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Frontiers in physiology2017; 8; 664; doi: 10.3389/fphys.2017.00664

Seasonal Variations in Heart Rate Variability as an Indicator of Stress in Free-Ranging Pregnant Przewalski’s Horses (E. ferus przewalskii) within the Hortobágy National Park in Hungary.

Abstract: Ecosystems with seasonal fluctuations in climate and food availability present physiological challenges to resident mammals and may cause "stress." The two predominant physiological responses to stressors are (1) the activation of the hypothalamic-pituitary-adrenal axis and (2) the modulation of the autonomic nervous system. To date, the primary indicator for "stress" in wildlife- and zoo animal research are glucocorticoid levels. By measuring the autonomic regulation of cardiac activity, particularly the vagal tone, heart rate variability (HRV) is presently emerging as a suitable indicator of "stress" in farm- and domestic animal research. The aim of this study was to use HRV, a novel method in wildlife research, to assess seasonal patterns of "stress" in a group of free-ranging Przewalski's horses (). Six pregnant Przewalski's horses from one harem within the Hortobágy National Park in Hungary were subjected to the study. We used a dedicated telemetry system consisting of a subcutaneously implanted transmitter and a receiver and storage unit in a collar to record HRV, heart rate (HR), subcutaneous body temperature, and activity throughout a one-year study period-climate data was also collected. We defined "stress" as a decrease in parasympathetic nervous system tone and calculated RMSSD (root mean square of successive differences) as a measure of HRV. Linear mixed effects models with random intercept per individual were used for statistical analysis. HRV and HR varied considerably throughout the year. Similar to temperate ruminants and hibernating mammals, Przewalski's horses experienced lower HR and HRV during winter, when resources are limited indicating decreased metabolic rates coupled with "stress." In spring, we observed a drop of HRV along with a peak in HR indicating an increase of allostatic load that is most likely associated with increased energy demands during pregnancy and/or seasonal routines such as the adjustment of the gastrointestinal system to better quality diet. Measuring telemetric HRV is a proven method to study undisturbed reactions of wild animals to their changing environment over the long term. Przewalski's horses experience a loss of complexity in cardiovascular dynamics over the winter and particularly during spring, indicating seasonal "stress."
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Publication Date: 2017-09-07 PubMed ID: 28936179PubMed Central: PMC5594093DOI: 10.3389/fphys.2017.00664Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research focuses on understanding stress levels in Przewalski’s horses using heart rate variability (HRV) in relation to seasonal changes. Factors such as climate and metabolic rates, especially during winter and spring, were observed to influence the stress levels of six pregnant Przewalski’s horses in the Hortobágy National Park in Hungary.

Methodology

  • The study employed Heart Rate Variability (HRV) as a stress indicator, which is an emerging method in livestock and domestic animal research. HRV reflects the autonomic regulation of cardiac activity, in particular, the vagal (parasympathetic nervous system) tone.
  • The stress levels of six pregnant Przewalski’s horses from one harem in the Hortobágy National Park in Hungary were examined over one year.
  • A specific telemetry system was used for data collection which involved a subcutaneously implanted transmitter and a receiver fitted in a collar to chronicle HRV, heart rate, subcutaneous body temperature, and physical activity.
  • The measure of stress was defined as a reduction in parasympathetic nervous system tone, with root mean square of successive differences (RMSSD) being utilized to account for HRV.
  • Climate data was also captured in correspondence with the readings from the telemetry system. The data was then statistically analyzed using linear mixed effects models.

Findings

  • There were notable fluctuations in heart rate and HRV throughout the year, indicative of varied stress levels.
  • Substantially lower HR and HRV were observed during winter, a period associated with limited resources, hinting at reduced metabolic rates and heightened stress.
  • A drop in HRV and a peak in heart rate were observed in spring, illustrating an increased allostatic load. This was associated with rising energy demands during pregnancy and seasonal routines like gastrointestinal system adjustments to higher quality diets.

Conclusion

  • Tracking HRV telemetrically was confirmed as an effective way to observe the undisturbed reactions of wild animals to their changing environments over the long term.
  • The study deduced that Przewalski’s horses experience a decrease in complexity in their cardiovascular dynamics during winter and particularly spring, signaling seasonal stress.

Cite This Article

APA
Pohlin F, Brabender K, Fluch G, Stalder G, Petit T, Walzer C. (2017). Seasonal Variations in Heart Rate Variability as an Indicator of Stress in Free-Ranging Pregnant Przewalski’s Horses (E. ferus przewalskii) within the Hortobágy National Park in Hungary. Front Physiol, 8, 664. https://doi.org/10.3389/fphys.2017.00664

Publication

Frontiers in physiology
ISSN: 1664-042X
NlmUniqueID: 101549006
Country: Switzerland
Language: English
Volume: 8
Pages: 664
PII: 664

Researcher Affiliations

Pohlin, Friederike
  • Department of Integrative Biology and Evolution, Research Institute of Wildlife Ecology, University of Veterinary Medicine ViennaVienna, Austria.
Brabender, Kristin
  • Hortobagy National ParkHortobágy, Hungary.
Fluch, Gerhard
  • Department of Integrative Biology and Evolution, Research Institute of Wildlife Ecology, University of Veterinary Medicine ViennaVienna, Austria.
Stalder, Gabrielle
  • Department of Integrative Biology and Evolution, Research Institute of Wildlife Ecology, University of Veterinary Medicine ViennaVienna, Austria.
Petit, Thierry
  • Zoo de la PalmyreLes Mathes, France.
Walzer, Chris
  • Department of Integrative Biology and Evolution, Research Institute of Wildlife Ecology, University of Veterinary Medicine ViennaVienna, Austria.
  • Wildlife Conservation SocietyBronx, NY, United States.

References

This article includes 97 references
  1. Ackerman JT, Takekawa JY, Kruse KL, Orthmeyer DL, Yee JL, Ely CR. Using radiotelemetry to monitor cardiac response of free-living tule greater white-fronted geese (Anser albifrons elgasi) to human disturbance. Wilson Bull. 116, 146–151.
    doi: 10.1676/03-110google scholar: lookup
  2. Arnold W, Ruf T, Kuntz R. Seasonal adjustment of energy budget in a large wild mammal, the Przewalski horse (Equus ferus przewalskii) II. Energy expenditure.. J Exp Biol 2006 Nov;209(Pt 22):4566-73.
    doi: 10.1242/jeb.02536pubmed: 17079726google scholar: lookup
  3. Arnold W, Ruf T, Reimoser S, Tataruch F, Onderscheka K, Schober F. Nocturnal hypometabolism as an overwintering strategy of red deer (Cervus elaphus).. Am J Physiol Regul Integr Comp Physiol 2004 Jan;286(1):R174-81.
    doi: 10.1152/ajpregu.00593.2002pubmed: 12969877google scholar: lookup
  4. Battipaglia I, Lanza GA. The autonomic nervous system of the heart in slart, Autonomic Innervation of the Heart. Role of Molecular Imaging. 1st Edn, eds Riemer HJA, Tio RA, Elsinga PH, Schwaiger M (Berlin; Heidelberg: Springer; ), 1–12.
    doi: 10.1007/978-3-662-45074-1_1google scholar: lookup
  5. Berger A, Scheibe KM, Eichhorn K, Scheibe A, Streich J. Diurnal and ultradian rhythms of behaviour in a mare group of Przewalski horse (Equus ferus przewalskii), measured through one year under semi-reserve conditions. Appl. Anim. Behav. Sci. 64, 1–17.
    doi: 10.1016/S0168-1591(99)00026-Xgoogle scholar: lookup
  6. Boonstra R. Coping with changing northern environments: the role of the stress axis in birds and mammals.. Integr Comp Biol 2004 Apr;44(2):95-108.
    doi: 10.1093/icb/44.2.95pubmed: 21680490google scholar: lookup
  7. Boyd L, Houpt K. Przewalski's Horse: The History and Biology of an Endangered Species. Albany, NY: State University of New York Press.
  8. Buijs RM, la Fleur SE, Wortel J, Van Heyningen C, Zuiddam L, Mettenleiter TC, Kalsbeek A, Nagai K, Niijima A. The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons.. J Comp Neurol 2003 Sep 8;464(1):36-48.
    doi: 10.1002/cne.10765pubmed: 12866127google scholar: lookup
  9. Buller MJ, Tharion WJ, Cheuvront SN, Montain SJ, Kenefick RW, Castellani J, Latzka WA, Roberts WS, Richter M, Jenkins OC, Hoyt RW. Estimation of human core temperature from sequential heart rate observations.. Physiol Meas 2013 Jul;34(7):781-98.
    doi: 10.1088/0967-3334/34/7/781pubmed: 23780514google scholar: lookup
  10. Busch DS, Hayward LS. Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biol. Conserv. 142, 2844–2853.
    doi: 10.1016/j.biocon.2009.08.013google scholar: lookup
  11. Butler PJ, Green JA, Boyd IL, Speakman JR. Measuring meatabolic rate in the fiels: the pros and cons of the doubly labeled water and heart rate methods. Funct. Ecol. 18, 168–183.
    doi: 10.1111/j.0269-8463.2004.00821.xgoogle scholar: lookup
  12. Chrousos GP. Stress and disorders of the stress system.. Nat Rev Endocrinol 2009 Jul;5(7):374-81.
    doi: 10.1038/nrendo.2009.106pubmed: 19488073google scholar: lookup
  13. Dantzer B, Fletcher QE, Boonstra R, Sheriff MJ. Measures of physiological stress: a transparent or opaque window into the status, management and conservation of species?. Conserv Physiol 2014;2(1):cou023.
    doi: 10.1093/conphys/cou023pmc: PMC4732472pubmed: 27293644google scholar: lookup
  14. Esco MR, Flatt AA. Ultra-short-term heart rate variability indexes at rest and post-exercise in athletes: evaluating the agreement with accepted recommendations.. J Sports Sci Med 2014 Sep;13(3):535-41.
    pmc: PMC4126289pubmed: 25177179
  15. Evans AL, Singh NJ, Friebe A, Arnemo JM, Laske TG, Fröbert O, Swenson JE, Blanc S. Drivers of hibernation in the brown bear.. Front Zool 2016;13:7.
    doi: 10.1186/s12983-016-0140-6pmc: PMC4750243pubmed: 26870151google scholar: lookup
  16. Fowden AL, Comline RS, Silver M. Insulin secretion and carbohydrate metabolism during pregnancy in the mare.. Equine Vet J 1984 Jul;16(4):239-46.
    doi: 10.1111/j.2042-3306.1984.tb01919.xpubmed: 6383807google scholar: lookup
  17. Gehrke EK, Baldwin A, Schiltz PM. Heart rate variability in horses engaged in equine-assisted activities. J. Equine Vet. Sci. 31, 78–84.
    doi: 10.1016/j.jevs.2010.12.007google scholar: lookup
  18. Green JA. The heart rate method for estimating metabolic rate: review and recommendations.. Comp Biochem Physiol A Mol Integr Physiol 2011 Mar;158(3):287-304.
    doi: 10.1016/j.cbpa.2010.09.011pubmed: 20869457google scholar: lookup
  19. Groscolas R, Viera V, Guerin N, Handrich Y, Côté SD. Heart rate as a predictor of energy expenditure in undisturbed fasting and incubating penguins.. J Exp Biol 2010 Jan 1;213(1):153-60.
    doi: 10.1242/jeb.033720pubmed: 20008372google scholar: lookup
  20. Hadinger U, Haymerle A, Knauer F, Schwarzenberger F, Walzer C. Faecal cortisol metabolites to assess stress in wildlife: evaluation of a field method in free-ranging chamois. Methods Ecol. Evol. 6, 1349–1357.
    doi: 10.1111/2041-210X.12422google scholar: lookup
  21. Harlow HJ, Thorne ET, Williams ES, Belden EL, Gern WA. Cardiac frequency: a potential predictor of blood cortisol levels during acute and chronic stress exposure in Rocky Mountain bighorn sheep (Ovis canadensis canadensis). Can. J. Zool. 65, 2028–2034.
    doi: 10.1139/z87-308google scholar: lookup
  22. Hastings M, O'Neill JS, Maywood ES. Circadian clocks: regulators of endocrine and metabolic rhythms.. J Endocrinol 2007 Nov;195(2):187-98.
    doi: 10.1677/JOE-07-0378pubmed: 17951531google scholar: lookup
  23. Heldmaier G, Ortmann S, Elvert R. Natural hypometabolism during hibernation and daily torpor in mammals.. Respir Physiol Neurobiol 2004 Aug 12;141(3):317-29.
    doi: 10.1016/j.resp.2004.03.014pubmed: 15288602google scholar: lookup
  24. Hill LK, Siebenbrock A. Are all measures created equal? Heart rate variability and respiration - biomed 2009.. Biomed Sci Instrum 2009;45:71-6.
    pubmed: 19369742
  25. Huber S, Palme R, Arnold W. Effects of season, sex, and sample collection on concentrations of fecal cortisol metabolites in red deer (Cervus elaphus).. Gen Comp Endocrinol 2003 Jan;130(1):48-54.
    doi: 10.1016/S0016-6480(02)00535-Xpubmed: 12535624google scholar: lookup
  26. King SRB, Asa C, Pluhacek J, Houpt K, Ransom JI. Behaviour of horses, zebras, and asses, in Wild Equids: Ecology, Management, and Conservation. eds Ransom JI, Kacenczky P (Baltimore, MA: Johns Hopkins University Press; ), 23–40.
  27. King SRB, Boyd L, Zimmermann W, Kendall BE. Equus ferus ssp. przewalskii The IUCN Red List of Threatened Species. e.T7961AT97.
    doi: 10.2305/IUCN.UK.2015-2.RLTS.T7961A45172099.engoogle scholar: lookup
  28. Kinnunen S, Laukkanen R, Haldi J, Hanninen O, Atalay M. Heart rate variability in trotters during different training periods.. Equine Vet J Suppl 2006 Aug;(36):214-7.
    doi: 10.1111/j.2042-3306.2006.tb05542.xpubmed: 17402421google scholar: lookup
  29. Kolter L, Zimmermann W. Die Haltung von junggesellengruppen für das EEP-Przewalskipferd – Hengste in Gehegen und Reservaten. Z. Kölner Zoon 44, 135–151.
  30. Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E. Stress revisited: a critical evaluation of the stress concept.. Neurosci Biobehav Rev 2011 Apr;35(5):1291-301.
    doi: 10.1016/j.neubiorev.2011.02.003pubmed: 21316391google scholar: lookup
  31. Kovács L, Kézér FL, Ruff F, Szenci O. Cardiac autonomic activity has a circadian rhythm in summer but not in winter in non-lactating pregnant dairy cows.. Physiol Behav 2016 Mar 1;155:56-65.
    doi: 10.1016/j.physbeh.2015.11.031pubmed: 26639202google scholar: lookup
  32. Kuntz R, Kubalek C, Ruf T, Tataruch F, Arnold W. Seasonal adjustment of energy budget in a large wild mammal, the Przewalski horse (Equus ferus przewalskii) I. Energy intake.. J Exp Biol 2006 Nov;209(Pt 22):4557-65.
    doi: 10.1242/jeb.02535pubmed: 17079725google scholar: lookup
  33. Kuwahara M, Hiraga A, Kai M, Tsubone H, Sugano S. Influence of training on autonomic nervous function in horses: evaluation by power spectral analysis of heart rate variability.. Equine Vet J Suppl 1999 Jul;(30):178-80.
    doi: 10.1111/j.2042-3306.1999.tb05213.xpubmed: 10659247google scholar: lookup
  34. Kuwahara M, Suzuki A, Tsutsumi H, Tanigawa M, Tsubone H, Sugano S. Power spectral analysis of heart rate variability for assessment of diurnal variation of autonomic nervous activity in miniature swine.. Lab Anim Sci 1999 Apr;49(2):202-8.
    pubmed: 10331551
  35. Laborde S, Mosley E, Thayer JF. Heart Rate Variability and Cardiac Vagal Tone in Psychophysiological Research - Recommendations for Experiment Planning, Data Analysis, and Data Reporting.. Front Psychol 2017;8:213.
    doi: 10.3389/fpsyg.2017.00213pmc: PMC5316555pubmed: 28265249google scholar: lookup
  36. Landys MM, Ramenofsky M, Wingfield JC. Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes.. Gen Comp Endocrinol 2006 Sep 1;148(2):132-49.
    doi: 10.1016/j.ygcen.2006.02.013pubmed: 16624311google scholar: lookup
  37. Laske TG, Garshelis DL, Iaizzo PA. Monitoring the wild black bear's reaction to human and environmental stressors.. BMC Physiol 2011 Aug 17;11:13.
    doi: 10.1186/1472-6793-11-13pmc: PMC3177774pubmed: 21849079google scholar: lookup
  38. Lauenroth WK, Sala OE. Long-Term Forage Production of North American Shortgrass Steppe.. Ecol Appl 1992 Nov;2(4):397-403.
    doi: 10.2307/1941874pubmed: 27759270google scholar: lookup
  39. MacArthur RA, Johnston RH, Geist V. Factors influencing heart rate in free-ranging bighorn sheep: a physiological approach to the study of wildlife harassment. Can. J. Zool. 57, 2010–2021.
    doi: 10.1139/z79-265google scholar: lookup
  40. Makra Z. Przewalski's Horse Populations in Hungary, World Equine Veterinary Association - The Horse Magazine. .
  41. . Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology.. Eur Heart J 1996 Mar;17(3):354-81.
    doi: 10.1093/oxfordjournals.eurheartj.a014868pubmed: 8737210google scholar: lookup
  42. McEwen BS, Wingfield JC. The concept of allostasis in biology and biomedicine.. Horm Behav 2003 Jan;43(1):2-15.
    doi: 10.1016/S0018-506X(02)00024-7pubmed: 12614627google scholar: lookup
  43. Mentaberre G, López-Olvera JR, Casas-Díaz E, Fernández-Sirera L, Marco I, Lavín S. Effects of azaperone and haloperidol on the stress response of drive-net captured Iberian ibexes (Capra pyrenaica). Eur. J. Wildlife Res. 56, 757–764.
    doi: 10.1007/s10344-010-0371-3google scholar: lookup
  44. Mesteig K, Tyler NJ, Blix AS. Seasonal changes in heart rate and food intake in reindeer (Rangifer tarandus tarandus).. Acta Physiol Scand 2000 Oct;170(2):145-51.
    doi: 10.1046/j.1365-201x.2000.00767.xpubmed: 11114952google scholar: lookup
  45. Millspaugh JJ, Washburn BE. Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation.. Gen Comp Endocrinol 2004 Sep 15;138(3):189-99.
    doi: 10.1016/j.ygcen.2004.07.002pubmed: 15364201google scholar: lookup
  46. Moen AN. Seasonal changes in heart rates, activity, metabolism, and forage intake of white-tailed deer. J. Wildlife Manage. 42, 715–738.
    doi: 10.2307/3800763google scholar: lookup
  47. Mohr E, Langbein J, Nürnberg G. Heart rate variability: a noninvasive approach to measure stress in calves and cows.. Physiol Behav 2002 Feb 1-15;75(1-2):251-9.
    doi: 10.1016/S0031-9384(01)00651-5pubmed: 11890975google scholar: lookup
  48. Möstl E, Palme R. Hormones as indicators of stress.. Domest Anim Endocrinol 2002 Jul;23(1-2):67-74.
    doi: 10.1016/S0739-7240(02)00146-7pubmed: 12142227google scholar: lookup
  49. Munoz ML, van Roon A, Riese H, Thio C, Oostenbroek E, Westrik I, de Geus EJ, Gansevoort R, Lefrandt J, Nolte IM, Snieder H. Validity of (Ultra-)Short Recordings for Heart Rate Variability Measurements.. PLoS One 2015;10(9):e0138921.
    doi: 10.1371/journal.pone.0138921pmc: PMC4586373pubmed: 26414314google scholar: lookup
  50. Murphy BA. Chronobiology and the horse: recent revelations and future directions.. Vet J 2010 Aug;185(2):105-14.
    doi: 10.1016/j.tvjl.2009.04.013pubmed: 19427248google scholar: lookup
  51. Nagel C, Aurich J, Aurich C. Heart rate and heart rate variability in the pregnant mare and its foetus.. Reprod Domest Anim 2011 Dec;46(6):990-3.
    doi: 10.1111/j.1439-0531.2011.01772.xpubmed: 21382105google scholar: lookup
  52. Nagel C, Erber R, Bergmaier C, Wulf M, Aurich J, Möstl E, Aurich C. Cortisol and progestin release, heart rate and heart rate variability in the pregnant and postpartum mare, fetus and newborn foal.. Theriogenology 2012 Sep 1;78(4):759-67.
    doi: 10.1016/j.theriogenology.2012.03.023pubmed: 22626780google scholar: lookup
  53. Nussinovitch U, Elishkevitz KP, Katz K, Nussinovitch M, Segev S, Volovitz B, Nussinovitch N. Reliability of Ultra-Short ECG Indices for Heart Rate Variability.. Ann Noninvasive Electrocardiol 2011 Apr;16(2):117-22.
    doi: 10.1111/j.1542-474X.2011.00417.xpmc: PMC6932379pubmed: 21496161google scholar: lookup
  54. Parker M, Goodwin D, Eager RA, Redhead ES, Marlin DJ. Comparison of Polar heart rate interval data with simultaneously recorded ECG signals in horses. Comp. Exerc. Physiol. 6, 137–142.
    doi: 10.1017/S1755254010000024google scholar: lookup
  55. Pashen RL. Maternal and foetal endocrinology during late pregnancy and parturition in the mare.. Equine Vet J 1984 Jul;16(4):233-8.
    doi: 10.1111/j.2042-3306.1984.tb01918.xpubmed: 6383806google scholar: lookup
  56. Penttilä J, Helminen A, Jartti T, Kuusela T, Huikuri HV, Tulppo MP, Coffeng R, Scheinin H. Time domain, geometrical and frequency domain analysis of cardiac vagal outflow: effects of various respiratory patterns.. Clin Physiol 2001 May;21(3):365-76.
    doi: 10.1046/j.1365-2281.2001.00337.xpubmed: 11380537google scholar: lookup
  57. Physick-Sheard PW, Marlin DJ, Thornhill R, Schroter RC. Frequency domain analysis of heart rate variability in horses at rest and during exercise.. Equine Vet J 2000 May;32(3):253-62.
    doi: 10.2746/042516400776563572pubmed: 10836482google scholar: lookup
  58. Platt H. Growth of the equine foetus.. Equine Vet J 1984 Jul;16(4):247-52.
    doi: 10.1111/j.2042-3306.1984.tb01920.xpubmed: 6383808google scholar: lookup
  59. Plews DJ, Laursen PB, Stanley J, Kilding AE, Buchheit M. Training adaptation and heart rate variability in elite endurance athletes: opening the door to effective monitoring.. Sports Med 2013 Sep;43(9):773-81.
    doi: 10.1007/s40279-013-0071-8pubmed: 23852425google scholar: lookup
  60. Poljakov IS. Przewalski's horse (Equus przewalskii n. sp.). Isvestia Russki Geograph. Obs. St Petersburg 17, 1–20.
  61. Porges SW. Cardiac vagal tone: a physiological index of stress.. Neurosci Biobehav Rev 1995 Summer;19(2):225-33.
    doi: 10.1016/0149-7634(94)00066-Apubmed: 7630578google scholar: lookup
  62. Porges SW. Orienting in a defensive world: mammalian modifications of our evolutionary heritage. A Polyvagal Theory.. Psychophysiology 1995 Jul;32(4):301-18.
    pubmed: 7652107doi: 10.1111/j.1469-8986.1995.tb01213.xgoogle scholar: lookup
  63. Porges SW. The polyvagal perspective.. Biol Psychol 2007 Feb;74(2):116-43.
    doi: 10.1016/j.biopsycho.2006.06.009pmc: PMC1868418pubmed: 17049418google scholar: lookup
  64. Pumprla J, Howorka K, Groves D, Chester M, Nolan J. Functional assessment of heart rate variability: physiological basis and practical applications.. Int J Cardiol 2002 Jul;84(1):1-14.
    doi: 10.1016/S0167-5273(02)00057-8pubmed: 12104056google scholar: lookup
  65. Reeder DM, Kramer KM. Stress in free-ranging mammals: integrating physiology, ecology, and natural history. J. Mammal. 86, 225–235.
    doi: 10.1644/BHE-003.1google scholar: lookup
  66. Robbins CT, Robbins BL. Fetal and neonatal growth patterns and maternal reproductive effort in ungulates and subungulates. Am. Nat. 114, 101–116.
  67. Romero LM. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates.. Gen Comp Endocrinol 2002 Aug;128(1):1-24.
    doi: 10.1016/S0016-6480(02)00064-3pubmed: 12270784google scholar: lookup
  68. Ruf T, Heldmaier G. The impact of daily torpor on energy requirements in the Djungarian hamster, Phodopus sungorus. Physiol. Zool. 65, 994–1010.
    doi: 10.1086/physzool.65.5.30158554google scholar: lookup
  69. Rutz C, Hays GC. New frontiers in biologging science.. Biol Lett 2009 Jun 23;5(3):289-92.
    doi: 10.1098/rsbl.2009.0089pmc: PMC2679933pubmed: 19324624google scholar: lookup
  70. Ryder OA. Przewalski's horse: prospects for reintroduction into the wild. Conserv. Biol. 7, 13–15.
    doi: 10.1046/j.1523-1739.1993.07010013.xgoogle scholar: lookup
  71. Ryder OA, Wedemeyer EA. A cooperative breeding programme for the Mongolian wild horse Equus przewalskii in the United States. Biol. Conserv. 22, 259–271.
  72. Saboul D, Pialoux V, Hautier C. The impact of breathing on HRV measurements: implications for the longitudinal follow-up of athletes.. Eur J Sport Sci 2013;13(5):534-42.
    doi: 10.1080/17461391.2013.767947pubmed: 24050471google scholar: lookup
  73. Satué K, Domingo R. Longitudinal study of the renin angiotensin aldosterone system in purebred Spanish broodmares during pregnancy.. Theriogenology 2011 Apr 15;75(7):1185-94.
    doi: 10.1016/j.theriogenology.2010.11.029pubmed: 21220157google scholar: lookup
  74. Schwarzenberger F. The many uses of non-invasive faecal steroid monitoring in zoo and wildlife species. Int. Zoo Yearbook 41, 52–74.
    doi: 10.1111/j.1748-1090.2007.00017.xgoogle scholar: lookup
  75. Selye H. A syndrome produced by diverse nocuous agents. 1936.. J Neuropsychiatry Clin Neurosci 1998 Spring;10(2):230-1.
    pubmed: 9722327doi: 10.1176/jnp.10.2.230agoogle scholar: lookup
  76. Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R. Measuring stress in wildlife: techniques for quantifying glucocorticoids.. Oecologia 2011 Aug;166(4):869-87.
    doi: 10.1007/s00442-011-1943-ypubmed: 21344254google scholar: lookup
  77. Sooyoung Sim, Heenam Yoon, Hosuk Ryou, Kwangsuk Park. Estimation of body temperature rhythm based on heart activity parameters in daily life.. Annu Int Conf IEEE Eng Med Biol Soc 2014;2014:2245-8.
    doi: 10.1109/EMBC.2014.6944066pubmed: 25570434google scholar: lookup
  78. Singh RB, Weydahl A, Otsuka K, Watanabe Y, Yano S, Mori H, Ichimaru Y, Mitsutake G, Sato Y, Fanghong L, Zhao ZY, Kartik C, Gvozdjakova A. Can nutrition influence circadian rhythm and heart rate variability?. Biomed Pharmacother 2001;55 Suppl 1:115s-124s.
    doi: 10.1016/S0753-3322(01)90016-2pubmed: 11774858google scholar: lookup
  79. Souris AC, Kaczensky P, Julliard R, Walzer C. Time budget-, behavioral synchrony- and body score development of a newly released Przewalski's horse group Equus ferus przewalskii, in the Great Gobi B Strictly Protected Area in SW Mongolia.. Appl Anim Behav Sci 2007 Nov;107(3-4):307-321.
    doi: 10.1016/j.applanim.2006.09.023pmc: PMC3207227pubmed: 22064904google scholar: lookup
  80. Støen OG, Ordiz A, Evans AL, Laske TG, Kindberg J, Fröbert O, Swenson JE, Arnemo JM. Physiological evidence for a human-induced landscape of fear in brown bears (Ursus arctos).. Physiol Behav 2015 Dec 1;152(Pt A):244-8.
    doi: 10.1016/j.physbeh.2015.09.030pubmed: 26476156google scholar: lookup
  81. Stucke D, Große Ruse M, Lebelt D. Measuring heart rate variability in horses to investigate the autonomic nervous system activity – Pros and cons of different methods. Appl. Anim. Behav. Sci. 166, 1–10.
    doi: 10.1016/j.applanim.2015.02.007google scholar: lookup
  82. Tarlow EM, Blumstein DT. Evaluating methods to quantify anthropogenic stressors on wild animals. Appl. Anim. Behav. Sci. 102, 429–451.
    doi: 10.1016/j.applanim.2006.05.040google scholar: lookup
  83. Theil PK, Coutant AE, Olesen CR. Seasonal changes and activity-dependent variation in heart rate of Roe Deer. J. Mammal. 85, 245–325.
    doi: 10.1644/1545-1542(2004)085<0245:SCAAVI>2.0.CO;2google scholar: lookup
  84. Touma C, Palme R. Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation.. Ann N Y Acad Sci 2005 Jun;1046:54-74.
    doi: 10.1196/annals.1343.006pubmed: 16055843google scholar: lookup
  85. Vandewalle G, Middleton B, Rajaratnam SM, Stone BM, Thorleifsdottir B, Arendt J, Dijk DJ. Robust circadian rhythm in heart rate and its variability: influence of exogenous melatonin and photoperiod.. J Sleep Res 2007 Jun;16(2):148-55.
    doi: 10.1111/j.1365-2869.2007.00581.xpubmed: 17542944google scholar: lookup
  86. von Borell E, Langbein J, Després G, Hansen S, Leterrier C, Marchant J, Marchant-Forde R, Minero M, Mohr E, Prunier A, Valance D, Veissier I. Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals -- a review.. Physiol Behav 2007 Oct 22;92(3):293-316.
    doi: 10.1016/j.physbeh.2007.01.007pubmed: 17320122google scholar: lookup
  87. Wakefield S, Zimmermann W, Van Dierendonck MC. Status and action plan for the przewalski's horse (Equus ferus przewalskii), in Equids: Zebras, Asses and Horses. IUCN/SCC Equid Specialist Group, ed Moehlman P (Cambridge: IUCN Publication Services Unit; ), 82–92.
  88. Walzer C, Stalder G, Petit T, Sos E, Molnar V, Brabender K. Surgical field anesthesia in Przewalski's horse (Equus ferus przewalskii) in Hortobagy national park, in Hungary AAZV Annual Conference. .
  89. Weimerskirch H, Shaffer SA, Mabille G, Martin J, Boutard O, Rouanet JL. Heart rate and energy expenditure of incubating wandering albatrosses: basal levels, natural variation, and the effects of human disturbance.. J Exp Biol 2002 Feb;205(Pt 4):475-83.
    doi: 10.1385/1592591639pubmed: 11893761google scholar: lookup
  90. Weiner J. Energy metabolism of the roe deer. Acta Theriol. 22, 3–24.
    doi: 10.4098/AT.arch.77-1google scholar: lookup
  91. Weisenberger ME, Krausman PR, Wallace MC, DeYoung DW, Maughan OE. Effects of simulated jet aircraft noise on heart rate and behavior of desert ungulates. J. Wildlife Manage. 60, 52–61.
    doi: 10.2307/3802039google scholar: lookup
  92. Werger MJA, VanStaalduinen MA. Eurasian Steppes. Ecological Problems and Livelihoods in a Changing World. Dordrecht: Springer Netherlands.
  93. White GC, Garrott RA. Analysis of Wildlife Radio- Tracking Data. San Diego, CA: Academic Press.
  94. Wikelski M, Cooke SJ. Conservation physiology.. Trends Ecol Evol 2006 Jan;21(1):38-46.
    doi: 10.1016/j.tree.2005.10.018pubmed: 16701468google scholar: lookup
  95. Zimmermann W. Przewalski's horses on the track to reintroduction- various projects compared. Z. Kölner Zoon 48, 183–209.
  96. Zimmermann W, Brabender K, Kolter L. A Przewalski's Horse Population in a Unique European Steppe Reserve – the Hortobágy Nationalpark in Hungary, Symposium proceedings Equus. Praha Zoon 257–288.
  97. Zimmermann W, Sandor I, Brabender K. Naturschutzprojekt Hortobágy – Jahresbericht 2008. Z. Kölner Zoon 52, 47–60.

Citations

This article has been cited 11 times.
  1. Leimgruber P, Songsasen N, Stabach JA, Horning M, Reed D, Buk T, Harwood A, Layman L, Mathews C, Vance M, Marinari P, Helmick KE, Delaski KM, Ware LH, Jones JC, Silva JLP, Laske TG, Moraes RN. Providing baseline data for conservation-Heart rate monitoring in captive scimitar-horned oryx. Front Physiol 2023;14:1079008.
    doi: 10.3389/fphys.2023.1079008pubmed: 36909234google scholar: lookup
  2. Seeley KE, Proudfoot KL, Edes AN. The application of allostasis and allostatic load in animal species: A scoping review. PLoS One 2022;17(8):e0273838.
    doi: 10.1371/journal.pone.0273838pubmed: 36040981google scholar: lookup
  3. Fu M, Guo J, Zhang Y, Zhao Y, Zhang Y, Hou Z, Wang Z. Effect of integrated management bundle on 1-year overall survival outcomes and perioperative outcomes in super elderly patients aged 90 and over with hip fracture: non-concurrent cohort study. BMC Musculoskelet Disord 2022 Aug 15;23(1):778.
    doi: 10.1186/s12891-022-05720-zpubmed: 35971104google scholar: lookup
  4. Mayer M, Lian M, Fuchs B, Robstad CA, Evans AL, Perrin KL, Greunz EM, Laske TG, Arnemo JM, Rosell F. Retention and loss of PIT tags and surgically implanted devices in the Eurasian beaver. BMC Vet Res 2022 Jun 10;18(1):219.
    doi: 10.1186/s12917-022-03333-1pubmed: 35689280google scholar: lookup
  5. Rauch H, Pohlin F, Einwaller J, Habe M, Gasch K, Haw A, Arnold W, Stalder G, Painer J. Effect of season and diet on heart rate and blood pressure in female red deer (Cervus elaphus) anaesthetised with medetomidine-tiletamine-zolazepam. PLoS One 2022;17(6):e0268811.
    doi: 10.1371/journal.pone.0268811pubmed: 35671269google scholar: lookup
  6. Moraes RN, Laske TG, Leimgruber P, Stabach JA, Marinari PE, Horning MM, Laske NR, Rodriguez JV, Eye GN, Kordell JE, Gonzalez M, Eyring T, Lemons C, Helmick KE, Delaski KM, Ware LH, Jones JC, Songsasen N. Inside out: heart rate monitoring to advance the welfare and conservation of maned wolves (Chrysocyon brachyurus). Conserv Physiol 2021;9(1):coab044.
    doi: 10.1093/conphys/coab044pubmed: 34188936google scholar: lookup
  7. Twiss SD, Brannan N, Shuert CR, Bishop AM, Pomeroy PP, Moss S. An external telemetry system for recording resting heart rate variability and heart rate in free-ranging large wild mammals. PLoS One 2021;16(6):e0252013.
    doi: 10.1371/journal.pone.0252013pubmed: 34086713google scholar: lookup
  8. Twiss SD, Shuert CR, Brannan N, Bishop AM, Pomeroy PP. Reactive stress-coping styles show more variable reproductive expenditure and fitness outcomes. Sci Rep 2020 Jun 12;10(1):9550.
    doi: 10.1038/s41598-020-66597-3pubmed: 32533041google scholar: lookup
  9. Oishi K, Himeno Y, Miwa M, Anzai H, Kitajima K, Yasunaka Y, Kumagai H, Ieiri S, Hirooka H. Correcting the Activity-Specific Component of Heart Rate Variability Using Dynamic Body Acceleration Under Free-Moving Conditions. Front Physiol 2018;9:1063.
    doi: 10.3389/fphys.2018.01063pubmed: 30131717google scholar: lookup
  10. Shuert CR, Pomeroy PP, Twiss SD. Stress-coping styles are associated with energy budgets and variability in energy management strategies in a capital breeder. Proc Biol Sci 2025 May;292(2046):20241787.
    doi: 10.1098/rspb.2024.1787pubmed: 40359978google scholar: lookup
  11. Ishimaru M, Tsuchiya T, Endo Y, Matsui A, Ohmura H, Murase H, Korosue K, Sato F, Taya K. Effects of different winter paddock management of Thoroughbred weanlings and yearlings in the cold region of Japan on physiological function, endocrine function and growth. J Vet Med Sci 2024 Jul 2;86(7):756-768.
    doi: 10.1292/jvms.24-0083pubmed: 38777756google scholar: lookup
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