#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Physiological stress reactivity and recovery related to behavioral traits in dogs (Canis familiaris)


Autoři: Rian C. M. M. Lensen aff001;  Christel P. H. Moons aff002;  Claire Diederich aff001
Působiště autorů: Department of Veterinary Medicine (IVRU), University of Namur, Namur, Belgium aff001;  Department of Nutrition, Genetics and Ethology, Ghent University, Merelbeke, Belgium aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222581

Souhrn

This study investigated whether stress responsiveness (in one context) can be used to predict dog behavior in daily life. On two occasions (NT1 = 32 puppies; NT2 = 16 young adults), dogs’ physiological stress response after a behavioral test at home was measured in terms of reactivity (10 min post-test) and recovery (40 min post-test) for three salivary markers: cortisol, chromogranin A (CgA) and secretory immunoglobulin A (sIgA). For each marker, it was determined whether dogs with a strong physiological response displayed different behavior in daily life compared to dogs with a weaker physiological response. The results revealed three main findings: first, for CgA and cortisol, different patterns were identified according to sample time. High reactivity related to desirable traits, whereas slow recovery after the behavioral test related to undesirable traits. The findings suggest that increased levels of CgA and cortisol 10 minutes after the behavioral test reflected an adaptive stress response, whereas elevated levels 40 minutes after the test reflected unsuccessful coping. Second, patterns for sIgA differed from CgA and cortisol: significant associations were only found with behavioral traits at T2, mostly considered desirable and related to Trainability. Possibly, the delayed reaction pattern of sIgA caused this difference between markers, as sIgA reflects the (secondary) immune response to stress, due to immunosuppressive effects of cortisol. Third, predictive capacity of puppies’ physiological stress response (T1) was inconclusive, and contrary relations were found with behavioral traits at T2, suggesting that developmental factors play an important role. This study provides new insights about the relation between stress physiology and behavioral traits, and methodological advice is given to study these patterns further. In conclusion, physiological markers could provide additional insights in dogs’ tendencies to display certain behaviors, especially at the young adult stage. Further studies are needed to confirm these patterns.

Klíčová slova:

Biology and life sciences – Biochemistry – Organisms – Eukaryota – Psychology – Animals – Social sciences – People and places – Population groupings – Anatomy – Medicine and health sciences – Physiology – Animal types – Pets and companion animals – Vertebrates – Amniotes – Mammals – Dogs – Zoology – Immunology – Immune response – Immune physiology – Hormones – Body fluids – Behavior – Age groups – Animal behavior – Lipid hormones – Young adults – Cortisol – Steroid hormones – Saliva


Zdroje

1. Carere C, Caramaschi D, Fawcett TW. Covariation between personalities and individual differences in coping with stress: Converging evidence and hypotheses. Curr Zool. 2010;56: 728–740.

2. Rayment DJ, De Groef B, Peters RA, Marston LC. Applied personality assessment in domestic dogs: Limitations and caveats. Appl Anim Behav Sci. 2015;163: 1–18. doi: 10.1016/j.applanim.2014.11.020

3. Sforzini E, Michelazzi M, Spada E, Ricci C, Carenzi C, Milani S, et al. Evaluation of young and adult dogs’ reactivity. J Vet Behav. 2009;4: 3–10. doi: 10.1016/j.jveb.2008.09.035

4. Jones AC, Gosling SD. Temperament and personality in dogs (Canis familiaris): A review and evaluation of past research. Appl Anim Behav Sci. 2005;95: 1–53.

5. Wolf M, van Doorn GS, Weissing FJ. Evolutionary emergence of responsive and unresponsive personalities. Proc Natl Acad Sci U S A. 2008;105: 15825–15830. doi: 10.1073/pnas.0805473105 18838685

6. Koolhaas JM, de Boer SF, Coppens CM, Buwalda B. Neuroendocrinology of coping styles: Towards understanding the biology of individual variation. Front Neuroendocrinol. 2010;31: 307–321. doi: 10.1016/j.yfrne.2010.04.001 20382177

7. Overall KL. Manual of Clinical Behavioral Medicine for Dogs and Cats. St. Louis, Missouri: Elsevier; 2013.

8. Wormald D, Lawrence AJ, Carter G, Fisher AD. Physiological stress coping and anxiety in greyhounds displaying inter-dog aggression. Appl Anim Behav Sci. 2016;180: 93–99. doi: 10.1016/j.applanim.2016.04.007

9. Barnard S, Marshall-Pescini S, Passalacqua C, Beghelli V, Capra A, Normando S, et al. Does Subjective Rating Reflect Behavioural Coding? Personality in 2 Month-Old Dog Puppies: An Open-Field Test and Adjective-Based Questionnaire. PLoS One. 2016;11: e0149831. doi: 10.1371/journal.pone.0149831 26977588

10. Riemer S, Müller C, Virányi Z, Huber L, Range F. The predictive value of early behavioural assessments in pet dogs—A longitudinal study from neonates to adults. PLoS One. 2014;9: e101237. doi: 10.1371/journal.pone.0101237 25003341

11. Ley J, Coleman GJ, Holmes R, Hemsworth PH. Assessing fear of novel and startling stimuli in domestic dogs. Appl Anim Behav Sci. 2007;104: 71–84. doi: 10.1016/j.applanim.2006.03.021

12. Ng ZY, Pierce BJ, Otto CM, Buechner-Maxwell VA, Siracusa C, Werre SR. The effect of dog–human interaction on cortisol and behavior in registered animal-assisted activity dogs. Appl Anim Behav Sci. 2014;159: 69–81. doi: 10.1016/j.applanim.2014.07.009

13. Stamps J, Groothuis TGG. The development of animal personality: Relevance, concepts and perspectives. Biol Rev. 2010;85: 301–325. doi: 10.1111/j.1469-185X.2009.00103.x 19961473

14. Horváth Z, Igyártó B-Z, Magyar A, Miklósi Á. Three different coping styles in police dogs exposed to a short-term challenge. Horm Behav. 2007;52: 621–630. doi: 10.1016/j.yhbeh.2007.08.001 17900575

15. Sherman BL, Gruen ME, Case BC, Foster ML, Fish RE, Lazarowski L, et al. A test for the evaluation of emotional reactivity in Labrador retrievers used for explosives detection. J Vet Behav. 2015;10: 94–102. doi: 10.1016/j.jveb.2014.12.007

16. Lensen CMM, Moons CPH, Diederich C. Saliva sampling in dogs: How to select the most appropriate procedure for your study. J Vet Behav. 2015;10: 504–512. doi: 10.1016/j.jveb.2015.08.006

17. Hekman JP, Karas AZ, Sharp CR. Psychogenic stress in hospitalized dogs: Cross species comparisons, implications for health care, and the challenges of evaluation. Animals. 2014;4: 331–347. doi: 10.3390/ani4020331 25126422

18. Beerda B, Schilder MBH, van Hooff JARAM, de Vries HW, Mol JA. Behavioural, saliva cortisol and heart rate responses to different types of stimuli in dogs. Appl Anim Behav Sci. 1998;58: 365–381. doi: 10.1016/S0168-1591(97)00145-7

19. Dreschel NA, Granger DA. Physiological and behavioral reactivity to stress in thunderstorm-phobic dogs and their caregivers. Appl Anim Behav Sci. 2005;95: 153–168. doi: 10.1016/j.applanim.2005.04.009

20. Mormède P, Andanson S, Aupérin B, Beerda B, Guémené D, Malmkvist J, et al. Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiol Behav. 2007;92: 317–339. doi: 10.1016/j.physbeh.2006.12.003 17234221

21. Protopopova A. Effects of sheltering on physiology, immune function, behavior, and the welfare of dogs. Physiol Behav. 2016;159: 95–103. doi: 10.1016/j.physbeh.2016.03.020 26996275

22. Kikkawa A, Uchida Y, Nakade T, Taguchi K. Salivary secretory IgA concentrations in beagle dogs. J Vet Med Sci. 2003;65: 689–693. doi: 10.1292/jvms.65.689 12867728

23. Lucassen PJ, Pruessner J, Sousa N, Almeida OFX, Van Dam AM, Rajkowska G, et al. Neuropathology of stress. Acta Neuropathol. 2014;127: 109–135. doi: 10.1007/s00401-013-1223-5 24318124

24. Hiby EF, Rooney NJ, Bradshaw JWS. Behavioural and physiological responses of dogs entering re-homing kennels. Physiol Behav. United States; 2006;89: 385–391. doi: 10.1016/j.physbeh.2006.07.012 16905163

25. Haverbeke A, Diederich C, Depiereux E, Giffroy JM. Cortisol and behavioral responses of working dogs to environmental challenges. Physiol Behav. 2008;93: 59–67. doi: 10.1016/j.physbeh.2007.07.014 17868751

26. Ott S, Soler L, Moons CPH, Kashiha MA, Bahr C, Vandermeulen J, et al. Different stressors elicit different responses in the salivary biomarkers cortisol, haptoglobin, and chromogranin A in pigs. Res Vet Sci. 2014;97: 124–128. doi: 10.1016/j.rvsc.2014.06.002 24957408

27. Ivković N, Božović Đ, Račić M, Popović-Grubač D, Davidović B. Biomarkers of Stress in Saliva / Biomarkeri stresa u pljuvački. Acta Fac Medicae Naissensis. 2015;32: 91–99. doi: 10.1515/afmnai-2015-0010

28. Kennedy B, Dillon E, Mills PJ, Ziegler MG. Catecholamines in human saliva. Life Sci. 2001;69: 87–99. doi: 10.1016/s0024-3205(01)01111-0 11411808

29. Akiyoshi H, Aoki M, Shimada T, Noda K, Kumagai D, Saleh N, et al. Measurement of plasma chromogranin A concentrations for assessment of stress responses in dogs with insulin-induced hypoglycemia. Am J Vet Res. 2005;66: 1830–1835. 16273918

30. Toda M, Morimoto K. Effect of lavender aroma on salivary endocrinological stress markers. Arch Oral Biol. 2008;53: 964–968. doi: 10.1016/j.archoralbio.2008.04.002 18635155

31. Escribano D, Soler L, Gutiérrez AM, Martínez-Subiela S, Cerón JJ. Measurement of chromogranin A in porcine saliva: validation of a time-resolved immunofluorometric assay and evaluation of its application as a marker of acute stress. Animal. 2013;7: 640–647. doi: 10.1017/S1751731112002005 23137814

32. Ninomiya S, Sato S. The assessment of the effect of presenting a companion’s face picture on social isolation stress using saliva sampling in cows. Anim Sci J. 2011;82: 787–791. doi: 10.1111/j.1740-0929.2011.00896.x 22111636

33. Kanai K, Hino M, Hori Y, Nakao R, Hoshi F, Itoh N, et al. Circadian variations in salivary chromogranin a concentrations during a 24-hour period in dogs. J Vet Sci. 2008;9: 421–423. doi: 10.4142/jvs.2008.9.4.421 19052500

34. Skandakumar S, Stodulski G, Hau J. Salivary IgA: a Possible Stress Marker In Dogs. Anim Welf. 1995;4: 339–350.

35. Hsu Y, Serpell JA. Development and validation of a questionnaire for measuring behavior and temperament traits in pet dogs. J Am Vet Med Assoc. 2003;223: 1293–1300. doi: 10.2460/javma.2003.223.1293 14621216

36. Mills DS. Medical paradigms for the study of problem behaviour: a critical review. Appl Anim Behav Sci. 2003;81: 265–277. doi: 10.1016/S0168-1591(02)00286-1

37. Duffy DL, Serpell JA. Predictive validity of a method for evaluating temperament in young guide and service dogs. Appl Anim Behav Sci. 2012;138: 99–109. doi: 10.1016/j.applanim.2012.02.011

38. Foyer P, Bjällerhag N, Wilsson E, Jensen P. Behaviour and experiences of dogs during the first year of life predict the outcome in a later temperament test. Appl Anim Behav Sci. 2014;155: 93–100. doi: 10.1016/j.applanim.2014.03.006

39. van den Berg L, Schilder MB, de Vries H, Leegwater PA, van Oost BA. Phenotyping of aggressive behavior in golden retriever dogs with a questionnaire. Behav Genet. 2006;36: 882–902. doi: 10.1007/s10519-006-9089-0 16799833

40. Sandri M, Colussi A, Perrotta MG, Stefanon B. Salivary cortisol concentration in healthy dogs is affected by size, sex, and housing context. J Vet Behav. 2015;10: 302–306.

41. Glenk LM, Kothgassner OD, Stetina BU, Palme R, Kepplinger B, Baran H. Salivary cortisol and behavior in therapy dogs during animal-assisted interventions: A pilot study. J Vet Behav. 2014;9: 98–106. doi: 10.1016/j.jveb.2014.02.005

42. Salimetrics LLC, SalivaBio. Saliva collection and handling advice, 3rd edition [Internet]. 2013 [cited 10 Feb 2014]. Available: https://www.salimetrics.com/assets/documents/Saliva_Collection_Handbook.

43. Hennessy MB T. Williams M, Miller DD, Douglas CW, Voith VL. Influence of male and female petters on plasma cortisol and behaviour: can human interaction reduce the stress of dogs in a public animal shelter? Appl Anim Behav Sci. 1998;61: 63–77. doi: 10.1016/s0168-1591(98)00179-8

44. Kobelt AJ, Hemsworth PH, Barnett JL, Butler KL. Sources of sampling variation in saliva cortisol in dogs. Res Vet Sci. 2003;75: 157–161. doi: 10.1016/s0034-5288(03)00080-8 12893165

45. Ricos C. Biologic variation and desirable specifications for QC [Internet]. [cited 9 Feb 2015]. Available: https://www.westgard.com/guest17.htm

46. Schalke E, Stichnoth J, Ott S, Jones-Baade R. Clinical signs caused by the use of electric training collars on dogs in everyday life situations. Appl Anim Behav Sci. 2007;105: 369–380. doi: 10.1016/j.applanim.2006.11.002

47. King T, Hemsworth PH, Coleman GJ. Fear of novel and startling stimuli in domestic dogs. Appl Anim Behav Sci. 2003;82: 45–64. doi: 10.1016/s0168-1591(03)00040-6

48. Forstmeier W, Wagenmakers E-J, Parker TH. Detecting and avoiding likely false-positive findings–a practical guide. Biol Rev. 2016;92: 1941–1968. doi: 10.1111/brv.12315 27879038

49. Hennessy MB. Using hypothalamic-pituitary-adrenal measures for assessing and reducing the stress of dogs in shelters: A review. Appl Anim Behav Sci. 2013;149: 1–12. doi: 10.1016/j.applanim.2013.09.004

50. Beerda B, Schilder MBH, Van Hooff JARAM, De Vries HW, Mol JA. Behavioural and hormonal indicators of enduring environmental stress in dogs. Anim Welf. 2000;9: 49–62.

51. Beerda B, Schilder MBH, Bernadina W, Van Hooff JARAM, De Vries HW, Mol JA. Chronic Stress in Dogs Subjected to Social and Spatial Restriction. II. Hormonal and Immunological Responses. Physiol Behav. 1999;66: 243–254. doi: 10.1016/s0031-9384(98)00290-x 10336150

52. Rosado B, García-Belenguer S, León M, Chacón G, Villegas A, Palacio J. Blood concentrations of serotonin, cortisol and dehydroepiandrosterone in aggressive dogs. Appl Anim Behav Sci. 2010;123: 124–130. doi: 10.1016/j.applanim.2010.01.009

53. Kikkawa A, Uchida Y, Suwa Y, Taguchi K. A novel method for estimating the adaptive ability of guide dogs using salivary sIgA. J Vet Med Sci. 2005;67: 707–712. doi: 10.1292/jvms.67.707 16082119

54. Bosch JA, Ring C, de Geus EJC, Veerman ECI, Nieuw Amerongen AV. Stress and secretory immunity. Int Rev Neurobiol. 2002; 52: 213–253. doi: 10.1016/S0074-7742(02)52011-0 12498106

55. Nakane H, Asami O, Yamada Y, Harada T, Matsui N, Kanno T, et al. Salivary Chromogranin A as an index of psychosomatic stress response. Biomed Res. 1998;19: 401–406. doi: 10.2220/biomedres.19.401

56. Svobodová I, Chaloupková H, Končel R, Bartoš L, Hradecká L, Jebavý L. Cortisol and Secretory Immunoglobulin A Response to Stress in German Shepherd Dogs. PLoS One. 2014;9: e90820. doi: 10.1371/journal.pone.0090820 24637917

57. Uher J. Individual behavioral phenotypes: An integrative meta-theoretical framework. Why “behavioral syndromes” are not analogs of “personality.” Dev Psychobiol. 2011;53: 521–548. doi: 10.1002/dev.20544 21432848

58. Day MJ. Immune System Development in the Dog and Cat. J Comp Pathol. 2007;137: S10–S15. doi: 10.1016/j.jcpa.2007.04.005 17560591

59. Cobb ML, Iskandarani K, Chinchilli VM, Dreschel NA. A systematic review and meta-analysis of salivary cortisol measurement in domestic canines. Domest Anim Endocrinol. 2016;57: 31–42. doi: 10.1016/j.domaniend.2016.04.003 27315597

60. Appleby D, Pluijmakers J. Separation anxiety in dogs. The function of homeostasis in its development and treatment. Vet Clin North Am Small Anim Pract. 2003;33: 321–344. doi: 10.1016/S0195-5616(02)00101-8 12701515

61. Bennett A, Hayssen V. Measuring cortisol in hair and saliva from dogs: coat color and pigment differences. Domest Anim Endocrinol. 2010/08/14. 2010;39: 171–180. doi: 10.1016/j.domaniend.2010.04.003 20705413

62. Siniscalchi M, McFarlane JR, Kauter KG, Quaranta A, Rogers LJ. Cortisol levels in hair reflect behavioural reactivity of dogs to acoustic stimuli. Res Vet Sci. 2013;94: 49–54. doi: 10.1016/j.rvsc.2012.02.017 22449333


Článok vyšiel v časopise

PLOS One


2019 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#