Stress affects salivary alpha-Amylase activity in bonobos

Physiology and Behavior

Volumn 105, Issue 2, 2012, Pages 476-482

  Behringer, Verena ^a   Deschner, Tobias ^a   Möstl, Erich ^b   Selzer, Dieter ^c   Hohmann, Gottfried ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Alpha Amylase; Bonobo; Cortisol; Saliva; Stress

Indexed keywords

ALPHA AMYLASE SALIVA ISOENZYME; HYDROCORTISONE;

APE; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; BEHAVIOR; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HUMAN; MALE; MENTAL STRESS; NONHUMAN; PRIORITY JOURNAL; SPECIES COMPARISON;

ADULT; AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; CIRCADIAN RHYTHM; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; HYDROCORTISONE; LINEAR MODELS; MALE; MIDDLE AGED; PAN PANISCUS; SALIVA; SALIVARY ALPHA-AMYLASES; SEX FACTORS; SPECIES SPECIFICITY; STRESS, PSYCHOLOGICAL;

EID: 80053509346     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2011.09.005     Document Type: Article

References (69)

1. Zakowski J.J., Bruns D.E. Biochemistry of human alpha amylase isoenzymes. Crit Rev Clin Lab Sci 1985, 21:283-322.
2. Mandel A., Peyrot des Gachons C., Plank K.L., Alarcon S., Breslin P.A.S. Individual differences in AMY1 gene copy number, salivary α-amylase levels, and the perception of oral starch. PLoS One 2010, 5(10):e13352.
3. Perry G.H., Dominy N.J., Claw K.G., Lee A.S., Fiegler H., Redon R., et al. Diet and the evolution of human amylase gene copy number variation. Nat Genet 2007, 39:1256-1260.
4. Baum B.J. Principles of saliva secretion. Ann N Y Acad Sci 1993, 694:17-23.
5. Emmelin N. Nerve interactions in salivary glands. J Dent Res 1978, 66:509-517.
6. Nater U.M., Rohleder N. Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: current state of research. Psychoneuroendocrinology 2009, 34:486-496.
7. Chatterton R.T., Vogelsong K.M., Lu Y., Ellman A.B., Hudgens G.A. Salivary α-amylase as a measure of endogenous adrenergic activity. Clin Physiol 1996, 16:433-448.
8. Kivlighan K.T., Granger D.A. Salivary α-amylase response to competition: relation to gender, previous experience, and attitudes. Psychoneuroendocrinology 2006, 31:703-714.
9. van Stegeren A., Wolf O.T., Kindt M. Salivary alpha amylase and cortisol response to different stress tasks: impact of sex. Int J Psychophysiol 2008, 69:33-40.
10. Fortunato C.K., Dribin A.E., Granger D.A., Buss K.A. Salivary alpha-amylase and cortisol in toddlers: differential relations to affective behavior. Dev Psychobiol 2008, 50:807-818.
11. Nater U.M., Rohleder N., Gaab J., Berger S., Jud A., Kirschbaum C., et al. Human salivary alpha-amylase reactivity in a psychosocial stress paradigm. Int J Psychophysiol 2005, 55:333-342.
12. Rohleder N., Nater U.M., Wolf J.M., Ehlert U., Kirschbaum C. Psychosocial stress-induced activation of salivary alpha-amylase. Ann N Y Acad Sci 2004, 1032:258-263.
13. Strahler J., Mueller A., Rosenloecher F., Kirschbaum C., Rohleder N. Salivary α-amylase stress reactivity across different age groups. Psychophysiology 2010, 47:587-595.
14. Takai N., Yamaguchi M., Aragaki T., Eto K., Uchihashi K., Nishikawa Y. Effect of psychological stress on the salivary cortisol and amylase levels in healthy young adults. Arch Oral Biol 2004, 49:963-968.
15. Kirschbaum C., Hellhammer D.H. Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 1994, 19:313-333.
16. Antonini S.R.R., Jorge S.M., Moreira A.C. The emergence of salivary cortisol circadian rhythm and its relationship to sleep activity in preterm infants. Clin Endocrinol 2000, 52:423-426.
17. de Weerth C., Jansen J., Vos M.H., Maitimu I., Lentjes E.G.W.M. A new device for collecting saliva for cortisol determination. Psychoneuroendocrinology 2007, 32:1144-1148.
18. Essex M.J., Klein M.H., Cho E., Kalin N.H. Maternal stress beginning in infancy may sensitize children to later stress exposure: effects on cortisol and behavior. Biol Psychiatry 2002, 52:776-784.
19. Harmon A.G., Hibel L.C., Rumyantseva O., Granger D.A. Measuring salivary cortisol in studies of child development: watch out-what goes in may not come out of saliva collection devices. Dev Psychobiol 2007, 49:495-500.
20. Kirschbaum C., Prüssner J.C., Stone A.A., Federenko I., Gaab J., Lintz D., et al. Persistent high cortisol responses to repeated psychological stress in a subpopulation of healthy men. Psychosom Med 1995, 57:468-474.
21. Santiago L.B., Jorge S.M., Moreira A.C. Longitudinal evaluation of the development of salivary cortisol circadian rhythm in infancy. Clin Endocrinol 1996, 44:157-161.
22. Ange-van Heugten K.D., van Heugten E., Timmer S., Bosch G., Elias A., Whisnant S., et al. Fecal and salivary cortisol concentrations in woolly (Lagothrix ssp.) and spider monkeys (Ateles spp.). Int J Zool 2009, 1-9.
23. Cross N., Rogers L.J. Diurnal cycle in salivary cortisol levels in common marmosets. Dev Psychobiol 2004, 45:134-139.
24. Pearson B.L., Judge P.G., Reeder D.M. Effectiveness of saliva collection and enzyme-immunoassay for the quantification of cortisol in socially housed baboons. Am J Primatol 2008, 70:1145-1151.
25. Behringer V., Clauß W., Hachenburger K., Kuchar A., Möstl E., Selzer D. Effect of giving birth on the cortisol level in a bonobo groups' (Pan paniscus) saliva. Primates 2009, 50:190-193.
26. Elder C.M., Menzel C.R. Dissociation of cortisol and behavioral indicators of stress in an orangutan (Pongo pygmaeus) during a computerized task. Primates 2001, 42:345-357.
27. Hohmann G., Mundry R., Deschner T. The relationship between socio-sexual behavior and salivary cortisol in bonobos: tests of the tension regulation hypothesis. Am J Primatol 2009, 71:223-232.
28. Kuhar C.W., Bettinger T.L., Laudenslager M.L. Salivary cortisol and behaviour in an all-male group of western lowland gorillas (Gorilla g. gorilla). Anim Welf 2005, 14:187-193.
29. Kutsukake N., Ikeda K., Honma S., Teramoto M., Mori Y., Hayasaka I., et al. Validation of salivary cortisol and testosterone assays in chimpanzees by liquid chromatography-tandem mass spectrometry. Am J Primatol 2009, 71:696-706.
30. Granger D.A., Kivlighan K.T., Blair C., El-Sheikh M., Mize J., Lisonbee J.A., et al. Integrating the measurement of salivary a-amylase into studies of child health, development, and social relationships. J Soc Pers Relatsh 2006, 23:267-290.
31. Koolhaas J.M., Korte S.M., de Boer S.F., van der Vegt B.J., van Reenen C.G., Hopster H., et al. Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 1999, 23:925-935.
32. McGeachin R.L., Akin J.R. Amylase levels in the tissues and body fluids of several primate species. Comp Biochem Physiol 1982, 72:267-269.
33. Higham J.P., Vitale A.B., Rivera A.M., Ayala J.E., Maestripieri D. Measuring salivary analytes from free-ranging monkeys. Physiol Behav 2010, 101:601-607.
34. Jacobsen N., Sönju T. Molecular weight and amino acid composition of Macaca irus parotid alpha-amylase. Eur J Oral Sci 1971, 79:193-201.
35. Williams B.L., Keller P.J. Amylase and other protein components of parotid saliva of the baboon, Papio anubis. Comp Biochem Physiol A Mol Integr Physiol 1973, 44:393-400.
36. Mau M., Südekum K.-H., Sliwa A., Kaiser T.M. Indication of higher salivary α-amylase expression in hamadryas baboons and geladas compared to chimpanzees and humans. J Med Primatol 2010, 39:187-190.
37. Samuelson L.C., Philips R.S., Swanberg L.J. Amylase gene structures in primates: retroposon insertions and promoter evolutions. Mol Biol Evol 1996, 13:767-779.
38. Smiley T., Spelman L., Lukasik-Braum M., Mukherjee J., Kaufman G., Akiyoshi D.E., et al. Noninvasive saliva collection techniques for free-ranging mountain gorillas and captive eastern gorillas. J Zoo Wildl Med 2010, 41:201-209.
39. Wilson G.M., Flibotte S., Missirlis P.I., Marra M.A., Jones S., Thornton K., et al. Identification by fully-coverage array CGH of human DNA copy number increases relative to chimpanzee and gorilla. Genome Res 2006, 16:173-181.
40. Chauncey H.H., Henriques B.L., Tanzer J.M. Comparative enzyme activity of saliva from the sheep, dog, rabbit, rat, and human. Arch Oral Biol 1963, 8:615-627.
41. Palme R., Möstl E. Measurement of cortisol meatbolites in faeces of sheep as a parameter of cortisol concentration in blood. Z fuer Saeugetierkunde - Int J Mammal Biol 1997, 62(Supplementary 2):192-197.
42. Kirschbaum C., Hellhammer D.H. Salivary cortisol. Encyclopedia of stress 2000, 379-383. Academic Press, San Diego. G. Fink (Ed.).
43. Nater U.M., Rohleder N., Schlotz W., Ehlert U., Kirschbaum C. Determinants of the diurnal course of salivary alpha-amylase. Psychoneuroendocrinology 2007, 32:392-401.
44. Strahler J., Berndt C., Kirschbaum C., Rohleder N. Aging diurnal rhythms and chronic stress: distinct alteration of diurnal rhythmicity of salivary α-amylase and cortisol. Biol Psychol 2010, 84:248-256.
45. Behringer V. Haltungsbedingte Einflüsse auf das Verhalten und die Stresssituation von Westlichen Flachlandgorillas (Gorilla g. gorilla), Sumatra Orang-Utans (Pongo abelii) und Bonobos (Pan pansicus) unter Zoobedingungen. Dissertation. Gießen: Justus-Liebig Universität; 2011.
46. Heintz M.R., Santymire R.M., Parr L.A., Lonsdorf E.V. Validation of a cortisol enzyme immunoassay and characterization of salivary cortisol circadian rhythm in chimpanzees (Pan troglodytes). Am J Primatol 2011, 73:1-6.
47. Nater U.M., La Marca R., Florin L., Moses A., Langhans W., Koller M.M., et al. Stress-induced changes in human salivary alpha-amylase activity-associations with adrenergic activity. Psychoneuroendocrinology 2006, 31:49-58.
48. Maestripieri D., Schino G., Aureli F., Troisi A. A modest proposal: displacement activities as an indicator of emotions in primates. Anim Behav 1992, 44:967-979.
49. Sánchez C. Stress-induced vocalisation in adult animals. A valid model of anxiety?. Eur J Pharmacol 2003, 133-143.
50. Baayen R.H. Analyzing linguistic data 2008, Cambridge University Press, Cambridge.
51. Bates D., Maechler M. lme4: linear mixed-effects models using S4 classes. R package version 0.999375-33 2010.
52. Baayen R.H. LanguageR: data sets and functions with "Analyzing linguistic data: a practical introduction to statistics". R package version 1.0 2010.
53. Haccou P., Meelis E. Statistical analyses of behavioural data 1994, University Press, Oxford.
54. Mundry R., Fischer J. Use of statistical programs for nonparametric tests of small samples often leads to incorrect P values: examples from Animal Behaviour. Anim Behav 1998, 56:256-259.
55. Abbott D.H., Keverne E.B., Bercovitch F.B., Shively C.A., Mendoza S.P., Saltzman W., et al. Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 2003, 43:67-82.
56. Sapolsky R.M. Why zebras don't get ulcers: the acclaimed guide to stress, stress-related diseases, and coping 2004, Owl Books, New York.
57. Gordis E.B., Granger D.A., Susman E.J., Trickett P.K. Salivary alpha amylase-cortisol asymmetry in maltreated youth. Horm Behav 2008, 53:96-103.
58. Takai N., Yamaguchi M., Aragaki T., Eto K., Uchihashi K., Nishikawa Y. Gender-specific differences in salivary biomarker response to acute psychological stress. Ann N Y Acad Sci 2007, 1098:510-515.
59. Smeets T. Autonomic and hypothalamic-pituitary-adrenal stress resilience: impact of cardiac vagal tone. Biol Psychol 2010, 84:290-295.
60. Rohleder N., Wolf J.M., Maldonado E.F., Kirschbaum C. The psychosocial stress-induced increase in salivary alpha-amylase is independent of saliva flow rate. Psychophysiology 2006, 43:645-652.
61. O'Donnell M.D., Miller N.J. Plasma pancreatic and salivary-type amylase and immunoreactive trypsin concentrations: variations with age and reference ranges for children. Clin Chim Acta 1980, 104:265-273.
62. Mackie D.A., Pangborn R.M. Mastication and its influence on human salivary flow and alpha-amylase secretion. Physiol Behav 1990, 47:593-595.
63. Maekinen K.K., Chen C.-Y., Mäkinen P.-L., Bennett C.A., Isokangas P.J., Isotupa K.P., et al. Properties of whole saliva and dental plaque in relation to 40-month consumption of chewing gums containing Xylitol, Sorbitol or Sucrose. Caries Res 1996, 30:180-188.
64. Fraser O.N., Stahl D., Aureli F. Stress reduction through consolation in chimpanzees. PNAS 2008, 105:8557-8562.
65. Troisi A. Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects. Stress 2002, 47-54.
66. Jordan C. Das Verhalten zoolebender Zwergschimpansen. Dissertation. Frankfurt am Main: Johann-Goethe University, 1977.
67. Almy T.P., Kern F., Abbott F.K. Constipation and diarrhea, as a reaction to life stress. Res Publ Assoc Res Nerv Ment Dis 1949, 724-733.
68. Wobber V., Hare B., Maboto J., Lipson S., Wrangham R., Ellison P.T. Differential changes in steroid hormones before competition in bonobos and chimpanzees. PNAS 2010, 107:12457-12462.
69. Whiten A., Byrne R.W., Barton R.A., Waterman P.G., Henzi S.P., Hawkes K., et al. Dietary and foraging strategies of baboons. Philos Trans R Soc Lond B 1991, 334:187-197.