in reptiles: structure and function. In: Gans C, Crews D (eds) Biology of the reptilia, physiology E, hormones, brain, and behavior, 2nd edn. University of Chicago Press, Chicago, pp 423–523

    Google Scholar 

  • Hauser R, Wiergowski M, Marczak M, Karaszewski B, Wodniak-Ochocinska L (2005) Alarm pheromones as an exponent of emotional state shortly before death - Science fiction or a new challenge? Forensic Sci Int 155:226–230

    Article  PubMed  CAS  Google Scholar 

  • Hauser R et al (2008) A preliminary study for identifying olfactory markers of fear in the rat. Lab Animal 37:76–80

    Article  PubMed  Google Scholar 

  • Hemson G, Johnson PJ, South A, Kenward RE, Ripley R, Macdonald D (2005) Are kernels the mustard? Data from global positioning system (GPS) collars suggests problems for kernel home-range analyses with least-squares cross-validation. J Anim Ecol 74:455–463. doi:10.1111/j.1365-2656.2005.00944.x

    Article  Google Scholar 

  • Hendrie CA, Weiss SM, Eilam D (1998) Behavioural response of wild rodents to the calls of an owl: a comparative study. J Zool 245:439–446. doi:10.1017/S0952836998008073

    Article  Google Scholar 

  • Hews DK (1988) Alarm response in larval western toads, Bufo boreas: release of larval chemicals by a natural predator and its effect on predator capture efficiency. Anim Behav 36:125–133. doi:10.1016/s0003-3472(88)80255-0

    Article  Google Scholar 

  • Hollén LI, Radford AN (2009) The development of alarm call behaviour in mammals and birds. Animal Behav 78:791–800. doi:10.1016/j.anbehav.2009.07.021

    Article  Google Scholar 

  • Hrbáček J (1950) On the flight reaction of tadpoles of the common toad caused by chemical substances. Cell Mol Life Sci 6:100–102. doi:10.1007/bf02153372

    Article  Google Scholar 

  • Kavaliers M, Choleris E (2001) Antipredator responses and defensive behavior: ecological and ethological approaches for the neurosciences. Neurosci Biobehav R 25:577–586. doi:10.1016/s0149-7634(01)00042-2

    Article  CAS  Google Scholar 

  • Kikusui T, Takigami S, Takeuchi Y, Mori Y (2001) Alarm pheromone enhances stress-induced hyperthermia in rats. Physiol Behav 72:45–50

    Article  PubMed  CAS  Google Scholar 

  • Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y (2004a) Alarm pheromones with different functions are released from different regions of the body surface of male rats. Chem Senses 29:35–40. doi:10.1093/chemse/bjh004

    Article  PubMed  Google Scholar 

  • Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y (2004b) Modulatory role of testosterone in alarm pheromone release by male rats. Horm Behav 45:122–127

    Article  PubMed  CAS  Google Scholar 

  • Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y (2005) Alarm pheromone that aggravates stress-induced hyperthermia is soluble in water. Chem Senses 30:513–519

    Article  PubMed  CAS  Google Scholar 

  • Kiyokawa Y, Shimozuru M, Kikusui T, Takeuchi Y, Mori Y (2006) Alarm pheromone increases defensive and risk assessment behaviors in male rats. Physiol Behav 87:383–387

    Article  PubMed  CAS  Google Scholar 

  • Lawrence B, Smith R (1989) Behavioral response of solitary fathead minnows, Pimephales promelas, to alarm substance. J Chem Ecol 15:209–219. doi:10.1007/bf02027783

    Article  Google Scholar 

  • Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. In: Møller AP, Milinski M, Slater PJB (eds) Advances in studies of behavior. Academic Press, London, pp 215–290

    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. doi:10.1139/z90-092

    Article  Google Scholar 

  • Lind J, Cresswell W (2005) Determining the fitness consequences of antipredation behavior. Behav Ecol 16:945–956. doi:10.1093/beheco/ari075

    Article  Google Scholar 

  • Mackaysim A, Laing DG (1981) The sources of odors from stressed rats. Physiol Behav 27:511–513

    Article  CAS  Google Scholar 

  • Mackay-Sim A, Laing DG (1980) Discrimination of odors from stressed rats by non-stressed rats. Physiol Behav 24:699–704. doi:10.1016/0031-9384(80)90400-x

    Article  PubMed  CAS  Google Scholar 

  • Mathis A, Smith RJF (1992) Avoidance of areas marked with a chemical alarm substance by fathead minnows (Pimephales promelas) in a natural habitat. Can J Zool 70:1473–1476

    Article  Google Scholar 

  • Mathis A, Smith RJ (1993) Chemical alarm signals increase the survival time of fathead minnows (Pimephales promelas) during encounters with northern pike (Esox Lucius). Behav Ecol 4:260–265. doi:10.1093/beheco/4.3.260

    Article  Google Scholar 

  • Mathis A, Chivers DP, Smith R (1995) Chemical alarm signals: predator deterrents or predator attractants? Am Nat 145:994–1005

    Article  Google Scholar 

  • Mira A, Marques CC, Santos SM, Rosario IT, Mathias ML (2008) Environmental determinants of the distribution of the cabrera vole (Microtus cabrerae) in Portugal: implications for conservation. Mamm Biol 73:102–110. doi:10.1016/j.mambio.2006.11.003

    Google Scholar 

  • Moser JC, Brownlee RC, Silverstein R (1968) Alarm pheromones of the ant Atta texana. J Insect Physiol 14:529–535. doi:10.1016/0022-1910(68)90068-1

    Article  PubMed  CAS  Google Scholar 

  • Palomo LJ, Gisbert J (2002) Atlas de los mamíferos terrestres de espanã. Dirección general de conservación de la naturaleza. SECEM, SECEMU, Madrid

    Google Scholar 

  • Pita R, Mira A, Beja P (2006) Conserving the cabrera vole, Microtus cabrerae, in intensively used Mediterranean landscapes. Agr Ecosyst Environ 115:1–5

    Article  Google Scholar 

  • Pita R, Beja P, Mira A (2007) Spatial population structure of the cabrera vole in Mediterranean farmland: the relative role of patch and matrix effects. Biol Conserv 134:383–392

    Article  Google Scholar 

  • Pita R, Mira A, Beja P (2010) Spatial segregation of two vole species (Arvicola sapidus and Microtus cabrerae) within habitat patches in a highly fragmented farmland landscape. Eur J Wildlife Res 56:651–662. doi:10.1007/s10344-009-0360-6

    Article  Google Scholar 

  • Preisser EL, Bolnick DI (2008) The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. PLoS One 3:e2465. doi:10.1371/journal.pone.0002465

    Article  PubMed  Google Scholar 

  • Price EO (1999) Behavioral development in animals undergoing domestication. Appl Anim Behav Sci 65:245–271

    Article  Google Scholar 

  • Ramos A, Mormède P (1997) Stress and emotionality: a multidimensional and genetic approach. Neurosci Biobehav R 22:33–57. doi:10.1016/s0149-7634(97)00001-8

    Article  Google Scholar 

  • Rottman SJ, Snowdon CT (1972) Demonstration and analysis of an alarm pheromone in mice. J Comp Physiol Psych 81:483–490

    Article  CAS  Google Scholar 

  • Santos SM, Do Rosario IT, Mathias ML (2005) Microhabitat preference of the cabrera vole in a Mediterranean cork oak woodland of southern Portugal. Vie Milieu 55:53–59

    Google Scholar 

  • Santos SM, Mathias MDL, Mira A, Simoes MP (2007) Vegetation structure and composition of road verge and meadow sites colonized by cabrera vole (Microtus Cabrerae Thomas). Pol J Ecol 55:481–493

    Google Scholar 

  • Sherman PW (1977) Nepotism and the evolution of alarm calls. Science 197:1246–1253. doi:10.1126/science.197.4310.1246

    Article  PubMed  CAS  Google Scholar 

  • Sherman PW (1985) Alarm calls of Belding's ground squirrels to aerial predators: nepotism or self-preservation? Behav Ecol Sociobiol 17:313–323. doi:10.1007/bf00293209

    Article  Google Scholar 

  • Smith RJF (1986) Evolution of alarm signals: role of benefits of retaining group members or territorial neighbors. Am Nat 128:604–610

    Article  Google Scholar 

  • Smith J, Hurst JL, Barnard CJ (1994) Comparing behaviour in wild and laboratory strains of the house mouse: levels of comparison and functional inference. Behav Process 32:79–86. doi:10.1016/0376-6357(94)90029-9

    Article  Google Scholar 

  • Taché Y, Martinez V, Million M, Wang LW (2001) III. Stress-related alterations of gut motor function: role of brain corticotropin-releasing factor receptors. Am J Physiol 280:G173–G177

    Google Scholar 

  • Taylor RJ, Balph DF, Balph MH (1990) The evolution of alarm calling: a cost–benefit analysis. Animal Behav 39:860–868. doi:10.1016/s0003-3472(05)80950-9

    Article  Google Scholar 

  • Trivers RL (1971) The evolution of reciprocal altruism. Q Rev Biol 46:35–57

    Article  Google Scholar 

  • Valenta JG, Rigby MK (1968) Discrimination of the odor of stressed rats. Science 161:599–601

    Article  PubMed  CAS  Google Scholar 

  • Vieuille-Thomas C, Signoret JP (1992) Pheromonal transmission of an aversive experience in domestic pig. J Chem Ecol 18:1551–1557

    Article  Google Scholar 

  • Williams GC (1964) Measurement of consociation among fishes and comments on the evolution of schooling. Michigan State University Museum, East Lansing

    Google Scholar 

  • Williams GC (1992) Natural selection: domains, levels, and challenges. Oxford University Press, Oxford

    Google Scholar 

  • Wilson EO (1975) Enemy specification in the alarm-recruitment system of an ant. Science 190:798–800. doi:10.1126/science.1198097

    Article  PubMed  CAS  Google Scholar 

  • Witkin SR, Fitkin MS (1979) Chickadee alarm calls: does mate investment pay dividends? Anim Behav 27:1275–1276

    Article  Google Scholar 

  • Wu G-M, Boivin G, Brodeur J, Giraldeau L-A, Outreman Y (2010) Altruistic defence behaviours in aphids. BMC Evol Biol 10:1–10. doi:10.1186/1471-2148-10-19

    Article  CAS  Google Scholar 

  • Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Zalaquett C, Thiessen D (1991) The effects of odors from stressed mice on conspecific behavior. Physiol Behav 50:221–227

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was funded by the Portuguese Foundation for Science and Technology through a PhD grant awarded to LG (SFRH/BD/23699/2005). Further support was provided by a grant awarded to LG by the University of Évora – Programa Bento de Jesus Caraça. Capture and handling of voles were conducted with the permission of the Portuguese nature conservation authority (ICNB). We are grateful to Pedro Salgado for his assistance in field data collection. We are also grateful to Professor Alfredo Pereira for providing access to the space where the laboratory experiments were carried out.

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Authors and Affiliations

  1. Grupo de Ecossistemas e Paisagens Mediterrânicas, Instituto de Ciências Agrárias e Ambientais Mediterrânicas, Universidade de Évora, Núcleo da Mitra, Apartado 94, 7002-554, Évora, Portugal

    Luis Alexandre Piteira Gomes

  2. Unidade de Biologia da Conservação, Universidade de Évora, Núcleo da Mitra, Apartado 94, 7002-554, Évora, Portugal

    Luis Alexandre Piteira Gomes, Pedro Miguel Pedreirinho Salgado & António Paulo Pereira Mira

  3. Departamento de Biologia, Universidade de Évora, Apartado 94, 7002-554, Évora, Portugal

    Eduardo Nuno Barata

  4. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Pólo de, Évora, Portugal

    António Paulo Pereira Mira

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  1. Luis Alexandre Piteira Gomes
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  2. Pedro Miguel Pedreirinho Salgado
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  3. Eduardo Nuno Barata
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  4. António Paulo Pereira Mira
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Correspondence to Luis Alexandre Piteira Gomes.

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Gomes, L.A.P., Salgado, P.M.P., Barata, E.N. et al. Alarm scent-marking during predatory attempts in the Cabrera vole (Microtus cabrerae Thomas, 1906). Ecol Res 28, 335–343 (2013). https://doi.org/10.1007/s11284-012-1023-8

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