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Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Olfactory behavioural responses in captive male southern hairy-nosed wombats (Lasiorhinus latifrons) exposed to oestrous and non-oestrous urine samples

Alyce M. Swinbourne A C D , Stephen D. Johnston A , Tina Janssen B , Allan Lisle A , Tamara Keeley A and Clive J. C. Phillips C
+ Author Affiliations
- Author Affiliations

A Wildlife Science Unit, School of Agriculture and Food Science, The University of Queensland, Gatton, Qld 4343, Australia.

B Australian Animals Care and Education, Mt Larcom, Qld 4695, Australia.

C Centre of Animal Welfare and Ethics, School of Veterinary Science, The University of Queensland, Gatton, Qld 4343, Australia.

D Corresponding author. Email: a.swinbourne@uq.edu.au

Australian Journal of Zoology 64(6) 395-401 https://doi.org/10.1071/ZO16088
Submitted: 9 May 2016  Accepted: 10 March 2017   Published: 5 April 2017

Abstract

Whilst flehmen behaviour has been observed in some marsupials, including the southern hairy-nosed wombat (Lasiorhinus latifrons), it is unknown whether it, or other male-specific behaviours are exhibited differentially in response to the detection of oestrous females, which if proven, could assist in the detection of oestrus in breeding programs for captive southern hairy-nosed wombats. Six captive male southern hairy-nosed wombats were exposed to urine samples collected from a single female that was confirmed to be in oestrus and mid-pregnancy. Urine samples were presented to the males simultaneously and subsequent behaviours recorded for five minutes. There were no significant differences in the number of times flehmen behaviour was displayed in response to oestrous and non-oestrous urine samples (P = 0.577), the number of times the male sniffed each sample (P = 0.595), or the time spent investigating each urine sample (P = 0.414). Our results suggest that neither male flehmen behaviour nor any specific male-related precopulatory behaviour was associated with the olfaction of urine from a female in different stages of the oestrous cycle, and is thus unlikely to be a reliable management tool for the detection of oestrus.


References

Allen, M. L., Wallace, C. F., and Wilmers, C. C. (2015). Patterns in bobcat (Lynx rufus) scent marking and communication behaviors. Journal of Ethology 33, 9–14.
Patterns in bobcat (Lynx rufus) scent marking and communication behaviors.Crossref | GoogleScholarGoogle Scholar |

Apfelbach, R., Blanchard, C. D., Blanchard, R. J., Hayes, R. A., and McGregor, I. S. (2005). The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neuroscience and Biobehavioral Reviews 29, 1123–1144.
The effects of predator odors in mammalian prey species: a review of field and laboratory studies.Crossref | GoogleScholarGoogle Scholar |

Baggott, L. M., Davis-Butler, S., and Moore, H. D. M. (1987). Characterization of oestrus and timed collection of oocytes in the grey short-tailed opossum, Monodelphis domestica. Journal of Reproduction and Fertility 79, 105–114.
Characterization of oestrus and timed collection of oocytes in the grey short-tailed opossum, Monodelphis domestica.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s7ktV2nsA%3D%3D&md5=de5e120a8e77fdd777d80366a7e847d1CAS |

Coulson, G. (1997). Repertoires of social behaviour in captive and free-ranging grey kangaroos, Macropus giganteus and Macropus fuliginosus (Marsupialia: Macropodidae). Journal of Zoology 242, 119–130.
Repertoires of social behaviour in captive and free-ranging grey kangaroos, Macropus giganteus and Macropus fuliginosus (Marsupialia: Macropodidae).Crossref | GoogleScholarGoogle Scholar |

Coulson, G., and Croft, D. (1981). Flehmen in kangaroos. Australian Mammalogy 4, 139–140.

Croft, D. (1982). Some observations on the behaviour of the antilopine wallaroo, Macropus antilopinus (Marsupialia: Macropodidae). Australian Mammalogy 5, 5–13.

Dehnhard, M. (2011). Mammal semiochemicals: understanding pheromones and signature mixtures for better zoo‐animal husbandry and conservation. International Zoo Yearbook 45, 55–79.
Mammal semiochemicals: understanding pheromones and signature mixtures for better zoo‐animal husbandry and conservation.Crossref | GoogleScholarGoogle Scholar |

Descovich, K. A., Lisle, A. T., Johnston, S., Nicolson, V., and Phillips, C. J. C. (2012). Differential responses of captive southern hairy-nosed wombats (Lasiorhinus latifrons) to the presence of faeces from different species and male and female conspecifics. Applied Animal Behaviour Science 138, 110–117.
Differential responses of captive southern hairy-nosed wombats (Lasiorhinus latifrons) to the presence of faeces from different species and male and female conspecifics.Crossref | GoogleScholarGoogle Scholar |

Estes, R. D. (1972). The role of the vomeronasal organ in mammalian reproduction. Mammalia 36, 315–341.
The role of the vomeronasal organ in mammalian reproduction.Crossref | GoogleScholarGoogle Scholar |

Finlayson, G. R., Shimmin, G. A., Temple-Smith, P. D., Handasyde, K., and Taggart, D. A. (2003). Monitoring the activity of a southern hairy-nosed wombat, Lasiorhinus latifrons, using temperature dataloggers. Australian Mammalogy 25, 205–208.
Monitoring the activity of a southern hairy-nosed wombat, Lasiorhinus latifrons, using temperature dataloggers.Crossref | GoogleScholarGoogle Scholar |

Finlayson, G. R., Shimmin, G. A., Taggart, D. A., Skinner, J. F., Gilmore, A., and Paris, M. C. J. (2006). Oestrous cycle of captive southern hairy-nosed wombats (Lasiorhinus latifrons) in South Australia, Australia. Animal Reproduction Science 95, 295–306.
Oestrous cycle of captive southern hairy-nosed wombats (Lasiorhinus latifrons) in South Australia, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xosl2ksbs%3D&md5=0f72b27618d797627eae8fc2dff1f742CAS |

Gansloßer, U. (1979). Soziale interaktionen des Doria-Baumkänguruhs, Dendrolagus dorianus Ramsay, 1833 (Marsupialia, Macropodidae). Zeitschrift für Saugetierkunde 44, 1–18.

Gaughwin, M. D. (1979). The occurrence of flehmen in a marsupial – the hairy-nosed wombat (Lasiorhinus latifrons). Animal Behaviour 27, 1063–1065.
The occurrence of flehmen in a marsupial – the hairy-nosed wombat (Lasiorhinus latifrons).Crossref | GoogleScholarGoogle Scholar |

Gomez‐Diaz, C., and Benton, R. (2013). The joy of sex pheromones. EMBO Reports 14, 874–883.
The joy of sex pheromones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVerurnJ&md5=b4bba8bf3e08a8fce71b107028a47c01CAS |

Hoffmann, F., Musolf, K., and Penn, D. J. (2009). Freezing urine reduces its efficacy for eliciting ultrasonic vocalizations from male mice. Physiology & Behavior 96, 602–605.
Freezing urine reduces its efficacy for eliciting ultrasonic vocalizations from male mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1Ohs70%3D&md5=279679a9bf64b8d55aa19779833f2102CAS |

Hogan, L., Phillips, C., Lisle, A., Horsup, A., Janssen, T., and Johnston, S. (2010a). Reproductive behaviour of the southern-hairy nosed wombat (Lasiorhinus latifrons). Australian Journal of Zoology 58, 350–361.
Reproductive behaviour of the southern-hairy nosed wombat (Lasiorhinus latifrons).Crossref | GoogleScholarGoogle Scholar |

Hogan, L. A., Phillips, C. J. C., Lisle, A., Keeley, T., Horsup, A. B., Janssen, T., and Johnston, S. D. (2010b). Non-invasive methods of oestrus detection in captive southern hairy-nosed wombats (Lasiorhinus latifrons). Animal Reproduction Science 119, 293–304.
Non-invasive methods of oestrus detection in captive southern hairy-nosed wombats (Lasiorhinus latifrons).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktVait7o%3D&md5=95340d136b6b31a3d7c510a707148f1cCAS |

Hogan, L. A., Janssen, T., and Johnston, S. D. (2013). Wombat reproduction (Marsupialia; Vombatidae): an update and future directions for the development of artificial breeding technology. Reproduction 145, R157–R173.
Wombat reproduction (Marsupialia; Vombatidae): an update and future directions for the development of artificial breeding technology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVWmsbnP&md5=0d5b6f22f74b7d7d9d70d488598506f4CAS |

Jackson, S. (2003) Wombats. In ‘Australian Mammals: Biology and Captive Management’. pp. 183–203. (CSIRO Publishing: Melbourne.)

Manley, S. E., Burton, M. E., Fisher, K. E., Cull, C. A., and Turner, R. C. (1992). Decreases in albumin/creatinine and N-acetylglucosaminidase/creatinine ratios in urine samples stored at –20 degrees C. Clinical Chemistry 38, 2294–2299.
| 1:CAS:528:DyaK3sXjtlOk&md5=3d47416700a00ea534290fa0ccccac11CAS |

Marinier, S. L., Alexander, A. J., and Waring, G. H. (1988). Flehmen behaviour in the domestic horse: discrimination of conspecific odours. Applied Animal Behaviour Science 19, 227–237.
Flehmen behaviour in the domestic horse: discrimination of conspecific odours.Crossref | GoogleScholarGoogle Scholar |

Parsons, M. H., and Blumstein, D. T. (2010a). Familiarity breeds contempt: kangaroos persistently avoid areas with experimentally deployed dingo scents. PLoS One 5, e10403.
Familiarity breeds contempt: kangaroos persistently avoid areas with experimentally deployed dingo scents.Crossref | GoogleScholarGoogle Scholar |

Parsons, M. H., and Blumstein, D. T. (2010b). Feeling vulnerable? Indirect risk cues differently influence how two marsupials respond to novel dingo urine. Ethology 116, 972–980.
Feeling vulnerable? Indirect risk cues differently influence how two marsupials respond to novel dingo urine.Crossref | GoogleScholarGoogle Scholar |

Perrin, T. E., and Rasmussen, L. E. L. (1994). Chemosensory responses of female Asian elephants (Elephas maximus) to cyclohexanone. Journal of Chemical Ecology 20, 2857–2866.
Chemosensory responses of female Asian elephants (Elephas maximus) to cyclohexanone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXislertbk%3D&md5=f2e3ca010ba723773505dd62e357120eCAS |

Rajanarayanan, S, and Archunan, G (2004). Occurrence of flehmen in male buffaloes (Bubalus bubalis) with special reference to estrus. Theriogenology 61, 861–866.
Occurrence of flehmen in male buffaloes (Bubalus bubalis) with special reference to estrus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptFahsQ%3D%3D&md5=6582515a78e8284a437b6b33776bb94aCAS |

Rasmussen, L. E., Schmidt, M. J., Henneous, R., Groves, D., and Daves, G. D. (1982). Asian bull elephants: flehmen-like responses to extractable components in female elephant estrous urine. Science 217, 159–162.
Asian bull elephants: flehmen-like responses to extractable components in female elephant estrous urine.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL383itlOktQ%3D%3D&md5=a25487f741dad6fc09ff7e1cf4094637CAS |

Reinhardt, V. (1983). Flehmen, mounting and copulation among members of a semi-wild cattle herd. Animal Behaviour 31, 641–650.
Flehmen, mounting and copulation among members of a semi-wild cattle herd.Crossref | GoogleScholarGoogle Scholar |

Renfree, M. B., Fletcher, T. P., Blanden, D. R., Lewis, P. R., Shaw, G., Gordon, K., Short, R. V., Parer-Cook, E., and Parer, D. (1989). Physiological and behavioural events around the time of birth in macropodid marsupials. In ‘Kangaroos, Wallabies and Rat Kangaroos’. (Eds G. Griggs, P. Jarman and I. Hume.) pp. 323–337. (Surrey Beatty and Sons: Chipping Norton, NSW.)

Sankar, R., and Archunan, G. (2004). Flehmen response in bull: role of vaginal mucus and other body fluids of bovine with special reference to estrus. Behavioural Processes 67, 81–86.
Flehmen response in bull: role of vaginal mucus and other body fluids of bovine with special reference to estrus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MrksFWhsw%3D%3D&md5=dd56fd33bcb8389a50e3d8cb09d25bc9CAS |

SankarGanesh, D., Ramachandran, R., Muniasamy, S., Saravanakumar, V. R., Suriyakalaa, U., Kannan, S., Archunan, G., and Achiraman, S. (2014). A correlation of fecal volatiles and steroid hormone profiles with behavioral expression during estrous cycle of goat, Capra hircus. General and Comparative Endocrinology 206, 178–183.
A correlation of fecal volatiles and steroid hormone profiles with behavioral expression during estrous cycle of goat, Capra hircus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtleiur7O&md5=16acbe7ed86c5660d5d0222c7fa5fb22CAS |

Schaefer, M. L., Yamazaki, K., Osada, K., Restrepo, D., and Beauchamp, G. K. (2002). Olfactory fingerprints for major histocompatibility complex-determined body odors II: relationship among odor maps, genetics, odor composition, and behavior. The Journal of Neuroscience 22, 9513–9521.
| 1:CAS:528:DC%2BD3sXmsVGms7o%3D&md5=fba6e34bca8aa40c778d462e1cf1d12fCAS |

Schneider, N. Y., Fletcher, T. P., Shaw, G., and Renfree, M. B. (2008). The vomeronasal organ of the tammar wallaby. Journal of Anatomy 213, 93–105.
The vomeronasal organ of the tammar wallaby.Crossref | GoogleScholarGoogle Scholar |

Sparrow, E. E., Parsons, M. H., and Blumstein, D. T. (2016). Novel use for a predator scent: preliminary data suggest that wombats avoid recolonising collapsed burrows following application of dingo scent. Australian Journal of Zoology 64, 192–197.
Novel use for a predator scent: preliminary data suggest that wombats avoid recolonising collapsed burrows following application of dingo scent.Crossref | GoogleScholarGoogle Scholar |

Stahlbaum, C. C., and Houpt, K. A. (1989). The role of the flehmen response in the behavioral repertoire of the stallion. Physiology & Behavior 45, 1207–1214.
The role of the flehmen response in the behavioral repertoire of the stallion.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c%2FkslWnsg%3D%3D&md5=ad5383300a63585ed46e18932887d488CAS |

Swaisgood, R. R., Lindburg, D. G., Zhou, X., and Owen, M. A. (2000). The effects of sex, reproductive condition and context on discrimination of conspecific odours by giant pandas. Animal Behaviour 60, 227–237.
The effects of sex, reproductive condition and context on discrimination of conspecific odours by giant pandas.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2sbivFWhsQ%3D%3D&md5=6d84ae3c098547022e9d84543c8b1b02CAS |

Swinbourne, A. M., Janssen, T., Phillips, C. J., and Johnston, S. D. (2015). Non‐invasive urine collection in the female southern hairy‐nosed wombat (Lasiorhinus latifrons) with the aid of classical conditioning. Zoo Biology 34, 89–93.
Non‐invasive urine collection in the female southern hairy‐nosed wombat (Lasiorhinus latifrons) with the aid of classical conditioning.Crossref | GoogleScholarGoogle Scholar |

Taggart, D. A., and Temple-Smith, P. D. (2008). Southern hairy-nosed wombat. In ‘The Mammals of Australia’. (Eds S. Van Dyke and R. Strahan.) pp. 204–206. (New Holland Publishing Pty Ltd.)

Thitaram, C., Chansitthiwet, S., Pongsopawijit, P., Brown, J. L., Wongkalasin, W., Daram, P., Roongsri, R., Kalmapijit, A., Mahasawangkul, S., Rojanasthien, S., Colenbrander, B., Van Der Weijden, G. C., and van Eerdenburg, F. J. C. M. (2009). Use of genital inspection and female urine tests to detect oestrus in captive Asian elephants. Animal Reproduction Science 115, 267–278.
Use of genital inspection and female urine tests to detect oestrus in captive Asian elephants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptl2iu7w%3D&md5=e0774b61a642b26995e97ac62c9a60b2CAS |

Tirindelli, R., Dibattista, M., Pifferi, S., and Menini, A. (2009). From pheromones to behavior. Physiological Reviews 89, 921–956.
From pheromones to behavior.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpslyjsLk%3D&md5=7defea5706cfc6d3485c8557aaf5c2ddCAS |

Weeks, J. W., Crowell-Davis, S. L., and Heusner, G. (2002). Preliminary study of the development of the flehmen response in Equus caballus. Applied Animal Behaviour Science 78, 329–335.
Preliminary study of the development of the flehmen response in Equus caballus.Crossref | GoogleScholarGoogle Scholar |

Wells, D. L. (2009). Sensory stimulation as environmental enrichment for captive animals: a review. Applied Animal Behaviour Science 118, 1–11.
Sensory stimulation as environmental enrichment for captive animals: a review.Crossref | GoogleScholarGoogle Scholar |