Volume 3, Issue 4, July 2015, Page: 70-76
An Alarm Pheromone May Be Released by Defeated Competitors: A Possible Indicator of Danger
Ana G. Gutiérrez-García, School of Psychology, University of Veracruz, Veracruz, Mexico; Neuropharmacology section, Institute of Neuroethology, University of Veracruz, Veracruz, Mexico
Carlos M. Contreras, Neuropharmacology section, Institute of Neuroethology, University of Veracruz, Veracruz, Mexico; Peripherical Unit, Biomedical Research Institute, National Autonomous University of Mexico, Veracruz, Mexico
Remedios Mendoza-López, Analytic Resolution Services (SARA), University of Veracruz, Veracruz, Mexico
José Madrigal-Madariaga, Neuropharmacology section, Institute of Neuroethology, University of Veracruz, Veracruz, Mexico
Received: Jun. 19, 2015;       Accepted: Jul. 1, 2015;       Published: Jul. 14, 2015
DOI: 10.11648/j.ajpn.20150304.13      View  3843      Downloads  117
Abstract
Among many species, the establishment of hierarchical relations contains a highly ritualized behavioral context accompanied by the delivery of volatile agents, namely ketones and aldehydes, into environment. These substances act as signals contributing to defining and maintaining social hierarchies. Among mammals, some volatile compounds are released into the environment to report the presence of danger or conflict to conspecifics. For example, rats release an alarm pheromone, 2-heptanone, through their urine when subjected to physical stress. However, it is unknown whether some similarity occurs in human being, in spite that many possible alarm compounds have been identified in human fluids, including 2-heptanone. Contact sports may represent a situation of psychosocial interaction in which some hierarchy is established at the end of the contest. In such a case, the first match in martial arts competitions represents a natural model that is seemingly useful for studying alarm conditions in humans since there are two outcomes, winner and non-winner and after a stressful situation represented by contest, some kind of hierarchy is established. The present study measured urinary concentrations of 2-heptanone using gas chromatography-mass spectrometry and applied anxiety measures (State-Trait Anxiety Inventory, STAI) in a sample of healthy student athletes. Compared with martial-arts winners, the characteristics of the non-winners included an increase in their urinary 2-heptanone content (F2,18 = 5.541, p < 0.01), with no changes in anxiety scores (STAI-T: F2,18 = 0.052, p = 0.949; and STAI-S: F2,18 = 1.083, p = 0.360). The production of this ketone seems to be related with metabolic routes of fatty acids involving the participation of the so called stress hormones that may lead to an increase in the lipolysis of fatty acids and production of their metabolites, and among them, 2-heptanone. The increased release of 2-heptanone at the end of the match in non-winners may be interpreted as the release of an alarm signal that indicates imminent danger, similar to the occurrence in other species.
Keywords
Anxiety, 2-heptanone, Martial Arts, Winners, Tournament, Urine
To cite this article
Ana G. Gutiérrez-García, Carlos M. Contreras, Remedios Mendoza-López, José Madrigal-Madariaga, An Alarm Pheromone May Be Released by Defeated Competitors: A Possible Indicator of Danger, American Journal of Psychiatry and Neuroscience. Vol. 3, No. 4, 2015, pp. 70-76. doi: 10.11648/j.ajpn.20150304.13
Reference
[1]
D.C. Blanchard, R.J. “The colony model of aggression and defense”. In: D.A Dewsbury. Contemporary issues in comparative psychology. Sunderland, Massachusetts: Sinauer Associates, pp. 124-137, 1990.
[2]
D.C. Blanchard, R.R. Sakai, B. McEwen, S.M. Weiss, R.J. Blanchard. “Subordination stress: behavioral, brain, and neuroendocrine correlates”. Behav Brain Res, 58:113-121, 1993.
[3]
R.J. Blanchard, D.C. Blanchard, K.J. “Social stress, mortality and aggression in colonies and burrowing habitats”. Behav Proces, 11:209-213, 1985.
[4]
B. Jemiolo, T.M. Xie, M. Novotny. “Urine marking in male mice: responses to natural and synthetic chemosignals”. Physiol Behav, 52:521-526, 1992.
[5]
M. Novotny, S. Harvey, B. Jemiolo. “Chemistry of male dominance in the house mouse, Mus domesticus”. Experientia, 15:109-113, 1990.
[6]
L.A. Pohorecky, G.G. Blakley, H.A. Soini, D. Wiesler, K.E. Bruce, M.V. Novotny. “Social housing influences the composition of volatile compounds in the preputial glands of male rats”. Horm Behav, 53:536-545, 2008.
[7]
A.G. Gutiérrez-García, C.M. Contreras, R. Mendoza-López, S. Cruz-Sánchez, O. García-Barradas, J.F. Rodríguez-Landa, B. Bernal-Morales. “A single session of emotional stress produces anxiety in Wistar rats”. Behav Brain Res, 167:30-35, 2006.
[8]
L.J. Alport. “Comparative analysis of the role of olfaction and the neocortex in primate intrasexual competition”. Anat Rec A Discov Mol Cell Evol Biol, 281:1182-1189, 2004.
[9]
A. Salvador. “Coping with competitive situations in humans”. Neurosci Biobehav Rev, 29:195-205, 2005.
[10]
T.R. Zazryn, P.R. McCrory, P.A. Cameron. “Neurologic injuries in boxing and other combat sports”. Neurol Clin, 26: 257-270, 2008.
[11]
R. Hauser, M. Wiergowski, M. Kaliszan, T. Gos, G. Kernbach-Wighton, M. Studniarek, Z. Jankowski, J. Namiesnik. “Olfactory and tissue markers of fear in mammals including humans”. Med Hypotheses, 77:1062-1067, 2011.
[12]
C.D. Spielberg, R. Díaz-Guerrero. “IDARE. Inventario de Ansiedad: Rasgo-Estado”. México City: Manual Moderno, 1975.
[13]
A. Salvador, R. Costa. “Coping with competition: neuroendocrine responses and cognitive variables”. Neurosc Biobehav Rev, 33:160-170, 2009.
[14]
R.J. Blanchard, C.R. McKittrick, D.C. Blanchard. “Animal models of social stress: effects on behavior and brain neurochemical systems”. Physiol Behav, 73:261-271, 2001.
[15]
R. Costa, A. Salvador. “Associations between success and failure in a face-to-face competition and psychobiological parameters in young women”. Psychoneuroendocrinology, 37:1780-1790, 2012.
[16]
E. Reynes, J. Lorant. “Competitive martial arts and aggressiveness: a 2-yr. longitudinal study among young boys”. Percept Mot Skills, 98:103-115, 2004.
[17]
W. Lamarre, T.A. Nosanchuk. “Judo-the gentle way: a replication of studies on martial arts and aggression”. Percep Motor Skills, 88:992-996, 1999.
[18]
E. Franchini, S. Sterkowicz, C.M. Meira, F.R. Gómes, G. Tani. “Technical variation in a sample of high level judo players”. Percept Mot Skills, 106:859-869, 2008.
[19]
E.L. Melanson. “Resting heart rate variability in men varying in habitual physical activity”. Med Sci Sports Exerc, 32:1894-1901, 2000.
[20]
R. Wadey, S. “Basic psychological skills usage and competitive anxiety responses: perceived underlying mechanisms”. Res Q Exerc Sport, 79:363-373, 2008.
[21]
A.G. Gutiérrez-García, C.M. Contreras, M.R. Mendoza-López, O. García-Barradas, J.S. Cruz-Sánchez. “Urine from stressed rats increases immobility in receptor rats forced to swim: role of 2-heptanone”. Physiol Behav, 91:166-172, 2007.
[22]
C.M. Contreras, A.G. Gutiérrez-García, T. Molina-Jiménez, M.R. Mendoza-López. “2-Heptanone increases the firing rate of the basal amygdala: role of anterior olfactory epithelial organs”. Neuropsychobiology, 66:167-173, 2012.
[23]
C.M. Contreras, A.G. Gutiérrez-García, T. Molina-Jiménez. “Anterior olfactory organ removal produces anxiety-like behavior and increases spontaneous neuronal firing rate in basal amygdala”. Behav Brain Res, 252:101-109, 2012.
[24]
T. Molina-Jiménez, A.G. Gutiérrez-García, C.M. Contreras. “An alarm pheromone increases the responsivity of amygdaline-hippocampal neurons”. Salud Mental, 36(4):279-284, 2013.
[25]
R. Hauser, M. Wiergowski, G. Kernbach-Wighton, J. Namieśnik, M. Kaliszana.” study to identify olfactory markers of fear in rats a humans”. JSIMA, 3:82-84, 2011.
[26]
I. Rodríguez, C.A. Greer, M.Y. Mok, P. Mombaerts. “A putative pheromone receptor gene expressed in human olfactory mucosa”. Nature Genetics, 26:18-19, 2000.
[27]
B. de Lacy Costello, A. Amann, H. Al-Kateb, C. Flynn, W. Filipiak, T. Khalid, D. Osborne, N.M Ratcliffe. “A review of the volatiles from the healthy human body.” J Breath Res, 8(1):014001, 2014.
[28]
B.R. Wager, MD. Breed. “Does honey bee sting alarm pheromone give orientation information to defensive bees?” Ann Entomol Soc Am, 93:1329-1332, 2000.
[29]
W.O. Hughes, P.E. Howse, D. Goulson. “Mandibular gland chemistry of grass–cutting ants: species, caste, and colony variation”. J Chem Ecol, 27:109-124, 2001.
[30]
L.E. Rasmussen, T.D. Lee, W.L. Roelofs, A. Zhang, Jr.G.D.Daves. “Insect pheromone in elephants. Nature, 379:684, 1996.
[31]
L.E. Rasmussen, T.D. Lee, A. Zhang, W.L. Roelofs, Jr.G.D. Daves. “Purification, identification, concentration and bioactivity of (Z)-7-dodecen-1-yl acetate: sex pheromone of the female Asian elephant (Elephas maximus)”. Chem Senses, 22:417-437, 1997.
[32]
Z. Wang, C. Balet-Sindreu, V. Li, A. Nudelman, G.C. Chan, D.R. Storm. “Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium”. J Neurosci, 26:7375-7379, 2006.
[33]
H.E. Day, C.V. Masini, S. Campeau. “The pattern of brain c-fos mRNA induced by a component of fox odor, 2,5-dihydro-2,4,5-trimethylthiazoline (TMT), in rats, suggests both systemic and processive stress characteristics”. Brain Res, 1025:139-151, 2004.
[34]
L.G. Staples, G.E. Hunt, J.L. Cornish, I.S. McGregor. “Neural activation during cat odor-induced conditioned fear and ‘trial 2’ fear in rats”. Neurosci Biobehav Rev, 29:1265-1277, 2005.
[35]
M. Martínez, A. Calvo-Torrent, M.A. Picó-Alfonso. “Social defeat and subordination as models of social stress in laboratory rodents: a review”. Aggress Behav, 24:241-256, 1998.
[36]
F.J. Schwende, D. Wiesler, M. Novotny. “Volatile compounds associated with estrus in mouse urine: potential pheromones”. Experientia, 40:213-215, 1984.
[37]
M.J. Carroll, A.J. Duehl. “Collection of volatiles from honeybee larvae and adults enclosed on brood frames”. Apidologie, 43:715-730, 2012.
[38]
R.F. Gehrig, S.G. Knight. “Formation of ketones from fatty acids by spores of Penicillium roqueforti”. Nature, 182:1237, 1958.
[39]
P. Pasanen, A. Korpi, P. Kalliokoski, A.L. Pasanen. “Growth and volatile metabolite production of Aspergillus versicolor in house dust”. Environ Int, 23:425-432, 1997.
[40]
S. Cakmakci, E. Dagdemir, A.A. Hayaloglu, M. Gurses, B. Cetin, D. Tahmas-Kahyaoglu. “Effect of Penicillium roqueforti and incorporation of whey cheese on volatile profiles and sensory characteristics of mould-ripened Civil cheese”. Int J Dairy Technol, 66:512-526, 2013.
[41]
C. Larroche, I. Besson, J.B. Gros. “Behavior of spores of Penicillium roquefortii during fed-batch bioconversion of octanoic acid into 2-heptanone”. Biotechnol Bioeng, 44:699-709, 1994.
[42]
C. Larroche. “Internal substrate concentrations during biotransformation of octanoic acid into 2-heptanone by spores of Penicillium roquefortii”. J Ind Microbiol Biotechnol, 16:29-35, 1996.
[43]
P.H. Van der Schaft, N. Ter Burg, S. Van den Bosch, A.M. Cohen. “Fed-batch production of 2-heptanone by Fusarium poae”. Appl Microbiol Biotechnol, 36:709-711, 1992.
[44]
J.E.R. Santos, B.J. Villarino, A.R. Zosa, F.M. Dayrit “Analysis of volatile organic compounds in virgin coconut oil and their sensory attibutes”. Philip J Sci, 140:161-171, 2011.
[45]
F.J. Delgado, J. González-Crespo, R. Cava, R. Ramírez. “Formation of the aroma of a raw goat milk cheese during maturation analysed by SPME-GC-MS”. Food Chem, 129:1156-1163, 2011.
[46]
A.F. Atasoy, A.A. Hayaloglu, H. Kirmaci, O. Levent, H. Türkoǧlu. “Effects of partial substitution of caprine for ovine milk on the volatile compounds of fresh and mature Urfa cheeses”. Small Rum Res, 115:113-123, 2013.
[47]
V.P. Carnielli, E.J. Sulkers, C. Moretti, J.L. Wattimena, J.B. van Goudoever, H.J. Degenhart, F. Zacchello, P.J. Sauer. “Conversion of octanoic acid into long-chain saturated fatty acids in premature infants fed a formula containing medium-chain triglycerides”. Metabolism, 43:1287-1292, 1994.
[48]
A.A. Papamandjaris, D.E. MacDougall, P.J. Jones. “Medium chain fatty acid metabolism and energy expenditure: obesity treatment implications”. Life Sci, 62:1203-1215, 1998.
[49]
K. Jong-Yeon, R.C. Hickner, G.J. Dohm, J.A. Houmard. “Long- and medium-chain fatty acid oxidation is increased in exercise-trained human skeletal muscle”. Metabolism, 51:460-464, 2002.
[50]
C.B. Djurhuus, C.H. Gravholt, S. Nielsen, A. Mengel, J.S. Christiansen, O.E. Schmitz, N. Møller. “Effects of cortisol on lipolysis and regional interstitial glycerol levels in humans”. Am J Physiol Endocrinol Metab, 283:E172-177, 2002.
[51]
T.F. Denson, J.D. Creswell, I. Granville-SmithI.”Self-focus and social evaluative threat increase salivary cortisol responses to acute stress in men”. J Behav Med, 35:624-633, 2012.
[52]
S. Zilioli, N.V. Watson. “Winning isn't everything: mood and testosterone regulate the cortisol response in competition”. PLoS One, 8(1):e52582, 2013.
[53]
K.H. Schulpis, T. Parthimos, E.D. Papakonstantinou, T. Tsakiris, M. Parthimos, A.F. Mentis, S. Tsakiris. “Evidence for the participation of the stimulated sympathetic nervous system in the regulation of carnitine blood levels of soccer players during a game”. Metabolism, 58:1080-1086, 2009.
[54]
N. Ben Abdelkrim, C. Castagna, S. El Fazaa, Z. Tabka, J. El Ati. “Blood metabolites during basketball competitions”. J Strength Cond Res, 23:765-773, 2009.
[55]
T. Ojala, K. Häkkinen. “Effects of the tennis tournament on players' physical performance, hormonal responses, muscle damage and recovery”. J Sports Sci Med, 12:240-248, 2013.
[56]
A. Salvador, F. Suay, E. González-Bono, M.A. Serrano. “Anticipatory cortisol, testosterone and psychological responses to judo competition in young men”. Psychoneuroendocrinology, 28:364-375, 2003.
[57]
M. Jiménez, R. Aguilar, J.R. Alvero-Cruz. “Effects of victory and defeat on testosterone and cortisol response to competition: evidence for same response patterns in men and women”. Psychoneuroendocrinology, 37:1577-1581, 2012.
[58]
R. Aguilar, M. Jiménez, J.R. Alvero-Cruz. “Testosterone, cortisol and anxiety in elite field hockey players”. Physiol Behav, 119:38-42, 2013.
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