Is There a Link between Vomeronasalitis and Aggression in Stable Social Groups of Female Pigs?

Simple Summary The vomeronasal organ plays a key role in intraspecific animal behavior since it is able to detect pheromones. Induced and spontaneous lesions of this structure have been previously associated with various social behavior alterations in animals. In cats, the inflammation of this organ, named vomeronasalitis, has been associated with the presence of aggression towards other cats. The aim of this study was to describe this pathology in farm pigs and to evaluate if it is associated with social alterations as described in cats. Our study showed that farm pigs can be affected by the inflammation of the vomeronasal organ and that the pigs with this alteration present an increased number of skin lesions induced by fights with other pigs. These results open an interesting perspective that links the alteration of this organ to the presence of aggressive behaviors in farm animals, which implicates an important issue in animal welfare. Abstract The vomeronasal organ (VNO) is a bilateral chemosensory structure strongly involved in animal behaviour, thanks to its sensory epithelium (VNSE) that detects pheromones. Experimental VNO lesions can impair social, reproductive and maternal behaviour, while feline spontaneous vomeronasalitis has been associated with aggression. This study aimed to describe vomeronasalitis in farm pigs and explore its association with intraspecific behavioural alterations. Using 38 six-month-old pigs, the skin lesion score based on Welfare Quality® protocols was obtained during the fattening period. The seventy-six VNOs from these pigs were stained in haematoxylin-eosin for histological examinations. VNSE inflammation was classified considering its intensity. Skin lesions data were compared to vomeronasalitis. There were 34% of pigs that showed unilateral VNSE inflammation, while 66% were bilaterally affected. The mean ± SD number of skin lesions/animal was 4.4 ± 2.82, and 34% of pigs scored 1 (moderately wounded animals) at least once during the fattening period. Statistical analysis showed an association between bilateral vomeronasalitis and skin lesion score (p < 0.05) and between bilateral moderate vomeronasalitis and skin lesions number (p < 0.01). This is the first report linking vomeronasalitis to social life in farm animals. Considering the role of social life in animal welfare, our data opens a research field linking pathology to animal behaviour.

[1]  J. L. Rois,et al.  Does a third intermediate model for the vomeronasal processing of information exist? Insights from the macropodid neuroanatomy , 2021, Brain Structure and Function.

[2]  P. Pageat,et al.  Histological and Immunohistochemical Characterization of Vomeronasal Organ Aging in Mice , 2021, Animals : an open access journal from MDPI.

[3]  A. Szumny,et al.  MRI Features of the Vomeronasal Organ in Dogs (Canis Familiaris) , 2020, Frontiers in Veterinary Science.

[4]  A. Poli,et al.  Pathology and behaviour in feline medicine: investigating the link between vomeronasalitis and aggression , 2016, Journal of feline medicine and surgery.

[5]  Trese Leinders-Zufall,et al.  Signaling mechanisms and behavioral function of the mouse basal vomeronasal neuroepithelium , 2014, Front. Neuroanat..

[6]  T. Wyatt Pheromones and Animal Behavior: Chemical Signals And Signatures , 2014 .

[7]  C. Mucignat-Caretta Vomeronasal Organ: A Short History of Discovery and an Account of Development and Morphology in the Mouse -- Neurobiology of Chemical Communication , 2014 .

[8]  R. Henkin,et al.  Interleukin 6 in hyposmia. , 2013, JAMA otolaryngology-- head & neck surgery.

[9]  D. Creasy,et al.  Evaluation of the Rabbit Nasal Cavity in Inhalation Studies and a Comparison with Other Common Laboratory Species and Man , 2011, Toxicologic pathology.

[10]  E. Webb,et al.  Effect of Blockage of the Ducts of the Vomeronasal Organ on LH Plasma Levels during the “Whitten Effect” in Does , 2010, Veterinary medicine international.

[11]  R. Reed,et al.  Reversible Loss of Neuronal Marker Protein Expression in a Transgenic Mouse Model for Sinusitis-Associated Olfactory Dysfunction , 2010, American journal of rhinology & allergy.

[12]  R. Reed,et al.  A Genetic Model of Chronic Rhinosinusitis-Associated Olfactory Inflammation Reveals Reversible Functional Impairment and Dramatic Neuroepithelial Reorganization , 2010, The Journal of Neuroscience.

[13]  R Roehe,et al.  Genetic validation of postmixing skin injuries in pigs as an indicator of aggressiveness and the relationship with injuries under more stable social conditions. , 2009, Journal of animal science.

[14]  J. Cherry,et al.  Effect of vomeronasal organ removal from male mice on their preference for and neural Fos responses to female urinary odors. , 2006, Behavioral neuroscience.

[15]  Alistair Lawrence,et al.  The accumulation of skin lesions and their use as a predictor of individual aggressiveness in pigs , 2006 .

[16]  P. Nagnan-Le Meillour,et al.  Functional characterization of olfactory binding proteins for appeasing compounds and molecular cloning in the vomeronasal organ of pre-pubertal pigs. , 2003, Chemical senses.

[17]  L. Katz,et al.  Role of the Vomeronasal Organ in Neonatal Offspring Recognition in Sheep1 , 2000, Biology of reproduction.

[18]  R. Kern Candidate's Thesis: Chronic Sinusitis and Anosmia: Pathologic Changes in the Olfactory Mucosa , 2000 .

[19]  I. Salazar,et al.  A descriptive and comparative lectin histochemical study of the vomeronasal system in pigs and sheep , 2000, Journal of anatomy.

[20]  S. Edwards,et al.  Factors influencing aggression between sows after mixing and the consequences for welfare and production , 1998 .

[21]  C. Lindberg Animal behaviour and animal welfare , 1995 .

[22]  H W Gonyou,et al.  The effects of regrouping on behavioral and production parameters in finishing swine. , 1994, Journal of Animal Science.

[23]  G. Ugolini,et al.  Propagation of pseudorabies virus in the nervous system of the mouse after intranasal inoculation. , 1994, Virology.

[24]  C. Wysocki,et al.  Consequences of removing the vomeronasal organ , 1991, The Journal of Steroid Biochemistry and Molecular Biology.

[25]  K. Chin,et al.  Lymphoid tissue in the nasal mucosa of primates, with particular reference to intraepithelial lymphocytes. , 1974, Journal of anatomy.

[26]  I. Salazar,et al.  Anatomy of the olfactory mucosa. , 2019, Handbook of clinical neurology.

[27]  A. Prunier Scientific Opinion on the use of animal-based measures to assess welfare in pigs , 2012 .

[28]  Christoph Winckler,et al.  Guidance on good practice in conducting scientific assessments in animal health using modelling , 2022, EFSA journal. European Food Safety Authority.

[29]  T. Kikusui,et al.  Removal of the vomeronasal organ blocks the stress-induced hyperthermia response to alarm pheromone in male rats. , 2007, Chemical senses.

[30]  J. M. Bruce,et al.  12 – VENTILATION AND TEMPERATURE CONTROL CRITERIA FOR PIGS , 1981 .