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Murid stress odours: a review and a ‘low tech’ method of collection

Published online by Cambridge University Press:  01 January 2023

GJ Mason*
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Ontario N1G 2W1, Canada
J Dallaire
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Ontario N1G 2W1, Canada
N Ware
Affiliation:
St. Peter's College, Oxford University, New Inn Hall Street, Oxford OX1 2DL, UK
*
* Contact for correspondence and requests for reprints: [email protected]
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Abstract

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Stress cues can affect the welfare of animals in close proximity and are possibly useful non-invasive indicators of the emitters’ welfare. To facilitate their study in murids, we tested whether rats’ stress odours could be collected and stored using an enfleurage-type technique. ‘Donor’ rats were individually exposed to a compound stressor (carried circa 75 m inside a novel container, then euthanised with rising carbon dioxide) while on blotting paper dotted with melted vegetable lard. These sheets were sealed, left at room temperature for 2-5 h, and then ‘bioassayed’ by a blind observer for their effects on conspecifics. Compared with control sheets (exposed to unstressed rats, to CO2 alone, or untreated), stress-exposed sheets significantly affected the unconditioned behaviour of 16 pairs of detector rats trained to enter an arena from their home cage to obtain sucrose. When used to line this arena, the stress-exposed sheets significantly increased: i) rats’ latencies to eat, to place front feet into, and to completely step into the arena and ii) shuttling movements between arena and home cage. These pilot data thus suggest that odours produced by stressed rats can be simply and successfully collected and stored for several hours, though certain potential confounds (eg urine volume) may conceivably be alternative explanations for the observed effects. Future work should control for urine volume, and assess whether fat is needed for optimal odour absorption by paper and for how long sheets can be stored at various temperatures. Much fundamental work is also still needed on the nature, functions, and sources of stress odours.

Type
Research Article
Copyright
© 2009 Universities Federation for Animal Welfare

References

Abel, EL 1991 Gradient of alarm substance in the forced swimming test. Physiology & Behavior 49: 321323CrossRefGoogle ScholarPubMed
Abel, EL 1992 Response to alarm substance in different rat strains. Physiology & Behavior 51: 345347CrossRefGoogle ScholarPubMed
Abel, EL and Bilitzke, PJ 1990 A possible alarm substance in the forced swimming test. Physiology & Behavior 48: 233239CrossRefGoogle ScholarPubMed
Abel, EL, Bilitzke, PJ and Cotton, DB 1992 Alarm substance induces convulsions in imipramine-treated rats. Pharmacology Biochemistry and Behavior 41: 599601CrossRefGoogle ScholarPubMed
Aoyama, K and Okaichi, H 1994 The influence of conspecific distress responses on the lever choice behavior in the rat. Japanese Journal of Psychology 65: 286294Google ScholarPubMed
Axel, R and Dulac, C 1995 A novel family of genes encoding putative pheromone receptors in mammals. Cell 83: 195206Google Scholar
Balcombe, JP, Barnard, ND and Sandusky, C 2004 Laboratory routines cause animal stress. Contemporary Topics in Laboratory Animal Science 43: 4251Google ScholarPubMed
Bishop, J, McKay, H, Parrott, D and Allan, J 2003 Review of International Research Literature Regarding the Effectiveness of Auditory Bird Scaring Techniques and Potential Alternatives. DEFRA: London, UKGoogle Scholar
Blanchard, RJ, Blanchard, DC, Weiss, SM and Meyer, S 1990 The effects of ethanol and diazepam on reactions to predatory odors. Pharmacology Biochemistry & Behavior 35: 775780CrossRefGoogle ScholarPubMed
Blumstein, DT 2007 The evolution of alarm communication in rodents: Structure, function, and the puzzle of apparently altruistic calling. In: Wolff, JO and Sherman, PW (eds) Rodent Societies: An Ecological & Evolutionary Perspective pp 317327. University of Chicago Press: Chicago, USAGoogle Scholar
Boissy, A, Terlouw, C and Le Neindre, P 1998 Presence of cues from stressed conspecifics increased reactivity to aversive events in cattle: evidence for the existence of alarm substances in urine. Physiology & Behaviour 63: 489495CrossRefGoogle ScholarPubMed
Brown, RE 1992 Responses of dominant and subordinate male rats to the odors of male and female conspecifics. Aggressive Behavior 18: 1291383.0.CO;2-U>CrossRefGoogle Scholar
Brown, GE, Godin, JGJ and Pedersen, J 1999 Fin-flicking behaviour: a visual antipredator alarm signal in a characin fish, Hemmigrammus erythrozonus. Animal Behaviour 58: 469475CrossRefGoogle Scholar
Brown, GE, Poirier, JF and Adrian, JC 2004 Assessment of local predation risk - the role of subthreshold concentrations of chemical alarm cues. Behavioural Ecology 15: 810815CrossRefGoogle Scholar
Burn, CC 2008 What is it like to be a rat? Rat sensory perception and its implications for experimental design and rat welfare. Applied Animal Behaviour Science 112: 132CrossRefGoogle Scholar
Burn, CC and Mason, GJ 2008 Rats seem indifferent between their own scent-marked homecages and clean cages. Applied Animal Behaviour Science 115: 201210CrossRefGoogle Scholar
Burn, CC, Peters, A and Mason, GJ 2006 Acute effects of cage cleaning at different frequencies on laboratory rat behaviour and welfare. Animal Welfare 15: 161171Google Scholar
Carr, WJ, Martorano, RD and Krames, L 1970 Responses of mice to odours associated with stress. Journal of Comparative and Physiological Psychology 71: 223228CrossRefGoogle ScholarPubMed
Cocke, R, Moynihan, JA, Cohen, N, Grota, LJ and Ader, R 1993 Exposure to conspecific alarm chemosignals alters immune response in BALB/c mice. Brain, Behavior, and Immunity 7: 3646CrossRefGoogle ScholarPubMed
Cook, A, Rushton, S, Allan, J and Baxter, A 2008 An evaluation of techniques to control problem bird species on landfill sites. Environmental Management 41: 834843CrossRefGoogle ScholarPubMed
Covington, HE and Miczek, KA 2003 Vocalizations during withdrawal from opiates and cocaine: possible expressions of affective distress. European Journal of Pharmacology 467: 113CrossRefGoogle ScholarPubMed
Dua, JK and Dobson, MJ 1975 Gradients of olfactory cues in avoidance. Effect of shock intensity and duration of shock. Indian Journal of Psychology 50: 122132Google Scholar
Dunstone, N 1993 The Natural History of Mink. T & AD Poyser: London, UKGoogle Scholar
Dupuch, A, Magnan, P and Dill, LM 2004 Sensitivity of northern redbelly dace, Phoxinus eos, to chemical alarm cues. Canadian Journal of Zoology 82: 407415CrossRefGoogle Scholar
Fanselow, MS 1985 Odors released by stressed rats produce opioid analgesia in unstressed rats. Behavioral Neuroscience 99: 589592CrossRefGoogle ScholarPubMed
Grandin, T 1998 The feasibility of using vocalization scoring as an indicator of poor welfare during cattle slaughter. Applied Animal Behaviour Science 56: 121128CrossRefGoogle Scholar
Grandin, T 2001 Cattle vocalizations are associated with handling and equipment problems at beef slaughter plants. Applied Animal Behaviour Science 71: 191201CrossRefGoogle ScholarPubMed
Haley, DB, Bailey, DW and Stookey, JM 2005 The effects of weaning beef calves in two stages on their behavior and growth rate. Journal of Animal Science 83: 22052214CrossRefGoogle ScholarPubMed
Hawkins, P, Playle, L, Golledge, H, Leach, M, Banzett, R, Coenen, A, Cooper, J, Danneman, P, Flecknell, P, Kirkden, R, Niel, L and Raj, M 2006 Newcastle consensus meeting on carbon dioxide euthanasia of laboratory animals. Animal Technology & Welfare 5: 125134Google Scholar
Hucko, JA and Cupp, PV 2001 Avoidance of chemical alarm cues released from autotomized tails of ravine salamanders (Plethodon richmondi). Ethology 107: 315322CrossRefGoogle Scholar
Hughes, WOH, Howse, PE, Vilela, EF and Goulson, D 2001 The response of grass-cutting ants to natural and synthetic versions of their alarm pheromone. Physiological Entomology 26: 165172CrossRefGoogle Scholar
Hurst, JL, Payne, CE, Nevison, CM, Marie, AD, Humphries, RE, Robertson, DHL, Cavagioni, A and Beynon, RJ 2001 Individual recognition in mice mediated by major urinary proteins. Nature 414: 631634CrossRefGoogle ScholarPubMed
Inagaki, H, Kiyokawa, Y, Kikusui, T, Takeuchi, Y and Mori, Y 2008 Enhancement of the acoustic startle reflex by an alarm pheromone in male rats. Physiology & Behavior 93: 606611CrossRefGoogle ScholarPubMed
Kavaliers, M, Fudge, MA, Colwell, DD and Choleris, E 2003 Aversive and avoidance responses of female mice to the odors of males infected with an ectoparasite and the effects of prior familiarity. Behavioral Ecology and Sociobiology 54: 423430CrossRefGoogle Scholar
Kikusui, T, Takigami, S, Takeuchi, Y and Mori, Y 2001 Alarm pheromone enhances stress-induced hyperthermia in rats. Physiology & Behaviour 72: 4550CrossRefGoogle ScholarPubMed
Kiriazis, J and Slobodchikoff, CN 2006 Perceptual specificity in the alarm calls of Gunnison's prairie dogs. Behavioural Processes 73: 2935CrossRefGoogle ScholarPubMed
Kiyokawa, Y, Kikusui, T, Takeuchi, Y and Mori, Y 2004 Alarm pheromones with different functions are released from different regions of the body surface of male rats. Chemical Senses 29: 3540CrossRefGoogle ScholarPubMed
Kiyokawa, Y, Kikusui, T, Takeuchi, Y and Mori, Y 2005 Alarm pheromone that aggravates stress-induced hyperthermia is soluble in water. Chemical Senses 30: 513519CrossRefGoogle ScholarPubMed
Krams, I, Krama, T and Igaune, K 2006 Mobbing behaviour: reciprocity-based co-operation in breeding Pied Flycatchers Ficedula hypoleuca. Ibis 48: 5054CrossRefGoogle Scholar
Latham, N and Mason, G 2004 From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory. Applied Animal Behaviour Science 86: 261289CrossRefGoogle Scholar
Leach, MC, Bowell, VA, Allan, TF and Morton, DB 2002a Aversion to gaseous euthanasia agents in rats and mice. Comparative Medicine 52: 249257Google Scholar
Leach, MC, Bowell, VA, Allan, TF and Morton, DB 2002b Degrees of aversion shown by rats and mice to different concentrations of inhalational anaesthetics. Veterinary Record 150: 808815CrossRefGoogle Scholar
Ma, M 2007 Encoding olfactory signals via multiple chemosensory systems. Critical Reviews in Biochemistry and Molecular Biology 42: 463480CrossRefGoogle ScholarPubMed
Mackay-Sim, A and Laing, DG 1980 Discrimination of odours from stressed rats by non-stressed rats. Physiology & Behaviour 24: 699704CrossRefGoogle ScholarPubMed
Mackay-Sim, A and Laing, DG 1981a Rats’ responses to blood and body odours of stressed and non-stressed conspecifics. Physiology & Behaviour 27: 503510CrossRefGoogle Scholar
Mackay-Sim, A and Laing, DG 1981b The sources of odours from stressed rats. Physiology & Behaviour 27: 511513CrossRefGoogle Scholar
Manser, MB, Bell, MB and Fletcher, LB 2001 The information that receivers extract from alarm calls in suricates. Proceedings of the Royal Society of London B 268: 24852491CrossRefGoogle ScholarPubMed
Manteuffel, G, Puppe, B and Schön, PC 2004 Vocalization of farm animals as a measure of welfare. Applied Animal Behaviour Science 88: 163182Google Scholar
Mason, G and Littin, KE 2003 The humaneness of rodent pest control. Animal Welfare 12: 137Google Scholar
Mason, G, Wilson, D, Hampton, C and Würbel, H 2004 Non-invasively assessing disturbance and stress in laboratory rats by scoring chromodacryorrhoea. Alternatives to Laboratory Animals 32: S153S159CrossRefGoogle ScholarPubMed
Maynard-Smith, J and Harper, D 2003 Animal Signals. Oxford University Press: Oxford, UKGoogle Scholar
Miczek, KA, Weerts, EM, Vivian, JA and Barros, HM 1995 Aggression, anxiety and vocalizations in animals: GABAa and 5-HT anxiolytics. Psychopharmacology 121: 3856CrossRefGoogle ScholarPubMed
Morgan, PA and Howse, PE 1973 Avoidance conditioning of jackdaws (Corvus monedula) to distress calls. Animal Behaviour 21: 481491CrossRefGoogle Scholar
Moynihan, JA, Karp, D, Cohen, N and Cocke, R 1994 Alterations in interleukin-4 and antibody production following pheromone exposure: role of glucocorticoids. Journal of Neuroimmunology 54: 5158CrossRefGoogle ScholarPubMed
Moynihan, JA, Karp, JD, Cohen, N and Ader, R 2000 Immune deviation following stress odor exposure: role of endogenous opioids. Journal of Neuroimmunology 102: 145153CrossRefGoogle ScholarPubMed
Müller-Velten, H 1966 Über den Angstgeruch bei der Hausmaus (Mus musculus L). Zeitschrift fur Vergleichende Physiologie 52: 401429. [Title translation: Concerning ‘fear odour’ in the house mouse]Google Scholar
Niel, L and Weary, DM 2006a Behavioral responses of rats to gradual-fill carbon dioxide euthanasia and reduced oxygen concentrations. Applied Animal Behavior Science 100: 295308CrossRefGoogle Scholar
Niel, L and Weary, DM 2006b Rats avoid exposure to carbon dioxide and argon. Applied Animal Behavior Science 107: 100109CrossRefGoogle Scholar
Pitman, DL, Ottenweller, JE and Natelson, BH 1988 Plasma corticosterone levels during repeated presentation of two intensities of restraint stress: chronic stress and habituation. Physiology & Behavior 43: 4755CrossRefGoogle ScholarPubMed
Rajchard, J 2006 Antipredator pheromones in amphibians: a review. Veterinarni Medicina 51: 409413CrossRefGoogle Scholar
Randall, JA and Rogovin, KA 2002 Variation in and meaning of alarm calls in a social desert rodent Rhombomys opimus. Ethology 108: 513527CrossRefGoogle Scholar
Rimmel, E 1865 The Book of Perfumes. Chapman and Hall: London, UKGoogle Scholar
Rottman, SJ and Snowdon, CT 1972 Demonstration and analysis of an alarm pheromone in mice. Journal of Comparative and Physiological Psychology 81: 483490CrossRefGoogle ScholarPubMed
Russ, JM, Racey, PA and Jones, G 1998 Intraspecific responses to distress calls of the pipistrelle bat, Pipistrellus pipistrellus. Animal Behaviour 55: 705713CrossRefGoogle ScholarPubMed
Spanier, E 1980 The use of distress calls to repel night herons (Nycticorax nycticorax) from fish ponds. Journal of Applied Ecology 17: 287294CrossRefGoogle Scholar
Stevens, DA and Gerzog-Thomas, DA 1977 Fright reactions in rats to conspecific tissue. Physiology & Behaviour 18: 4751CrossRefGoogle ScholarPubMed
Süskind, P 1986 Perfume: The Story of a Murderer. Penguin: London, UKGoogle Scholar
Taylor, RD and Ludvigson, HW 1987 Airborne differences in odors emitted by Rattus norvegicus in response to reward and non-reward. Journal of Chemical Ecology 13: 11471161Google Scholar
Taylor, AA and Weary, DM 2000 Vocal responses of piglets to castration: identifying procedural sources of pain. Applied Animal Behaviour Science 70: 1726Google ScholarPubMed
Vieuille-Thomas, C and Signoret, JP 1992 Pheromonal transmission of an aversive experience in domestic pig. Journal of Chemical Ecology 18: 15511557CrossRefGoogle ScholarPubMed
Watts, JM and Stookey, JM 2000 Vocal behaviour in cattle: the animal's commentary on its biological processes and welfare. Applied Animal Behaviour Science 67: 1533CrossRefGoogle ScholarPubMed
Weary, DM, Braithwaite, LA and Fraser, D 1998 Vocal response to pain in piglets. Applied Animal Behaviour Science 56: 161172CrossRefGoogle Scholar
Weary, DM and Fraser, D 1995 Signalling need: costly signals and animal welfare assessment. Applied Animal Behaviour Science 44: 159169CrossRefGoogle Scholar
Willis, C and Poulin, R 2000 Preference of female rats for the odours of non-parasitised males: the smell of good genes? Folia Parasitologica 47: 610CrossRefGoogle ScholarPubMed
Wilson, EO 1965 Chemical communication in social insects. Science 149: 10641071CrossRefGoogle ScholarPubMed
Zala, SM, Potts, WK and Penn, DJ 2004 Scent-marking displays provide honest signals of health and infection. Behavioral Ecology 15: 338344CrossRefGoogle Scholar
Zalaquett, C and Thiessen, D 1991 The effects of odors from stressed mice on conspecific behaviour. Physiology & Behaviour 50: 221227Google Scholar