Abstract
To reverse the trend of declining wildlife populations globally, individuals must be provided with conditions that allow them to not just survive, but to thrive. It is no longer only the remit of captive breeding programs to ensure animal well-being; in situ conservation efforts also must consider how environmental and anthropogenic pressures impact wild populations, and how to mitigate them—especially with regards to reproduction and survival. Stress and welfare are complex concepts that necessitate an understanding of how stressors affect animals on both individual and population levels. There are species differences in how factors impact well-being, related in part to natural history, which also are shaped by individual perceptions and coping abilities. A multitude of stress-related responses then have the potential to disrupt fertility on many levels, and ultimately fitness. A major limitation to advancing welfare science is the lack of definitive tests to verify welfare status; i.e., is the animal happy or not? While analyses of circulating or excreted glucocorticoids have for decades been the primary method of assessing stress, today we recognize the need for more objective indicators that incorporate multiple physiological systems, including behavior, to assess both negative and positive welfare states. In this chapter, we discuss the potential for stress to disrupt, and sometimes facilitate reproduction, including the key role that glucocorticoids play. We then discuss a number of physiological biomarkers, which in addition to glucocorticoids, have the potential to assess well-being and the role of stress on reproduction. Finally, we discuss allostatic load, a method by which multiple physiological markers are used to inform on morbidity and mortality risk in humans, which if applied to wildlife, could be a powerful tool for conservation.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Medoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T, Sapolsky RM. Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav. 2003;43:67–82.
Accardi M, Boulay E, Pouliot M, Maghezzi S, Forster R, Authier S. qEEG as a biomarker of animal welfare: assessing the influence of different caging. J Pharmacol Toxicol Methods. 2017;88:193–4.
Accortt EE, Mirocha J, Schetter CD, Hobel CJ. Adverse perinatal outcomes and postpartum multi-systemic dysregulation. Matern Child Health J. 2017;21:398–406.
Adamec T, Kunc P, Knížková I, Dolejš J, Toufar O. By evaporative cooling in summer session is possible to improve growth and feed conversion in pig fattening. In: 48th annual meeting of EAAP, Vienna, Austria; 1998. p. 219–20.
Adesiyun AA, Caesar K, Inder L. Prevalence of Salmonella and Campylobacter species in animals at Emperor Valley Zoo, Trinidad. J Zoo Wildl Med. 1998;29:237–9.
Aerts J, Metz JR, Ampe B, Decostere A, Flik G, De Saeger S. Scales tell a story on the stress history of fish. PLoS One. 2015;10:e0123411.
Agnew RC, Smith VJ, Fowkes RC. Wind turbines cause chronic stress in badgers (Meles meles) in Great Britain. J Wildl Dis. 2016;52:459–67.
Akiyoshi H, Aoki M, Shimada T, Noda K, Kumagai D, Saleh N, Sugii S, Ohashi F. Measurement of plasma chromogranin A concentrations for assessment of stress responses in dogs with insulin-induced hypoglycemia. Am J Vet Res. 2005;66:1830–5.
Ali N, Pruessner JC. The salivary alpha amylase over cortisol ratio as a marker to assess dysregulations of the stress systems. Physiol Behav. 2012;106:65–72.
Alley DE, Seeman TE, Kim JK, Karlamangla A, Hu P, Crimmins EM. Socioeconomic status and C-reactive protein levels in the US population: NHANES IV. Brain Behav Immun. 2006;20:498–504.
Almeida P, Weber P, Burton J, Zanella A. Depressed DHEA and increased sickness response behaviors in lame dairy cows with inflammatory foot lesions. Domest Anim Endocrinol. 2008;34:89–99.
Al-Murrani W, Al-Rawi I, Raof N. Genetic resistance to Salmonella typhimurium in two lines of chickens selected as resistant and sensitive on the basis of heterophil/lymphocyte ratio. Br Poultry Sci. 2002;43:501–7.
Al-Murrani W, Al-Rawi A, Al-Hadithi M, Al-Tikriti B. Association between heterophil/lymphocyte ratio, a marker of ‘resistance’to stress, and some production and fitness traits in chickens. Br Poultry Sci. 2006;47:443–8.
Altschul DM, Hopkins WD, Herrelko ES, Inoue-Murayama M, Matsuzawa T, King JE, Ross SR, Weiss A. Personality links with lifespan in chimpanzees. Elife. 2018;7:e33781.
Anderson B, Watson D, Colditz I. The effect of dexamethasone on some immunological parameters in cattle. Vet Res Commun. 1999;23:399–413.
Anestis SF. Urinary cortisol responses to unusual events in captive chimpanzees (Pan troglodytes). Stress. 2009;12:49–57.
Angelier F, Chastel O. Stress, prolactin and parental investment in birds: a review. Gen Comp Endocrinol. 2009;163:142–8.
Ange-van Heugten KD, van Heugten E, Timmer S, Bosch G, Elias A, Whisnant S, Swarts HJM, Ferket P, Verstegen MWA. Fecal and salivary cortisol concentrations in woolly (Lagothrix ssp.) and spider monkeys (Ateles spp.). Int J Zool. 2009;2009:1–9.
Archie EA, Tung J, Clark M, Altmann J, Alberts SC. Social affiliation matters: both same-sex and opposite-sex relationships predict survival in wild female baboons. Proc R Soc Lond B. 2014;281:1–9.
Armario A, Restrepo C, Hidalgo J, Lopez-Calderon A. Differences in prolactin and LH responses to acute stress between peripuberal and adult male rats. J Endocrinol. 1987;112:9–13.
Arthington J, Eicher S, Kunkle W, Martin F. Effect of transportation and commingling on the acute-phase protein response, growth, and feed intake of newly weaned beef calves. J Anim Sci. 2003;81:1120–5.
Ashley PJ, Ringrose S, Edwards KL, Wallington E, McCrohan CR, Sneddon LU. Effect of noxious stimulation upon antipredator responses and dominance status in rainbow trout. Anim Behav. 2009;77:403–10.
Atkins L, Zong J-C, Tan J, Mejia A, Heaggans SY, Nofs SA, Stanton JJ, Flanagan JP, Howard L, Latimer E, Stevens MR, Hoffman DS, Hayward GS, Ling PD. Elephant endotheliotropic herpesvirus 5, a newly recognized elephant herpesvirus associated with clinical and subclinical infections in captive Asian elephants (Elephas maximus). J Zoo Wildl Med. 2013;44:136–43.
Atkinson HC, Waddell BJ. The hypothalamic-pituitary-adrenal axis in rat pregnancy and lactation: circadian variation and interrelationship of plasma adrenocorticotropin and corticosterone. Endocrinology. 1995;136:512–20.
Ball K, Berch DB, Helmers KF, Jobe JB, Leveck MD, Marsiske M, Morris JN, Rebok GW, Smith DM, Tennstedt SL, Unverzagt FW, Willis SL. Effects of cognitive training interventions with older adults. JAMA. 2002;288:2271–81.
Ballard PL, Ballard RA. Glucocorticoid receptors and the role of glucocorticoids in fetal lung development. Proc Natl Acad Sci U S A. 1972;69:2668–72.
Ballard PL, Baxter JD, Higgins SJ, Rousseau GG, Tomkins GM. General presence of glucocorticoid receptors in mammalian tissues. Endocrinology. 1974;94:998–1002.
Barboza Solís C, Kelly-Irving M, Fantin R, Darnaudéry M, Torrisani J, Lang T, Delpierre C. Adverse childhood experiences and physiological wear-and-tear in midlife: findings from the 1958 British birth cohort. Proc Natl Acad Sci U S A. 2015;112:E738–E46.
Barker DJP. The fetal and infant origins of adult disease. Br Med J. 1992;301:1111.
Barker DJP. The developmental origins of adult disease. Eur J Epidemiol. 2003;18:733–6.
Barreto RE, Volpato GL. Ventilation rates indicate stress-coping styles in Nile tilapia. J Biosci. 2011;36:851–5.
Barrett ES, Vitek W, Mbowe O, Thurston SW, Legro RS, Alvero R, Baker V, Bates GW, Casson P, Coutifaris C, Eisenberg E, Hansen K, Krawetz S, Robinson R, Rosen M, Usadi R, Zhang H, Santoro N, Diamond M. Allostatic load, a measure of chronic physiological stress, is associated with pregnancy outcomes, but not fertility, among women with unexplained infertility. Hum Reprod. 2018;33:1757–66.
Barron AB, Klein C. What insects can tell us about the origins of consciousness. Proc Natl Acad Sci U S A. 2016;113:4900–8.
Barron DG, Brawn JD, Butler LK, Romero LM, Weatherhead PJ. Effects of military activity on breeding birds. J Wildl Manage. 2012;76:911–8.
Bartolomucci A, Pasinetti G, Salton S. Granins as disease-biomarkers: translational potential for psychiatric and neurological disorders. Neuroscience. 2010;170:289–97.
Baxter-Gilbert JH, Riley JL, Mastromonaco GF, Litzgus JD, Lesbarrères D. A novel technique to measure chronic levels of corticosterone in turtles living around a major roadway. Conserv Physiol. 2014;2:cou036.
Bechshøft TØ, Sonne C, Rigét FF, Letcher RJ, Novak MA, Henchey E, Meyer JS, Eulaers I, Jaspers VL, Covaci A. Polar bear stress hormone cortisol fluctuates with the North Atlantic oscillation climate index. Polar Biol. 2013;36:1525–9.
Beck EM, Smits JE, St. Clair CC. Health of domestic mallards (Anas platyrhynchos domestica) following exposure to oil sands process-affected water. Environ Sci Technol. 2014;48:8847–54.
Beckie TM. A systematic review of allostatic load, health, and health disparities. Biol Res Nurs. 2012;14:311–46.
Beerda B, Schilder MBH, van Hooff J, de Vries HW, Mol JA. Behavioural and hormonal indicators of enduring environmental stress in dogs. Anim Welf. 2000;9:49–62.
Behringer V, Deschner T, Möstl E, Selzer D, Hohmann G. Stress affects salivary alpha-amylase activity in bonobos. Physiol Behav. 2012;105:476–82.
Behringer V, Borchers C, Deschner T, Möstl E, Selzer D, Hohmann G. Measurements of salivary alpha amylase and salivary cortisol in hominoid primates reveal within-species consistency and between-species differences. PLoS One. 2013;8:e60773.
Benhaiem S, Hofer H, Dehnhard M, Helms J, East ML. Sibling competition and hunger increase allostatic load in spotted hyaenas. Biol Lett. 2013;9:1–4.
Benn AL, McLelland DJ, Whittaker AL. A review of welfare assessment methods in reptiles, and preliminary application of the welfare quality(R) protocol to the pygmy blue-tongue skink, tiliqua adelaidensis, using animal-based measures. Animals. 2019;9:22.
Bennett C, Fripp D, Othen L, Jarsky T, French J, Loskutoff N. Urinary corticosteroid excretion patterns in the okapi (Okapia johnstoni). Zoo Biol. 2008;27:381–93.
Berg MT, Simons RL, Barr A, Beach SRH, Philibert RA. Childhood/adolescent stressors and allostatic load in adulthood: support for a calibration model. Soc Sci Med. 2017;193:130–9.
Berk LS, Tan SA, Fry WF, Napier BJ, Lee JW, Hubbard RW, Lewis JE, Eby WC. Neuroendocrine and stress hormone changes during mirthful laughter. Am J Med Sci. 1989;298:390–6.
Berkvens CN, Hyatt C, Gilman C, Pearl DL, Barker IK, Mastromonaco GF. Validation of a shed skin corticosterone enzyme immunoassay in the African house snake (Lamprophis fuliginosus) and its evaluation in the eastern massasauga rattlesnake (Sistrurus catenatus catenatus). Gen Comp Endocrinol. 2013;194:1–9.
Bernard C. An introduction to the study of experimental medicine. New York: Dover; 1865.
Bernton E, Hoover D, Galloway R, Popp K. Adaptation to chronic stress in military trainees: adrenal androgens, testosterone, glucocorticoids, IGF-1, and immune function. Ann N Y Acad Sci. 1995;774:217–31.
Berntson GG, Boysen ST. Specificity of the cardiac response to conspecific vocalizations in chimpanzees. Behav Neurosci. 1989;103:235–45.
Beuving G, Blokhuis HJ. Effect of novelty and restraint on catecholamines in plasma of laying hens. Br Poultry Sci. 1997;38:297–300.
Bilandžić N, Žurić M, Lojkić M, Šimić B, Milić D, Barač I. Cortisol and immune measures in boars exposed to three-day administration of exogenous adrenocorticotropic hormone. Vet Res Commun. 2006;30:433–44.
Blas J, Baos R, Bortolotti GR, Marchant TA, Hiraldo F. Age-related variation in the adrenocortical response to stress in nestling white storks (Ciconia ciconia) supports the developmental hypothesis. Gen Comp Endocrinol. 2006;148:172–80.
Boissy A, Manteuffel G, Jensen MB, Moe RO, Spruijt B, Keeling LJ, Winckler C, Forkman B, Dimitrov I, Langbein J. Assessment of positive emotions in animals to improve their welfare. Physiol Behav. 2007;92:375–97.
Boivin J, Sanders K, Schmidt L. Age and social position moderate the effect of stress on fertility. Evol Hum Behav. 2006;27:345–56.
Bolhuis JE, Parmentier HK, Schouten WG, Schrama JW, Wiegant VM. Effects of housing and individual coping characteristics on immune responses of pigs. Physiol Behav. 2003;79:289–96.
Bonier F, Martin PR, Moore IT, Wingfield JC. Do baseline glucocorticoids predict fitness? Trends Ecol Evol. 2009;24:634–42.
Booij SH, Bos EH, Bouwmans ME, van Faassen M, Kema IP, Oldehinkel AJ, de Jonge P. Cortisol and α-amylase secretion patterns between and within depressed and non-depressed individuals. PLoS One. 2015;10:e0131002.
Boomsma CM, Keay SD, Macklon NS. Peri-implantation glucocorticoid administration for assisted reproductive technology cycles. Cochrane Database Syst Rev. 2007;6:CD005996.
Boonstra R, Hik D, Singleton GR, Tinnikov A. The impact of predator-induced stress on the snowshoe hare cycle. Ecol Monogr. 1998;68:371–94.
Boonstra R, McColl CJ, Karels TJ. Reproduction at all costs: the adaptive stress response of male Arctic ground squirrels. Ecology. 2001;82:1930–46.
Booth T, Royle NA, Corley J, Gow AJ, Valdés Hernádez Mdel C, Maniega SM, Ritchie SJ, Bastin ME, Starr JM, Wardlaw JM, Deary IJ. Association of allostatic load with brain structure and cognitive ability in later life. Neurobiol Aging. 2015;36:1390–9.
Borrell LN, Crawford ND. Social disparities in periodontitis among US adults: the effect of allostatic load. J Epidemiol Community Health. 2011;65:144–9.
Borrell LN, Dallo FJ, Nguyen N. Racial/ethnic disparities in all-cause mortality in U.S. adults: the effect of allostatic load. Public Health Rep. 2010;125:810–6.
Bortolotti GR, Marchant TA, Blas J, German T. Corticosterone in feathers is a long-term, integrated measure of avian stress physiology. Funct Ecol. 2008;22:494–500.
Bosch JA, Brand HS, Ligtenberg TJ, Bermond B, Hoogstraten J, Amerongen AVN. Psychological stress as a determinant of protein levels and salivary-induced aggregation of Streptococcus gordonii in human whole saliva. Psychosom Med. 1996;58:374–82.
Bosch J, Brand H, Ligtenberg A, Bermond B, Hoogstraten J, Nieuw Amerongen A. The response of salivary protein levels and S-IgA to an academic examination are associated with daily stress. J Psychophysiol. 1998;12:384–91.
Bosch JA, de Geus EJ, Veerman EC, Hoogstraten J, Amerongen AVN. Innate secretory immunity in response to laboratory stressors that evoke distinct patterns of cardiac autonomic activity. Psychosom Med. 2003;65:245–58.
Braden A, Moule G. Effects of stress on ovarian morphology and oestrus cycles in ewes. Aust J Agr Res. 1964;15:937–49.
Brann DW, Mahesh VB. Regulation of gonadotropin secretion by steroid hormones. Front Neuroendocrinol. 1991a;12:165–207.
Brann DW, Mahesh VB. Role of corticosteroids in female reproduction. FASEB J. 1991b;5:2691–8.
Brann DW, Putnam CD, Mahesh VB. Corticosteroid regulation of gonadotropin and prolactin secretion in the rat. Endocrinology. 1990;126:159–66.
Brann DW, Putnam CD, Mahesh VB. Validation of the mechanisms proposed for the stimulatory and inhibitory effects of progesterone on gonadotropin secretion in the estrogenprimed rat: a possible role for adrenal steroids. Steroids. 1991;56:103–11.
Brann DW, Putnam CD, Mahesh VB. Regulation of follicle stimulating hormone secretion by natural and synthetic corticosteroids. In: Hunzicker-Dunn M, Schwartz NB, editors. Follicle stimulating hormone. New York: Springer; 1992. p. 303–9.
Brearley G, McAlpine C, Bell S, Bradley A. Influence of urban edges on stress in an arboreal mammal: a case study of squirrel gliders in southeast Queensland, Australia. Landsc Ecol. 2012;27:1407–19.
Breuner CW. Stress and reproduction in birds. In: David ON, Kristin HL, editors. Hormones and reproduction of vertebrates. London: Academic Press; 2011. p. 129–51.
Breuner CW, Patterson SH, Hahn TP. In search of relationships between the acute adrenocortical response and fitness. Gen Comp Endocrinol. 2008;157:288–95.
Briski KP, Sylvester PW. Effect of specific acute stressors on luteinizing hormone release in ovariectomized and ovariectomized estrogen-treated female rats. Neuroendocrinology. 1988;47:194–202.
Broom DM. Indicators of poor welfare. Br Vet J. 1986;142:524–6.
Brown C. Fish intelligence, sentience and ethics. Anim Cogn. 2015;18:1–17.
Brown JL, Kersey DC, Freeman EW, Wagener T. Assessment of diurnal urinary cortisol excretion in Asian and African elephants using different endocrine methods. Zoo Biol. 2010;29:274–83.
Brown JL, Paris S, Prado-Oviedo NA, Meehan CL, Hogan JN, Morfeld KA, Carlstead K. Reproductive health assessment of female elephants in North American zoos and association of husbandry practices with reproductive dysfunction in African elephants (Loxodonta africana). PLoS One. 2016;11:e0145673.
Bryan HM, Darimont CT, Paquet PC, Wynne-Edwards KE, Smits JE. Stress and reproductive hormones reflect inter-specific social and nutritional conditions mediated by resource availability in a bear–salmon system. Conserv Physiol. 2014;2:cou010.
Bryan HM, Smits JE, Koren L, Paquet PC, Wynne-Edwards KE, Musiani M. Heavily hunted wolves have higher stress and reproductive steroids than wolves with lower hunting pressure. Funct Ecol. 2015;29:347–56.
Brydon L, Edwards S, Mohamed-Ali V, Steptoe A. Socioeconomic status and stress-induced increases in interleukin-6. Brain Behav Immun. 2004;18:281–90.
Bundgaard CJ, Kalliokoski O, Abelson KS, Hau J. Acclimatization of mice to different cage types and social groupings with respect to fecal secretion of IgA and corticosterone metabolites. In Vivo. 2012;26:883–8.
Burgess EA, Hunt KE, Kraus SD, Rolland RM. Adrenal responses of large whales: integrating fecal aldosterone as a complementary biomarker to glucocorticoids. Gen Comp Endocrinol. 2017;252:103–10.
Burgess EA, Hunt KE, Kraus SD, Rolland RM. Quantifying hormones in exhaled breath for physiological assessment of large whales at sea. Sci Rep. 2018;8:10031.
Burke T, Page B, Van Dyk G, Millspaugh J, Slotow R. Risk and ethical concerns of hunting male elephant: behavioural and physiological assays of the remaining elephants. PLoS One. 2008;3:e2417.
Burks KD, Mellen JD, Miller GW, Lehnhardt J, Weiss A, Figueredo A, Maple TL. Comparison of two introduction methods for African elephants (Loxodonta africana). Zoo Biol. 2004;23:109–26.
Burn CC. Bestial boredom: a biological perspective on animal boredom and suggestions for its scientific investigation. Anim Behav. 2017;130:141–51.
Burnard C, Ralph C, Hynd P, Edwards JH, Tilbrook A. Hair cortisol and its potential value as a physiological measure of stress response in human and non-human animals. Anim Prod Sci. 2017;57:401–14.
Busch DS, Hayward LS. Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biol Conserv. 2009;142:2844–53.
Buwalda B, Scholte J, de Boer SF, Coppens CM, Koolhaas JM. The acute glucocorticoid stress response does not differentiate between rewarding and aversive social stimuli in rats. Horm Behav. 2012;61:218–26.
Cabagna MC, Lajmanovich RC, Stringhini G, Sanchez-Hernandez JC, Peltzer PM. Hematological parameters of health status in the common toad Bufo arenarum in agroecosystems of Santa Fe Province, Argentina. Appl Herpetol. 2005;2:373–80.
Cameron EZ, Ryan SJ. Welfare at multiple scales: importance of zoo elephant population welfare in a world of declining wild populations. PLoS One. 2016;11:e0158701.
Cannon WB. Bodily changes in pain, hunger, fear and rage: an account of recent researches into the function of emotional excitement. New York: Appleton; 1929.
Cannon WB. The wisdom of the body. New York: W.W. Norton; 1932.
Capiro JM, Stoops MA, Freeman EW, Clawson D, Schook MW. Effects of management strategies on glucocorticoids and behavior in Indian rhinoceros (Rhinoceros unicornis): translocation and operant conditioning. Zoo Biol. 2014;33:131–43.
Cardinet G, Littrell J, Schalm O. Effects of sustained muscular activity upon blood morphology of the horse. Calif Vet. 1964;18:31–5.
Carlitz EH, Miller R, Kirschbaum C, Gao W, Hänni DC, van Schaik CP. Measuring hair cortisol concentrations to assess the effect of anthropogenic impacts on wild chimpanzees (Pan troglodytes). PLoS One. 2016;11:e0151870.
Carlstead K, Brown JL. Relationships between patterns of fecal corticoid excretion and behavior, reproduction and environmental factors in captive black (Diceros bicornis) and white (Ceratotherium simum) rhinoceros. Zoo Biol. 2005;24:215–32.
Carlstead K, Shepherdson D. Effects of environmental enrichment on reproduction. Zoo Biol. 1994;13:447–58.
Carlstead K, Brown J, Seidensticker J. Behavioral and adrenocortical responses to environmental changes in leopard cats (Felis bengalensis). Zoo Biol. 1993;12:321–31.
Caroprese M, Annicchiarico G, Schena L, Muscio A, Migliore R, Sevi A. Influence of space allowance and housing conditions on the welfare, immune response and production performance of dairy ewes. J Dairy Res. 2009;76:66–73.
Carr JA. Stress and reproduction in amphibians. In: David ON, Kristin HL, editors. Hormones and reproduction of vertebrates. London: Academic Press; 2011. p. 99–116.
Carrasco L, Colell M, Calvo M, Abelló MT, Velasco M, Posada S. Benefits of training/playing therapy in a group of captive lowland gorillas (Gorilla gorilla gorilla). Anim Welf. 2009;18:9–19.
Carter S. Neuroendocrinology of sexual behavior in the female. In: Becker J, Breedlove S, Crews D, editors. Behavioral endocrinology. Cambridge: MIT Press; 1992. p. 71–96.
Carver C, Scheier M, Segerstrom S. Optimism. Clin Psychol Rev. 2010;30:879–89.
Casal N, Manteca X, Escribano D, Cerón J, Fàbrega E. Effect of environmental enrichment and herbal compound supplementation on physiological stress indicators (chromogranin A, cortisol and tumour necrosis factor-α) in growing pigs. Animal. 2017;11:1228–36.
Case BC, Lewbart GA, Doerr PD. The physiological and behavioural impacts of and preference for an enriched environment in the eastern box turtle (Terrapene carolina carolina). Appl Anim Behav Sci. 2005;92:353–65.
Casey TM, Plaut K. The role of glucocorticoids in secretory activation and milk secretion, a historical perspective. J Mammary Gland Biol Neoplasia. 2007;12:293–304.
Caslini C, Comin A, Peric T, Prandi A, Pedrotti L, Mattiello S. Use of hair cortisol analysis for comparing population status in wild red deer (Cervus elaphus) living in areas with different characteristics. Eur J Wildl Res. 2016;62:713–23.
Castagné R, Garès V, Karimi M, Chadeau-Hyam M, Vineis P, Delpierre C, Kelly-Irving M. Allostatic load and subsequent all-cause mortality: which biological markers drive the relationship? Findings from a UK birth cohort. Eur J Epidemiol. 2018;33:441–58.
Cavanaugh J, Carp SB, Rock CM, French JA. Oxytocin modulates behavioral and physiological responses to a stressor in marmoset monkeys. Psychoneuroendocrinology. 2016;66:22–30.
Cavigelli SA, Caruso MJ. Sex, social status and physiological stress in primates: the importance of social and glucocorticoid dynamics. Philos Trans R Soc Lond B Biol Sci. 2015;370:20140103.
Chaise LL, Paterson W, Laske TG, Gallon SL, McCafferty DJ, Théry M, Ancel A, Gilbert C. Implantation of subcutaneous heart rate data loggers in southern elephant seals (Mirounga leonina). Polar Biol. 2017;40:2307–12.
Chambers MA. Review of the diagnosis and study of tuberculosis in non-bovine wildlife species using immunological methods. Transbound Emerg Dis. 2009;56:215–27.
Chen X, Niu C, Pu L. Effects of stocking density on growth and non-specific immune responses in juvenile soft-shelled turtle, Pelodiscus sinensis. Aquacult Res. 2007;38:1380–6.
Christensen DS, Flensborg-Madsen T, Garde E, Hansen ÅM, Pedersen JM, Mortensen EL. Early life predictors of midlife allostatic load: a prospective cohort study. PLoS One. 2018a;13:e0202395.
Christensen DS, Flensborg-Madsen T, Garde E, Hansen ÅM, Pedersen JM, Mortensen EL. Parental socioeconomic position and midlife allostatic load: a study of potential mediators. BMC Public Health. 2018b;18:1029.
Chrousos GP, Torpy DJ, Gold PW. Interactions between the hypothalamic-pituitary-adrenal axis and the female reproductive system: clinical implications. Ann Intern Med. 1998;129:229–40.
Church JS, Cook NJ, Schaefer AL. Recent applications of infrared thermography for animal welfare and veterinary research: everything from chicks to elephants. Proc Inframation. 2009;10:215–24.
Clark FE, Fitzpatrick M, Hartley A, King AJ, Lee T, Routh A, Walker SL, George K. Relationship between behavior, adrenal activity, and environment in zoo-housed western lowland gorillas (Gorilla gorilla gorilla). Zoo Biol. 2011;31:306–21.
Clauss M, Wilkins T, Hartley A, Hatt JM. Diet composition, food intake, body condition, and fecal consistency in captive tapirs (Tapirus spp.) in UK collections. Zoo Biol. 2009;28:279–91.
Clegg I. Cognitive bias in zoo animals: an optimistic outlook for welfare assessment. Animals. 2018;8:104.
Clegg IL, Rödel HG, Delfour F. Bottlenose dolphins engaging in more social affiliative behaviour judge ambiguous cues more optimistically. Behav Brain Res. 2017;322:115–22.
Cockrem JF. Individual variation in glucocorticoid stress responses in animals. Gen Comp Endocrinol. 2013;181:45–58.
Codispoti M, Gerra G, Montebarocci O, Zaimovic A, Augusta Raggi M, Baldaro B. Emotional perception and neuroendocrine changes. Psychophysiology. 2003;40:863–8.
Cohen S, Wills TA. Stress, social support, and the buffering hypothesis. Psychol Bull. 1985;98:310–57.
Cohen S, Doyle WJ, Turner RB, Alper CM, Skoner DP. Emotional style and susceptibility to the common cold. Psychosom Med. 2003;65:652–7.
Cohn D, Zangerle R, Fischer-Colbrie R, Chu L, Elting J, Hamilton J, Winkler H. Similarity of secretory protein I from parathyroid gland to chromogranin A from adrenal medulla. Proc Natl Acad Sci U S A. 1982;79:6056–9.
Colborn D, Thompson D, Roth T, Capehart J, White K. Responses of cortisol and prolactin to sexual excitement and stress in stallions and geldings. J Anim Sci. 1991;69:2556–62.
Comizzoli P, Holt WV. Breakthroughs and new horizons in reproductive biology of rare and endangered animal species. Biol Reprod. 2019:ioz031.
Conlon JM. Granin-derived peptides as diagnostic and prognostic markers for endocrine tumors. Regul Pept. 2010;165:5–11.
Contreras-Aguilar MD, Tecles F, Martínez-Subiela S, Escribano D, Bernal LJ, Cerón JJ. Detection and measurement of alpha-amylase in canine saliva and changes after an experimentally induced sympathetic activation. BMC Vet Res. 2017;13:266.
Contreras-Aguilar MD, Escribano D, Martínez-Subiela S, Martínez-Miró S, Cerón JJ, Tecles F. Changes in alpha-amylase activity, concentration and isoforms in pigs after an experimental acute stress model: an exploratory study. BMC Vet Res. 2018;14:256.
Cook C, Mellor D, Harris P, Ingram J, Matthews L. Hands-on and hands-off measurement of stress. In: Moberg G, Mench J, editors. The biology of animal stress: basic principles and implications for animal welfare. Wallingford: CABI Publishing; 2000. p. 123–46.
Cooke RG, Benhaj KM. Effects of ACTH and cortisol on luteolysis in the ewe. Anim Reprod Sci. 1989;20:201–11.
Cooke SJ, Sack L, Franklin CE, Farrell AP, Beardall J, Wikelski M, Chown SL. What is conservation physiology? Perspectives on an increasingly integrated and essential science. Conserv Physiol. 2013;1:cot001.
Cooper CL, Baglioni AJ Jr. A structural model approach toward the development of a theory of the link between stress and mental health. Br J Med Psychol. 1988;61:87–102.
Cordoni G, Palagi E, Tarli SB. Reconciliation and consolation in captive western gorillas. Int J Primatol. 2006;27:1365–82.
Corti C, Biaggini M, Berti R. Analysis of escape behaviour and ectoparasite load in Podarcis sicula (Lacertidate) populations in different agricultural habitats. Amphibia-Reptillia. 2009;30:453–61.
Cottontail VM, Wellinghausen N, Kalko EKV. Habitat fragmentation and haemoparasites in the common fruit bat, Artibeus jamaicensi (Phyllostomidae) in a tropical lowland forest in Panamá. Parasitology. 2009;136:1133–45.
Creel S. Social dominance and stress hormones. Trends Ecol Evol. 2001;16:491–7.
Creel S, Fox JE, Hardy A, Sands J, Garrott B, Peterson RO. Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conserv Biol. 2002;16:809–14.
Crimmins EM, Johnston M, Hayward M, Seeman TE. Age differences in allostatic load: an index of physiological dysregulation. Exp Gerontol. 2003;38:731–4.
Crimmins EM, Kim JK, Seeman TE. Poverty and biological risk: the earlier “aging” of the poor. J Gerontol A Biol Sci Med Sci. 2009;64A:286–92.
Cross N, Pines MK, Rogers LJ. Saliva sampling to assess cortisol levels in unrestrained common marmosets and the effect of behavioral stress. Am J Primatol. 2004;62:107–14.
Cummins DD. Dominance, status, and social hierarchies. In: Buss DM, editor. The handbook of evolutionary psychology. Hoboken: Wiley; 2005. p. 676–97.
Cummins DD. Status and dominance hierarchies. In: Weekes-Shackelford V, Shackelford TK, Weekes-Shackelford VA, editors. Encyclopedia of evolutionary psychological science. Cham: Springer; 2016. p. 1–10.
D’amico MA, Ghinassi B, Izzicupo P, Manzoli L, Di Baldassarre A. Biological function and clinical relevance of chromogranin A and derived peptides. Endocr Connect. 2014;3:R45–54.
Dai F, Cogi NH, Heinzl EUL, Dalla Costa E, Canali E, Minero M. Validation of a fear test in sport horses using infrared thermography. J Vet Behav. 2015;10:128–36.
Danese A, McEwen BS. Adverse childhood experiences, allostasis, allostatic load, an age-related disease. Physiol Behav. 2012;106:29–39.
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:cou023.
Davis N, Schaffner CM, Smith TE. Evidence that zoo visitors influence HPA activity in spider monkeys (Ateles geoffroyii rufiventris). Appl Anim Behav Sci. 2005;90:131–41.
Davis A, Maney D, Maerz J. The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol. 2008;22:760–72.
de Jong I, Sgoifo A, Lambooij E, Korte SM, Blokhuis HJ, Koolhaas JM. Effects of social stress on heart rate and heart rate variability in growing pigs. Can J Anim Sci. 2000;80:273–80.
Dehnhard M. Characterisation of the sympathetic nervous system of Asian (Elephas maximus) and African (Loxodonta africana) elephants based on urinary catecholamine analyses. Gen Comp Endocrinol. 2007;151:274–84.
Deinzer R, Schuller N. Dynamics of stress-related decrease of salivary immunoglobulin A (sIgA): relationship to symptoms of the common cold and studying behavior. Behav Med. 1998;23:161–9.
Delpierre C, Barbosa-Solis C, Torrisani J, Darnaudery M, Bartley M, Blane D, Kelly-Irving M, Tomasdottir MO, Robertson T, Gustafsson PE. Origins of health inequalities: the case for allostatic load. Longit Life Course Stud. 2016;7:79–103.
Dembiec DP, Snider RJ, Zanella AJ. The effects of transport stress on tiger physiology and behavior. Zoo Biol. 2004;23:335–46.
Dettling AC, Feldon J, Pryce CR. Repeated parental deprivation in the infant common marmoset (Callithrix jacchus, primates) and analysis of its effects on early development. Biol Psychiatry. 2002;52:1037–46.
Dettmer AM, Wooddell LJ, Rosenberg KL, Kaburu SSK, Novak MA, Meyer JS, Suomi SJ. Associations between early life experience, chronic HPA axis activity, and adult social rank in rhesus macaques. Soc Neurosci. 2017;12:92–101.
Di Comite G, Marinosci A, Di Matteo P, Manfredi A, Rovere-Querini P, Baldissera E, Aiello P, Corti A, Sabbadini MG. Neuroendocrine modulation induced by selective blockade of TNF-α in rheumatoid arthritis. Ann N Y Acad Sci. 2006;1069:428–37.
Dillon KM, Minchoff B, Baker KH. Positive emotional states and enhancement of the immune system. Int J Psychiatry Med. 1986;15:13–8.
Ditmer MA, Vincent JB, Werden LK, Tanner JC, Laske TG, Iaizzo PA, Garshelis DL, Fieberg JR. Bears show a physiological but limited behavioral response to unmanned aerial vehicles. Curr Biol. 2015;25:2278–83.
Ditmer MA, Werden LK, Tanner JC, Vincent JB, Callahan P, Iaizzo PA, Laske TG, Garshelis DL. Bears habituate to the repeated exposure of a novel stimulus, unmanned aircraft systems. Conserv Physiol. 2019;7:coy067-coy.
Dobson H, Smith R. Stress and reproduction in farm animals. J Reprod Fertil. 1995;49:451–61.
Dobson H, Smith RF. What is stress, and how does it affect reproduction? Anim Reprod Sci. 2000;60–61:743–52.
Dobson H, Ghuman S, Prabhakar S, Smith R. A conceptual model of the influence of stress on female reproduction. Reproduction. 2003;125:151–63.
Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK, Lanctôt KL. A meta-analysis of cytokines in major depression. Biol Psychiatry. 2010;67:446–57.
Drake K, Nussear K, Esque T, Barber A, Vittum K, Medica P, Tracy C, Hunter K. Does translocation influence physiological stress in the desert tortoise? Anim Conserv. 2012;15:560–70.
Duong HT, Piotrowska-Tomala KK, Acosta TJ, Bah MM, Sinderewicz E, Majewska M, Jankowska K, Okuda K, Skarzynski DJ. Effects of cortisol on pregnancy rate and corpus luteum function in heifers: an in vivo study. J Reprod Dev. 2011:1112060422.
Duong MT, Bingham BA, Aldana PC, Chung ST, Sumner AE. Variation in the calculation of allostatic load scores: 21 examples from NHANES. J Racial Ethn Health Disparities. 2017;4:455–61.
Duque M, Modlin IM, Gupta A, Saif MW. Biomarkers in neuroendocrine tumors. JOP. 2013;14:372–6.
Duru OK, Harawa NT, Kermah D, Norris KC. Allostatic load burden and racial disparities in mortality. J Natl Med Assoc. 2012;104:89–95.
Edes AN. Dehydroepiandrosterone-sulfate (DHEA-S), sex, and age in zoo-housed western lowland gorillas (Gorilla gorilla gorilla). Primates. 2017;58:385–92.
Edes AN, Crews DE. Allostatic load and biological anthropology. Am J Phys Anthropol. 2017;162:44–70.
Edes AN, Wolfe BA, Crews DE. Assessing stress in zoo-housed western lowland gorillas (Gorilla gorilla gorilla) using allostatic load. Int J Primatol. 2016a;37:241–59.
Edes AN, Wolfe BA, Crews DE. Rearing history and allostatic load in adult western lowland gorillas (Gorilla gorilla gorilla) in human care. Zoo Biol. 2016b;35:167–73.
Edes AN, Wolfe BA, Crews DE. Evaluating allostatic load: a new approach to measuring long-term stress in wildlife. J Zoo Wildl Med. 2018a;49:272–82.
Edes AN, Wolfe BA, Crews DE. The first multi-zoo application of an allostatic load index to western lowland gorillas (Gorilla gorilla gorilla). Gen Comp Endocrinol. 2018b;266:135–49.
Edwards KL, Walker SL, Bodenham RF, Ritchie H, Shultz S. Associations between social behaviour and adrenal activity in female Barbary macaques: consequences of study design. Gen Comp Endocrinol. 2013;186:72–9.
Edwards KL, Bansiddhi P, Paris S, Galloway M, Brown JL. The development of an immunoassay to measure immunoglobulin A in Asian elephant feces, saliva, urine and serum as a potential biomarker of well-being. Conserv Physiol. 2019;7:coy077.
Egorov AI, Converse R, Griffin SM, Styles J, Klein E, Sams E, Hudgens E, Wade TJ. Environmental risk factors for Toxoplasma gondii infections and the impact of latent infections on allostatic load in residents of central North Carolina. BMC Infect Dis. 2018;18:421.
Einarsson S, Madej A, Tsuma V. The influence of stress on early pregnancy in the pig. Anim Reprod Sci. 1996;42:165–72.
Elenkov IJ, Chrousos GP. Stress hormones, Th1/Th2 patterns, pro/anti-inflammatory cytokines and susceptibility to disease. Trends Endocrinol Metab. 1999;10:359–68.
Ellenberg U, Setiawan AN, Cree A, Houston DM, Seddon PJ. Elevated hormonal stress response and reduced reproductive output in yellow-eyed penguins exposed to unregulated tourism. Gen Comp Endocrinol. 2007;152:54–63.
Eriksson E, Royo F, Lyberg K, Carlsson HE, Hau J. Effect of metabolic cage housing on immunoglobulin A and corticosterone excretion in faeces and urine of young male rats. Exp Physiol. 2004;89:427–33.
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;7:640–7.
Escribano D, Tvarijonaviciute A, Tecles F, Cerón JJ. Serum paraoxonase type-1 activity in pigs: assay validation and evolution after an induced experimental inflammation. Vet Immunol Immunopathol. 2015;163:210–5.
Estensen ME, Hognestad A, Syversen U, Squire I, Ng L, Kjekshus J, Dickstein K, Omland T. Prognostic value of plasma chromogranin A levels in patients with complicated myocardial infarction. Am Heart J. 2006;152:927.e1.
Evain D, Morera AM, Saez JM. Glucocorticoid receptors in interstitial cells of the rat testis. J Steroid Biochem. 1976;7:1135–9.
Everly GS, Lating JM. The anatomy and physiology of the human stress response. A clinical guide to the treatment of the human stress response. 3rd ed. New York: Springer; 2013. p. 17–51.
Eysenck MW, Mogg K, May J, Richards A, Mathews A. Bias in interpretation of ambiguous sentences related to threat in anxiety. J Abnorm Psychol. 1991;100:144.
Fanson KV, Wielebnowski NC. Effect of housing and husbandry practices on adrenocortical activity in captive Canada lynx (Lynx canadensis). Anim Welf. 2013;22:159–65.
Fanson KV, Lynch M, Vogelnest L, Miller G, Keeley T. Response to long-distance relocation in Asian elephants (Elephas maximus): monitoring adrenocortical activity via serum, urine, and feces. Eur J Wildl Res. 2013;59:655–64.
Fanson KV, Keeley T, Fanson BG. Cyclic changes in cortisol across the estrous cycle in parous and nulliparous Asian elephants. Endocr Connect. 2014;3:57–66.
Farm Animal Welfare Council. Press release. 1979.
Fazio F, Ferrantelli V, Cicero A, Casella S, Piccione G. Utility of acute phase proteins as biomarkers of transport stress in ewes and beef cattle. Ital J Food Saf. 2015;4:4210.
Fenster L, Katz DF, Wyrobek AJ, Pieper C, Rempel DM, Oman D, Swan SH. Effects of psychological stress on human semen quality. J Androl. 1997;18:194–202.
Ferin M. Stress and the reproductive cycle. J Clin Endocrinol Metab. 1999;84:1768–74.
Fernandez CA, Loucks EB, Arheart KL, Hickson DA, Kohn R, Duka SL, Gjelsvik A. Evaluating the effects of coping style on allostatic load, by sex: the Jackson heart study, 2000–2004. Prev Chronic Dis. 2015;12:E165.
Filaire E, Ferreira JP, Oliveira M, Massart A. Diurnal patterns of salivary alpha-amylase and cortisol secretion in female adolescent tennis players after 16 weeks of training. Psychoneuroendocrinology. 2013;38:1122–32.
Filiberto AC, Maccani MA, Koestler DC, Wilhelm-Benartzi C, Avissar-Whiting M, Banister CE, Gagne LA, Marsit CJ. Birthweight is associated with DNA promoter methylation of the glucocorticoid receptor in human placenta. Epigenetics. 2011;6:566–72.
Floreani A, Titta M, Plebani M, Faggian D, Chiaramonte M, Naccarato R. Sex hormone changes in post-menopausal women with primary biliary cirrhosis (PBC) and with cryptogenic chronic liver disease. Clin Exp Obstet Gynecol. 1991;18:229–34.
Flory JD, Manuck SB, Matthews KA, Muldoon MF. Serotonergic function in the central nervous system is associated with daily ratings of positive mood. Psychiatry Res. 2004;129:11–9.
Fontúrbel FE, Candia AB, Salzar DA, Malebrán J, González-Browne C, Botto-Mahan C. How forest marsupials are affected by habitat degradation and fragmentation? A meta-analysis. Naturwissenchaften. 2014;101:599–602.
Fortunato CK, Dribin AE, Granger DA, Buss KA. Salivary alpha-amylase and cortisol in toddlers: differential relations to affective behavior. Dev Psychobiol. 2008;50:807–18.
Fox NA. Psychophysiological correlates of emotional reactivity during the first year of life. Dev Psychol. 1989;25:364.
Franceschini MD, Rubenstein DI, Low B, Romero LM. Fecal glucocorticoid metabolite analysis as an indicator of stress during translocation and acclimation in an endangered large mammal, the Grevy’s zebra. Anim Conserv. 2008;11:263–9.
Frank D, Gauthier A, Bergeron R. Placebo-controlled double-blind clomipramine trial for the treatment of anxiety or fear in beagles during ground transport. Can Vet J. 2006;47:1102.
Fraser D. Assessing animal welfare: different philosophies, different scientific approaches. Zoo Biol. 2009;28:507–18.
Frederick C, Fernandes D. Behavioral changes in pottos (Perodicticus potto): effects of naturalizing an exhibit. Int J Primatol. 1996;17:389–99.
Frederick C, Hunt K, Kyes R, Collins D, Durrant B, Ha J, Wasser SK. Social influences on the estrous cycle of the captive sun bear (Helarctos malayanus). Zoo Biol. 2013;32:581–91.
Freeman NE, Newman AE. Quantifying corticosterone in feathers: validations for an emerging technique. Conserv Physiol. 2018;6:coy051.
Freeman EW, Weiss E, Brown JL. Examination of the interrelationships of behavior, dominance status, and ovarian activity in captive Asian and African elephants. Zoo Biol. 2004;23:431–48.
Freeman EW, Guagnano G, Olson D, Keele M, Brown JL. Social factors influence ovarian acyclicity in captive African elephants (Loxodonta africana). Zoo Biol. 2009;28:1–15.
Frei R, Haile SR, Mutsch M, Rohrmann S. Relationship of serum vitamin D concentrations and allostatic load as a measure of cumulative biological risk among the US population: a cross-sectional study. PLoS One. 2015;10:1–17.
French SS, Fokidis HB, Moore MC. Variation in stress and innate immunity in the tree lizard (Urosaurus ornatus) across an urban–rural gradient. J Comp Physiol B. 2008;178:997–1005.
Friedman BH, Thayer JF. Anxiety and autonomic flexibility: a cardiovascular approach. Biol Psychol. 1998;47:243–63.
Fuentes M, Tecles F, Gutiérrez A, Otal J, Martínez-Subiela S, Cerón JJ. Validation of an automated method for salivary alpha-amylase measurements in pigs (Sus scrofa domesticus) and its application as a stress biomarker. J Vet Diagn Invest. 2011;23:282–7.
Fuentes-Rubio M, Fuentes F, Otal J, Quiles A, Tecles F, Cerón JJ, Hevia ML. Measurements of salivary alpha-amylase in horse: comparison of 2 different assays. J Vet Behav. 2015;10:122–7.
Fuller G, Allard S. Preliminary data showing potential for salivary C-reactive protein as an indicator of welfare in western lowland gorillas (Gorilla gorilla gorilla). J Vet Behav. 2018;28:58–62.
Fuller G, Kuhar CW, Dennis PM, Lukas KE. A survey of husbandry practices for lorisid primates in North American zoos and related facilities. Zoo Biol. 2013;32:88–100.
Fuller G, Lukas KE, Kuhar C, Dennis PM. A retrospective review of mortality in lorises and pottos in North American zoos, 1980-2010. Endanger Species Res. 2014;23:205–17.
Fürtbauer I, Heistermann M, Schülke O, Ostner J. Low female stress hormone levels are predicted by same- or opposite-sex sociality depending on season in wild Assamese macaques. Psychoneuroendocrinology. 2014;48:19–28.
Fuzzen MLM, Bernier NJ, Glen Van Der K. Stress and reproduction. In: David ON, Kristin HL, editors. Hormones and reproduction of vertebrates. London: Academic Press; 2011. p. 103–17.
Gácsi M, Maros K, Sernkvist S, Faragó T, Miklosi A. Human analogue safe haven effect of the owner: behavioural and heart rate response to stressful social stimuli in dogs. PLoS One. 2013;8:e58475.
Gallo LC, Fortmann AL, Mattei J. Allostatic load and the assessment of cumulative biological risk in biobehavioral medicine: challenges and opportunities. Psychosom Med. 2014;76:478–80.
Ganswindt A, Brown JL, Freeman EW, Kouba AJ, Penfold LM, Santymire RM, Vick MM, Wielebnowski N, Willis EL, Milnes MR. International Society for Wildlife Endocrinology: the future of endocrine measures for reproductive science, animal welfare and conservation biology. Biol Lett. 2012;8:695–7.
Garner MM, Helmick K, Ochsenreiter J, Richman LK, latimer E, Wise AG, Maes RK, Kiupel M, Nordhausen RW, Zong JC, Hayward GS. Clinico-pathologic features of fatal disease attributed to new variances of endotheliotropic herpesvirus in two Asian elephants (Elephas maximus). Vet Pathol. 2009;46:97–104.
Gasparotto OC, Lopes DM, Carobrez SG. Pair housing affects anxiety-like behaviors induced by a social but not by a physiological stressor in male Swiss mice. Physiol Behav. 2005;85:603–12.
Gay JL, Salinas JJ, Buchner DM, Mirza S, Kohl Iii HW, Fisher-Hoch SP, McCormick JB. Meeting physical activity guidelines is associated with lower allostatic load and inflammation in Mexican Americans. J Immigr Minor Health. 2015;17:574–81.
Gimeno D, Brunner EJ, Lowe GD, Rumley A, Marmot MG, Ferrie JE. Adult socioeconomic position, C-reactive protein and interleukin-6 in the Whitehall II prospective study. Eur J Epidemiol. 2007a;22:675–83.
Gimeno D, Ferrie J, Elovainio M, Pulkki-Raback L, Keltikangas-Jarvinen L, Eklund C, Hurme M, Lehtimäki T, Marniemi J, Viikari J. When do social inequalities in C-reactive protein start? A life course perspective from conception to adulthood in the Cardiovascular Risk in Young Finns Study. Int J Epidemiol. 2007b;37:290–8.
Ginther OJ. Reproductive biology of the mare: basic and applied aspects. Cross Plains: Equiservices; 1992.
Giovinazzo F, Schimmack S, Svejda B, Alaimo D, Pfragner R, Modlin I, Kidd M. Chromogranin A and its fragments as regulators of small intestinal neuroendocrine neoplasm proliferation. PLoS One. 2013;8:e81111.
Gleeson M, McDonald WA, Cripps AW, Pyne DB, Clancy RL, Fricker PA, Wlodarczyk JH. Exercise, stress and mucosal immunity in elite swimmers. Adv Exp Med Biol. 1995;371A:571–4.
Glei DA, Goldman N, Chuang Y-L, Weinstein M. Do chronic stressors lead to physiological dysregulation? Testing the theory of allostatic load. Psychosom Med. 2007;69:769–76.
Glei DA, Goldman N, Rodríguez G, Weinstein M. Beyond self-reports: changes in biomarkers as predictors of mortality. Popul Dev Rev. 2014;40:331–60.
Gobush KS, Mutayoba BM, Wasser SK. Long-term impacts of poaching on relatedness, stress physiology, and reproductive output of adult female African elephants. Conserv Biol. 2008;22:1590–9.
Goldman N, Glei DA, Seplaki C, Liu IW, Weinstein M. Perceived stress and physiological dysregulation in older adults. Stress. 2005;8:95–105.
Gopee NV, Adesiyun AA, Caesar K. Retrospective and longitudinal study of salmonellosis in captive wildlife in Trinidad. J Wildl Dis. 2000;36:284–93.
Gourkow N, LaVoy A, Dean GA, Phillips CJC. Associations of behaviour with secretory immunoglobulin A and cortisol in domestic cats during their first week in an animal shelter. Appl Anim Behav Sci. 2014;150:55–64.
Goymann W, Wingfield JC. Allostatic load, social status and stress hormones: the costs of social status matter. Anim Behav. 2004;67:591–602.
Granger DA, Kivlighan KT, Blair C, El-Sheikh M, Mize J, Lisonbee JA, Buckhalt JA, Stroud LR, Handwerger K, Schwartz EB. Integrating the measurement of salivary α-amylase into studies of child health, development, and social relationships. J Soc Pers Relat. 2006;23:267–90.
Greco BJ, Meehan CL, Hogan JN, Leighty KA, Mellen J, Mason GJ, Mench JA. The days and nights of zoo elephants: using epidemiology to better understand stereotypic behavior of African elephants (Loxodonta africana) and Asian elephants (Elephas maximus) in North American zoos. PLoS One. 2016;11:e0144276.
Green ML, Green RG, Santoro W. Daily relaxation modifies serum and salivary immunoglobulins and psychophysiologic symptom severity. Appl Psychophysiol Biofeedback. 1988;13:187–99.
Grobler DG, Raath JP, Braack LEO, Keet DF, Gerdes GH, Barnard BJH, Kriek NPJ, Jardine J, Swanepoel R. An outbreak of encephalomyocarditis-virus infection in free-ranging African elephants in the Kruger National Park. Onderstepoort J Vet Res. 1995;62:97–108.
Groombridge JJ, Massey JG, Bruch JC, Malcolm TR, Brosius CN, Okada MM, Sparklin B. Evaluating stress in a Hawaiian honeycreeper, Paroreomyza montana, following translocation. J Field Ornithol. 2004;75:183–7.
Grossi G, Perski A, Evengård B, Blomkvist V, Orth-Gomér K. Physiological correlates of burnout among women. J Psychosom Res. 2003;55:309–16.
Gruenewald TL, Seeman TE, Ryff CD, Karlamangla AS, Singer BH. Combinations of biomarkers predictive of later life mortality. Proc Natl Acad Sci U S A. 2006;103:14158–63.
Guhad FA, Hau J. Salivary IgA as a marker of social stress in rats. Neurosci Lett. 1996;216:137–40.
Guilliams TG, Edwards L. Chronic stress and the HPA axis. Standard. 2010;9:1–12.
Gundlach NH, Schmicke M, Ludes-Wehrmeister E, Ulrich SA, Araujo MG, Siebert U. New approach to stress research in phocids—potential of dehydroepiandrosterone and cortisol/dehydroepiandrosterone ratio as markers for stress in harbor seals (Phoca vitulina) and gray seals (Halichoerus grypus). J Zoo Wildl Med. 2018;49:556–63.
Haeussler S, Claus R. Expression of the glucocorticoid receptor and 11β-hydroxysteroid dehydrogenase 2 in pig testes cells along fetal development. Reprod Fertil Dev. 2007;19:664–9.
Hagen K, Langbein J, Schmied C, Lexer D, Waiblinger S. Heart rate variability in dairy cows—influences of breed and milking system. Physiol Behav. 2005;85:195–204.
Hainsworth R. The control and physiological importance of heart rate. In: Malik M, Camm AJ, editors. Heart rate variability. New York: Futura Publishing; 1995. p. 3–19.
Hämäläinen A, Heistermann M, Kraus C. The stress of growing old: sex- and season-specific effects of age on allostatic load in wild grey mouse lemurs. Oecologia. 2015;178:1063–75.
Hänichen T, Reid HW, Wiesner H, Hermanns W. Malignant catarrhal fever in zoo ruminants. Tierarztl Prax Ausg G Grosstiere Nutztiere. 1998;26:294–300.
Hänsel A, Hong S, Camara RJ, Von Kaenel R. Inflammation as a psychophysiological biomarker in chronic psychosocial stress. Neurosci Biobehav Rev. 2010;35:115–21.
Harding EJ, Paul ES, Mendl M. Animal behaviour: cognitive bias and affective state. Nature. 2004;427:312.
Hardy MP, Gao HB, Dong Q, Ge RS, Wang Q, Chai WR, Feng X, Sottas C. Stress hormone and male reproductive function. Cell Tissue Res. 2005;322:147–53.
Harper JY, Schulte BA. Social interactions in captive female Florida manatees. Zoo Biol. 2005;24:135–44.
Hau J, Andersson E, Carlsson HE. Development and validation of a sensitive ELISA for quantification of secretory IgA in rat saliva and faeces. Lab Anim. 2001;35:301–6.
Hay M, Mormède P. Urinary excretion of catecholamines, cortisol and their metabolites in Meishan and large white sows: validation as a non-invasive and integrative assessment of adrenocortical and sympathoadrenal axis activity. Vet Res. 1998;29:119–28.
Hayward LS, Bowles AE, Ha JC, Wasser SK. Impacts of acute and long-term vehicle exposure on physiology and reproductive success of the northern spotted owl. Ecosphere. 2011;2:1–20.
Haywood S, Perrins CM. Is clutch size in birds affected by environmental conditions during growth? Proc R Soc Lond B. 1992;249:195–7.
Heatley JJ, Oliver JW, Hosgood G, Columbini S, Tully TN. Serum corticosterone concentrations in response to restraint, anesthesia, and skin testing in Hispaniolan Amazon parrots (Amazona ventralis). J Avian Med Surg. 2000;14:172–6.
Heimbürge S, Kanitz E, Otten W. The use of hair cortisol for the assessment of stress in animals. Gen Comp Endocrinol. 2018;270:10–7.
Heistermann M, Ademmer C, Kaumanns W. Ovarian cycle and effect of social changes on adrenal and ovarian function in Pygathrix nemaeus. Int J Primatol. 2004;25:689–708.
Hemingway H, Shipley M, Mullen MJ, Kumari M, Brunner E, Taylor M, Donald AE, Deanfield JE, Marmot M. Social and psychosocial influences on inflammatory markers and vascular function in civil servants (the Whitehall II study). Am J Cardiol. 2003;92:984–7.
Henkel S, Heistermann M, Fischer J. Infants as costly social tools in male Barbary macaque networks. Anim Behav. 2010;79:1199–204.
Herrelko ES, Vick S-J, Buchanan-Smith HM. Cognitive research in zoo-housed chimpanzees: influence of personality and impact on welfare. Am J Primatol. 2012;74:828–40.
Herrera-Luna C, Budik S, Aurich C. Gene expression of ACTH, glucocorticoid receptors, 11βHSD enzymes, LH-, FSH-, GH receptors and aromatase in equine epididymal and testicular tissue. Reprod Domest Anim. 2012;47:928–35.
Herring G, Gawlik DE. Differential physiological responses to prey availability by the great egret and white Ibis. J Wildl Manage. 2013;77:58–67.
Herrington DM, Gordon GB, Achuff SC, Trejo JF, Weisman HF, Kwiterovich PO, Pearson TA. Plasma dehydroepiandrosterone and dehydroepiandrosterone sulfate in patients undergoing diagnostic coronary angiography. J Am Coll Cardiol. 1990;16:862–70.
Hickey M-C, Drennan M, Earley B. The effect of abrupt weaning of suckler calves on the plasma concentrations of cortisol, catecholamines, leukocytes, acute-phase proteins and in vitro interferon-gamma production. J Anim Sci. 2003;81:2847–55.
Higham JP, Vitale AB, Rivera AM, Ayala JE, Maestripieri D. Measuring salivary analytes from free-ranging monkeys. Physiol Behav. 2010;101:601–7.
Higuchi T, Honda K, Negoro H. Influence of oestrogen and noradrenergic afferent neurones on the response of LH and oxytocin to immobilization stress. J Endocrinol. 1986;110:245–50.
Hillier SG, Tetsuka M. An anti-inflammatory role for glucocorticoids in the ovaries? J Reprod Immunol. 1998;39:21–7.
Hilsberg S. Clinical application of infrared-thermography in inflammation diagnosis in mega-herbivores. In: Proceedings of European Association of Zoo and Wildlife Veterinarians 4th scientific meeting; 2002. p. 315–20.
Hing S, Northover AS, Narayan EJ, Wayne AF, Jones KL, Keatley S, Thompson RA, Godfrey SS. Evaluating stress physiology and parasite infection parameters in the translocation of critically endangered woylies (Bettongia penicillata). Ecohealth. 2017;14:128–38.
Hjortskov N, Rissén D, Blangsted AK, Fallentin N, Lundberg U, Søgaard K. The effect of mental stress on heart rate variability and blood pressure during computer work. Eur J Appl Physiol. 2004;92:84–9.
Hofer H, East M. Stress and immunosuppression as factors in the decline and extinction of wildlife populations: concepts, evidence and challenges. In: Aguirre A, Ostfeld R, Daszak P, editors. New directions in conservation medicine: applied cases of ecological health. New York: Oxford University Press; 2012. p. 82–107.
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;71:223–32.
Holt-Lunstad J, Smith TB, Layton JB. Social relationships and mortality risk: a meta-analytic review. PLoS Med. 2010;7:1–20.
Honess PE, Johnson PJ, Wolfensohn SE. A study of behavioural responses of non-human primates to air transport and re-housing. Lab Anim. 2004;38:119–32.
Hopper LM. Cognitive research in zoos. Behav Sci. 2017;16:100–10.
Hopper LM, Shender MA, Ross SR. Behavioral research as physical enrichment for captive chimpanzees. Zoo Biol. 2016;35:293–7.
Horan JM, Widom CS. From childhood maltreatment to allostatic load in adulthood: the role of social support. Child Maltreat. 2015;20:229–39.
Hostinar CE, Sullivan RM, Gunnar MR. Psychobiological mechanisms underlying the social buffering of the HPA axis: a review of animal models and human studies across development. Psychol Bull. 2014;140:256–82.
House JS, Landis KR, Umberson D. Social relationships and health. Science. 1988;241:540–5.
Hovland AL, Rød AMS, Eriksen MS, Palme R, Nordgreen J, Mason GJ. Faecal cortisol metabolites as an indicator of adrenocortical activity in farmed silver foxes (Vulpes vulpes). Appl Anim Behav Sci. 2017;197:75–80.
Howell CP, Cheyne SM. Complexities of using wild versus captive activity budget comparisons for assessing captive primate welfare. J Appl Anim Welf Sci. 2019;22:78–96.
Howell-Stephens JA, Brown JS, Bernier D, Mulkerin D, Santymire RM. Characterizing adrenocortical activity in zoo-housed southern three-banded armadillos (Tolypeutes matacus). Gen Comp Endocrinol. 2012;178:64–74.
Howren MB, Lamkin DM, Suls J. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom Med. 2009;71:171–86.
Huang S, Li L, Wu J, Li C, Bai J, Sun Y, Wang G. Seasonal variations in immunoreactive cortisol and fecal immunoglobulin levels in Sichuan golden monkey (Rhinopithecus roxellana). Turk J Zool. 2014;38:642–50.
Hucklebridge F, Clow A, Evans P. The relationship between salivary secretory immunoglobulin A and cortisol: neuroendocrine response to awakening and the diurnal cycle. Int J Psychophysiol. 1998;31:69–76.
Hughes P. Factors affecting the natural attainment of puberty in the gilt. In: Cole D, Foxcroft G, editors. Control of pig reproduction. London: Butterworths; 1982. p. 117–38.
Hunt KE, Lysiak NS, Moore MJ, Rolland RM. Longitudinal progesterone profiles in baleen from female North Atlantic right whales (Eubalaena glacialis) match known calving history. Conserv Physiol. 2016;4:cow014.
Hunt KE, Lysiak NS, Moore M, Rolland RM. Multi-year longitudinal profiles of cortisol and corticosterone recovered from baleen of North Atlantic right whales (Eubalaena glacialis). Gen Comp Endocrinol. 2017;254:50–9.
Hussain S, Ram MS, Kumar A, Shivaji S, Umapathy G. Human presence increases parasitic load in endangered lion-tailed macaques (Macaca silenus) in its fragmented rainforest habitats in southern India. PLoS One. 2013;8:e63685.
Hux VJ, Roberts JM. A potential role for allostatic load in preeclampsia. Matern Child Health J. 2015;19:591–7.
Hux VJ, Catov JM, Roberts JM. Allostatic load in women with a history of low birth weight infants: the national health and nutrition examination survey. J Womens Health. 2014;23:1039–45.
Hwang A-C, Peng L-N, Wen Y-W, Tsai Y-W, Chang L-C, Chiou S-T, Chen L-K. Predicting all-cause and cause-specific mortality by static and dynamic measurements of allostatic load: a 10-year population-based cohort study in Taiwan. J Am Med Dir Assoc. 2014;15:490–6.
Ioannou S, Chotard H, Davila-Ross M. No strings attached: physiological monitoring of rhesus monkeys (Macaca mulatta) with thermal imaging. Front Behav Neurosci. 2015;9:160.
Irvine RJ, White J, Chan R. The influence of restraint on blood pressure in the rat. J Pharmacol Toxicol Methods. 1997;38:157–62.
Jacobs RM, Ross SR, Wagner KE, Leahy M, Meiers ST, Santymire RM. Evaluating the physiological and behavioral response of a male and female gorilla (Gorilla gorilla gorilla) during an introduction. Zoo Biol. 2014;33:394–402.
Jang YH, Lee SJ, Lim JG, Lee HS, Kim TJ, Park JH, Chung BH, Choe NH. The rate of Salmonella spp. infection in zoo animals at Seoul Grand Park, Korea. J Vet Sci. 2008;9:177–81.
Jansson AM, Røsjø H, Omland T, Karlsson T, Hartford M, Flyvbjerg A, Caidahl K. Prognostic value of circulating chromogranin A levels in acute coronary syndromes. Eur Heart J. 2008;30:25–32.
Jarillo-Luna RA, Rivera-Aguilar V, Pacheco-Yépez J, Godínez-Victoria M, Oros-Pantoja R, Miliar-García A, Campos-Rodríguez R. Nasal IgA secretion in a murine model of acute stress. The possible role of catecholamines. J Neuroimmunol. 2015;278:223–31.
Jerem P, Jenni-Eiermann S, Herborn K, McKeegan D, McCafferty DJ, Nager RG. Eye region surface temperature reflects both energy reserves and circulating glucocorticoids in a wild bird. Sci Rep. 2018;8:1907.
Ji S, Yang L, Ge X, Wang B, Cao J, Hu D. Behavioural and physiological stress responses to transportation in a group of Przewalski’s horses (Equus ferus prezwalskii). J Anim Plant Sci. 2013;23:1077–84.
Johns DW, Marchant TA, Fairhurst GD, Speakman JR, Clark RG. Biomarker of burden: feather corticosterone reflects energetic expenditure and allostatic overload in captive waterfowl. Funct Ecol. 2018;32:345–57.
Johnstone CP, Reina RD, Lill A. Impact of anthropogenic habitat fragmentation on population health in a small, carnivorous marsupial. J Mammal. 2010;91:1332–41.
Jones P, Cordonnier N, Mahamba C, Burt FJ, Rakotovao F, Swanepoel R, André C, Dauger S, Bakkali Kassimi L. Encephalomyocarditis virus mortality in semi-wild bonobos (Pan paniscus). J Med Primatol. 2011;40:157–63.
Josserand R, Dupoué A, Agostini S, Haussy C, Le Galliard J-F, Meylan S. Habitat degradation increases stress-hormone levels during the breeding season, and decreases survival and reproduction in adult common lizards. Oecologia. 2017;184:75–86.
Jurke MH, Czekala NM, Lindburg DG, Millard SE. Fecal corticoid metabolite measurement in the cheetah (Acinonyx jubatus). Zoo Biol. 1997;16:133–47.
Juster RP, McEwen BS, Lupien SJ. Allostatic load biomarkers of chronic stress and impact on health and cognition. Neurosci Biobehav Rev. 2010;35:2–16.
Kagan R, Carter S, Allard S. A universal animal welfare framework for zoos. J Appl Anim Welf Sci. 2015;18:S1–S10.
Kalantaridou SN, Makrigiannakis A, Zoumakis E, Chrousos GP. Stress and the female reproductive system. J Reprod Immunol. 2004;62:61–8.
Kalantaridou SN, Zoumakis E, Makrigiannakis A, Lavasidis LG, Vrekoussis T, Chrousos GP. Corticotropin-releasing hormone, stress and human reproduction: an update. J Reprod Immunol. 2010;85:33–9.
Kanamaru Y, Kikukawa A, Shimamura K. Salivary chromogranin-A as a marker of psychological stress during a cognitive test battery in humans. Stress. 2006;9:127–31.
Kanno T, Asada N, Yanase H, Iwanaga T, Nishikawa Y, Hoshino M, Yanaihara N. Autonomic control of submandibular chromogranin A secretion in the anaesthetized rat. Biomed Res. 1998;19:411–4.
Kano F, Hirata S, Deschner T, Behringer V, Call J. Nasal temperature drop in response to a playback of conspecific fights in chimpanzees: a thermo-imaging study. Physiol Behav. 2016;155:83–94.
Karlamangla AS, Singer BH, McEwen BS, Rowe JW, Seeman TE. Allostatic load as a predictor of functional decline: MacArthur studies of successful aging. J Clin Epidemiol. 2002;55:696–710.
Karlamangla AS, Singer BH, Seeman TE. Reduction in allostatic load in older adults is associated with lower all-cause mortality risk: Macarthur studies of successful aging. Psychosom Med. 2006;68:500–7.
Karlamangla AS, Miller-Martinez D, Lachman ME, Tun PA, Koretz BK, Seeman TE. Biological correlates of adult cognition: midlife in the United States (MIDUS). Neurobiol Aging. 2014;35:387–94.
Kato Y, Kowalski CJ, Stohler CS. Habituation of the early pain-specific respiratory response in sustained pain. Pain. 2001;91:57–63.
Keay SD, Harlow CR, Wood PJ, Jenkins JM, Cahill DJ. Higher cortisol:cortisone ratios in the preovulatory follicle of completely unstimulated IVF cycles indicate oocytes with increased pregnancy potential. Hum Reprod. 2002;17:2410–4.
Kendall R, Howard L, Masters N, Grant R. The impact of elephant endotheliotropic herpesvirus on the captive Asian elephant (elephas maximus) population of the United Kingdom and Ireland (1995-2013). J Zoo Wildl Med. 2016;47:405–18.
Kerr MA. The structure and function of human IgA. Biochem J. 1990;271:285–96.
Kersey DC, Wildt DE, Brown JL, Snyder RJ, Huang Y, Monfort SL. Rising fecal glucocorticoid concentrations track reproductive activity in the female giant panda (Ailuropoda melanoleuca). Gen Comp Endocrinol. 2011;173:364–70.
Kershaw JL, Hall AJ. Seasonal variation in harbour seal (Phoca vitulina) blubber cortisol-a novel indicator of physiological state? Sci Rep. 2016;6:21889.
Khansari DN, Murgo AJ, Faith RE. Effects of stress on the immune system. Immunol Today. 1990;11:170–5.
Kiecolt-Glaser JK, Preacher KJ, MacCallum RC, Atkinson C, Malarkey WB, Glaser R. Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proc Natl Acad Sci U S A. 2003;100:9090–5.
Kikkawa A, Uchida Y, Nakade T, Taguchi K. Salivary secretory IgA concentrations in beagle dogs. J Vet Med Sci. 2003;65:689–93.
Kilgas P, Tilgar V, Mänd R. Hematological health state indices predict local survival in a small passerine bird, the great tit (Parus major). Physiol Biochem Zool. 2006;79:565–72.
Kimmel E, Arkin H, Berman A. Evaporative cooling of cattle: transport phenomena and thermovision. St. Joseph: American Society of Agricultural Engineers; 1992. p. 14.
Kirschbaum C, Kudielka BM, Gaab J, Schommer NC, Hellhammer DH. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom Med. 1999;61:154–62.
Knobil E, Neill J, editors. Encyclopedia of reproduction, vol. 1–4. New York: Academic Press; 1998.
Knutson B, Burgdorf J, Panksepp J. Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull. 2002;128:961.
Kock RA, Mihok SR, Wambua J, Mwanzia J, Saigawa K. Effects of translocation on hematologic parameters of free-ranging black rhinoceros (Diceros bicornis michaeli) in Kenya. J Zoo Wildl Med. 1999;30:389–96.
Kolbe T, Palme R, Tichy A, Rülicke T. Lifetime dependent variation of stress hormone metabolites in feces of two laboratory mouse strains. PLoS One. 2015;10:e0136112.
Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ. Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev. 1999;23:925–35.
Koren L, Whiteside D, Fahlman Å, Ruckstuhl K, Kutz S, Checkley S, Dumond M, Wynne-Edwards K. Cortisol and corticosterone independence in cortisol-dominant wildlife. Gen Comp Endocrinol. 2012;177:113–9.
Korgun E, Dohr G, Desoye G, Demir R, Kayisli U, Hahn T. Expression of insulin, insulin-like growth factor I and glucocorticoid receptor in rat uterus and embryo during decidualization, implantation and organogenesis. Reproduction. 2003;125:75–84.
Korhonen R, Lahti A, Hämäläinen M, Kankaanranta H, Moilanen E. Dexamethasone inhibits inducible nitric-oxide synthase expression and nitric oxide production by destabilizing mRNA in lipopolysaccharide-treated macrophages. Mol Pharmacol. 2002;62:698–704.
Koster A, Bosma H, Penninx BW, Newman AB, Harris TB, Van Eijk JTM, Kempen GI, Simonsick EM, Johnson KC, Rooks RN. Association of inflammatory markers with socioeconomic status. J Gerontol A Biol Sci Med Sci. 2006;61:284–90.
Kranendonk G, Hopster H, Eerdenburg FV, Reenen KV, Fillerup M, Groot JD, Korte M, Taverne M. Evaluation of oral administration of cortisol as a model for prenatal stress in pregnant sows. Am J Vet Res. 2005;66:780–90.
Kreuder C, Miller MA, Lowenstine LJ, Conrad PA, Carpenter TE, Jessup DA, Mazet JA. Evaluation of cardiac lesions and risk factors associated with myocarditis and dilated cardiomyopathy in southern sea otters (Enhydra lutris nereis). Am J Vet Res. 2005;66:289–99.
Kroboth PD, Salek FS, Pittenger AL, Fabian TJ, Frye RF. DHEA and DHEA-S: a review. J Clin Pharmacol. 1999;39:327–48.
Krohn TC, Hansen AK, Dragsted N. Telemetry as a method for measuring the impact of housing conditions on rats’ welfare. Anim Welf. 2003;12:53–62.
Kronfol Z, Turner R, Nasrallah H, Winokur G. Leukocyte regulation in depression and schizophrenia. Psychiatry Res. 1984;13:13–8.
Kubzansky LD, Kawachi I, Sparrow D. Socioeconomic status, hostility, and risk factor clustering in the normative aging study: any help from the concept of allostatic load? Ann Behav Med. 1999;21:330–8.
Kuraoka K, Nakamura K. The use of nasal skin temperature measurements in studying emotion in macaque monkeys. Physiol Behav. 2011;102:347–55.
Kurtycz LM, Wagner KE, Ross SR. The choice to access outdoor areas affects the behavior of great apes. J Appl Anim Welf Sci. 2014;17:185–97.
Kusano Y, Crews DE, Iwamoto A, Sone Y, Aoyagi K, Maeda T, Leahy R. Allostatic load differs by sex and diet, but not age in older Japanese from the Goto Islands. Ann Hum Biol. 2016;43:34–41.
Kvietkauskaite R, Vaicaitiene R, Mauricas M. The change in the amount of immunoglobulins as a response to stress experienced by soldiers on a peacekeeping mission. Int Arch Occup Environ Health. 2014;87:615–22.
Laitinen M, Valtonen T. Cardiovascular, ventilatory and total activity responses of brown trout to handling stress. J Fish Biol. 1994;45:933–42.
Lambert RB, Lambert NK. The effects of humor on secretory immunoglobulin A levels in school-aged children. Pediatr Nurs. 1995;21:16–9.
Lambeth SP, Hau J, Perlman JE, Martino M, Schapiro SJ. Positive reinforcement training affects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes). Am J Primatol. 2006;68:245–56.
Lamglait B, Joris A, Romey A, Bakkali-Kassimi L, Lemberger K. Fatal encephalomyocarditis virus infection in an African savanna elephant (Loxodonta africana) in a French zoo. J Zoo Wildl Med. 2015;46:393–6.
Lamond D. Synchronization of oestrus and ovulation in beef heifers. Proc Aust Soc Anim Prod. 1962;4:72–8.
Lantz EL, Lonsdorf EV, Heintz MR, Murray CM, Lipende I, Travis DA, Santymire RM. Non-invasive quantification of immunoglobulin A in chimpanzees (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania. Am J Primatol. 2016;80:e22558.
Laske TG, Garshelis DL, Iaizzo PA. Monitoring the wild black bear’s reaction to human and environmental stressors. BMC Physiol. 2011;11:13.
Laske TG, Iaizzo PA, Garshelis DL. Six years in the life of a mother bear-the longest continuous heart rate recordings from a free-ranging mammal. Sci Rep. 2017;7:40732.
Lattin CR, Ngai HM, Romero LM. Evaluating the stress response as a bioindicator of sub-lethal effects of crude oil exposure in wild house sparrows (Passer domesticus). PLoS One. 2014;9:e102106.
Laule G, Desmond T. Positive reinforcement training as an enrichment strategy. In: Shepherdson DJ, Mellen JD, Hutchins M, editors. Second nature: environmental enrichment for captive animals. Washington: Smithsonian Institution Press; 1998. p. 302–13.
Lazić MM, Carretero MA, Živković U, Crnobrnja-Isailović J. City life has fitness costs: reduced body condition and increased parasite load in urban common wall lizards, Podarcis muralis. Salamandra. 2017;53:10–7.
Lea AJ, Tung J, Archie EA, Alberts SC. Developmental plasticity: bridging research in evolution and human health. Evol Med Public Health. 2017;2017:162–75.
Lea AJ, Akinyi MY, Nyakundi R, Mareri P, Nyundo F, Kariuki T, Alberts SC, Archie EA, Tung J. Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons. Proc Natl Acad Sci U S A. 2018a;115:E12163–E71.
Lea JMD, Walker SL, Kerley GIH, Jackson J, Matevich SC, Shultz S. Non-invasive physiological markers demonstrate link between habitat quality, adult sex ratio and poor population growth rate in a vulnerable species, the Cape mountain zebra. Funct Ecol. 2018b;32:300–12.
Lèche A, Cortez MV, Della Costa NS, Navarro JL, Marin RH, Martella MB. Stress response assessment during translocation of captive-bred greater rheas into the wild. J Ornithol. 2016;157:599–607.
Lecorps B, Rödel HG, Féron C. Assessment of anxiety in open field and elevated plus maze using infrared thermography. Physiol Behav. 2016;157:209–16.
Lécu A, Ball R. Mycobacterial infections in zoo animals: relevance, diagnosis and management. Int Zoo Yearb. 2011;45:183–202.
Lee MS, Rim YH, Jeong D-M, Kim MK, Joo MC, Shin SH. Nonlinear analysis of heart rate variability during Qi therapy (external Qigong). Am J Chin Med. 2005;33:579–88.
Lee HY, Acosta TJ, Tanikawa M, Sakumoto R, Komiyama J, Tasaki Y, Piskula M, Skarzynski DJ, Tetsuka M, Okuda K. The role of glucocorticoid in the regulation of prostaglandin biosynthesis in non-pregnant bovine endometrium. J Endocrinol. 2007;193:127–35.
Leeds A, Boyer D, Ross SR, Lukas KE. The effects of group type and young silverbacks on wounding rates in western lowland gorilla (Gorilla gorilla gorilla) groups in North American zoos. Zoo Biol. 2015;34:296–304.
Leeds A, Elsner R, Lukas KE. The effect of positive reinforcement training on an adult female western lowland gorilla’s (Gorilla gorilla gorilla) rate of abnormal and aggressive behavior. Anim Behav Cogn. 2016;3:78–87.
Lees CM, Wilcken J. Sustaining the Ark: the challenges faced by zoos in maintaining viable populations. Int Zoo Yearb. 2009;43:6–18.
Lennartsson A-K, Kushnir MM, Bergquist J, Jonsdottir IH. DHEA and DHEA-S response to acute psychosocial stress in healthy men and women. Biol Psychol. 2012;90:143–9.
Leong KW, Ding JL. The unexplored roles of human serum IgA. DNA Cell Biol. 2014;33:823–9.
Leshyk R, Nol E, Chin EH, Burness G. Adult ovenbirds (Seiurus aurocapilla) show increased stress-responsiveness in logged forests. Gen Comp Endocrinol. 2013;194:295–9.
Levine ME, Crimmins EM. A comparison of methods for assessing mortality risk. Am J Hum Biol. 2014;26:768–76.
Levine S, Coe CL, Wiener SG. Psychoneuroendocrinology of stress: a psychobiological perspective. In: Brush FR, Levine S, editors. Psychoendocrinology. San Diego: Academic Press; 1989. p. 341–77.
Li H, Westover WC, Crawford TB. Sheep-associated malignant catarrhal fever in a petting zoo. J Zoo Wildl Med. 1999;30:408–12.
Liberzon I, Trujillo KA, Akil H, Young EA. Motivational properties of oxytocin in the conditioned place preference paradigm. Neuropsychopharmacology. 1997;17:353.
Lim YAL, Ngui R, Shukri J, Rohela M, Mat Naim HR. Intestinal parasites in various animals at a zoo in Malaysia. Vet Parasitol. 2008;157:154–9.
Lipowicz A, Szklarska A, Malina RM. Allostatic load and socioeconomic status in Polish adult men. J Biosoc Sci. 2014;46:155–67.
Liptrap R, Raeside J. Effect of cortisol on the response to gonadotrophin releasing hormone in the boar. J Endocrinol. 1983;97:75–81.
Lobato E, Moreno J, Merino S, Sanz JJ, Arriero E. Haematological variables are good predictors of recruitment in nestling pied flycatchers (Ficedula hypoleuca). Ecosci. 2005;12:27–34.
Loeding E, Thomas J, Bernier D, Santymire R. Using fecal hormonal and behavioral analyses to evaluate the introduction of two sable antelope at Lincoln Park Zoo. J Appl Anim Welf Sci. 2011;14:220–46.
Lomborg SR, Nielsen LR, Heegaard PM, Jacobsen S. Acute phase proteins in cattle after exposure to complex stress. Vet Res Commun. 2008;32:575–82.
López-Olvera JR, Marco I, Montané J, Casas-Díaz E, Lavín S. Effects of acepromazine on the stress response in southern chamois (Rupicapra pyrenaica) captured by means of drive-nets. Can J Vet Res. 2007;71:41.
Lopresti AL, Maker GL, Hood SD, Drummond PD. A review of peripheral biomarkers in major depression: the potential of inflammatory and oxidative stress biomarkers. Prog Neuropsychopharmacol Biol Psychiatry. 2014;48:102–11.
Łopucki R, Klich D, Ścibior A, Gołębiowska D, Perzanowski K. Living in habitats affected by wind turbines may result in an increase in corticosterone levels in ground dwelling animals. Ecol Indic. 2018;84:165–71.
Loucks EB, Sullivan LM, D’Agostino RB Sr, Larson MG, Berkman LF, Benjamin EJ. Social networks and inflammatory markers in the Framingham Heart Study. J Biosoc Sci. 2006;38:835–42.
Lowenstine LJ, McManamon R, Terio KA. Comparative pathology of aging great apes: bonobos, chimpanzees, gorillas, and orangutans. Vet Pathol. 2016;53:250–76.
Lubbock LA, Goh A, Ali S, Ritchie J, Whooley MA. Relation of low socioeconomic status to C-reactive protein in patients with coronary heart disease (from the heart and soul study). Am J Cardiol. 2005;96:1506–11.
Lucas RM, Ponsonby A-L, Dear K. Mid-life stress is associated with both up-and down-regulation of markers of humoral and cellular immunity. Stress. 2007;10:351–61.
Lupien SJ, Ouellet-Morin I, Hupbach A, Tu MT, Buss C, Walker D, Pruessner J, McEwen BS. Beyond the stress concept: allostatic load—a developmental biological and cognitive perspective. In: Ciccheti D, Cohen DJ, editors. Developmental psychopathology. 2nd ed. Hoboken: Wiley; 2006. p. 578–628.
Lutgendorf SK, Garand L, Buckwalter KC, Reimer TT, Hong S-Y, Lubaroff DM. Life stress, mood disturbance, and elevated interleukin-6 in healthy older women. J Gerontol A Biol Sci Med Sci. 1999;54:M434–M9.
Lutz W, Kierdorf H. Parasite loads of roe deer (Capreolus capreolus L.) from neighbouring habitats with different intensities of recreational traffic. Z Jagdwiss. 1997;43:251–8.
Lymbery AJ, Hassan M, Morgan DL, Beatty SJ, Doupé RG. Parasites of native and exotic freshwater fishes in south-western Australia. J Fish Biol. 2010;76:1770–85.
Macfarland LA, Mann DR. The inhibitory effects of ACTH and adrenalectomy on reproductive maturation in female rats. Biol Reprod. 1977;16:306–14.
Machatschke IH, Wallner B, Dittami J. Impact of social environment on female chimpanzee reproductive cycles. Horm Behav. 2006;50:126–31.
Madliger CL, Love OP. The need for a predictive, context-dependent approach to the application of stress hormones in conservation. Conserv Biol. 2014;28:283–7.
Maestripieri D, Georgiev AV. What cortisol can tell us about the costs of sociality and reproduction among free-ranging rhesus macaque females on Cayo Santiago. Am J Primatol. 2015;78:92–105.
Maestripieri D, Hoffman CL. Chronic stress, allostatic load, and aging in nonhuman primates. Dev Psychopathol. 2011;23:1187–95.
Mahesh VB, Brann DW. Regulation of the preovulatory gonadotropin surge by endogenous steroids. Steroids. 1998;63:616–29.
Mallavarapu S, Stoinski TS, Bloomsmith MA, Maple TL. Postconflict behavior in captive western lowland gorillas (Gorilla gorilla gorilla). Am J Primatol. 2006;68:789–801.
Mancera KF, Lisle A, Allavena R, Phillips CJ. The effects of mining machinery noise of different frequencies on the behaviour, faecal corticosterone and tissue morphology of wild mice (Mus musculus). Appl Anim Behav Sci. 2017;197:81–9.
Maninger N, Capitanio JP, Mason WA, Ruys JD, Mendoza SP. Acute and chronic stress increase DHEAS concentrations in rhesus monkeys. Psychoneuroendocrinology. 2010;35:1055–62.
Mann DR, Korowitz CD, Barraclough CA. Adrenal gland involvement in synchronizing the preovulatory release of LH in rats. Proc Soc Exp Biol Med. 1975;150:115–20.
Maple TL, Bocian D. Wellness as welfare. Zoo Biol. 2013;32:363–5.
Markowitz H. Behavioral enrichment in the zoo. New York: Van Norstrand Reinhold; 1982.
Markowitz H, Aday C. Power for captive animals: contingencies and nature. In: Shepherdson DJ, Mellen JD, Hutchins M, editors. Second nature: environmental enrichment for captive animals. Washington: Smithsonian Institution Press; 1998. p. 47–58.
Martin AL. The primatologist as a behavioral engineer. Am J Primatol. 2015;79:1–10.
Martinez-Mota R, Valdespino-Quevedo C, Sanchez-Ramos MA. Faecal cortisol levels as a measurement of stress due to habitat fragmentation in wild black howler monkeys (Alouatta pigra) in Mexico. Folia Primatol. 2004;75:299.
Masek-Hammerman K, Miller AD, Lin KC, MacKey J, Weissenböck H, Gierbolini L, Burgos A, Perez H, Mansfield KG. Epizootic myocarditis associated with encephalomyocarditis virus in a group of rhesus macaques (Macaca mulatta). Vet Pathol. 2012;49:386–92.
Masi A. Sex hormones and rheumatoid arthritis: cause or effect relationships in a complex pathophysiology? Clin Exp Rheumatol. 1995;13:227–40.
Mason GJ. Species differences in responses to captivity: stress, welfare and the comparative method. Trends Ecol Evol. 2010;25:713–21.
Mason GJ, Veasey JS. What do population-level welfare indices suggest about the well-being of zoo elephants? Zoo Biol. 2010;29:256–73.
Massironi S, Conte D, Sciola V, Spampatti MP, Ciafardini C, Valenti L, Rossi RE, Peracchi M. Plasma chromogranin A response to octreotide test: prognostic value for clinical outcome in endocrine digestive tumors. Am J Gastroenterol. 2010;105:2072.
Matas D, Keren-Rotem T, Koren L. A method to determine integrated steroid levels in wildlife claws. Gen Comp Endocrinol. 2016;230:26–8.
Mather JA. Cephalopod consciousness: behavioural evidence. Conscious Cogn. 2008;17:37–48.
Matsuura T, Takimura R, Yamaguchi M, Ichinose M. Estimation of restraint stress in rats using salivary amylase activity. J Physiol Sci. 2012;62:421–7.
Mattei J, Demissie S, Falcon LM, Ordovas JM, Tucker K. Allostatic load is associated with chronic conditions in the Boston Puerto Rican Health Study. Soc Sci Med. 2010;70:1988–96.
Matteri RL, Carroll JA, Dyer CJ. Neuroendocrine responses to stress. In: Moberg GP, Mench JA, editors. The biology of animal stress basic principles and implications for animal welfare. Oxon: CABI publishing; 2000. p. 43–76.
Mau M, Südekum KH, Johann A, Sliwa A, Kaiser T. Indication of higher salivary α-amylase expression in hamadryas baboons and geladas compared to chimpanzees and humans. J Med Primatol. 2010;39:187–90.
Mauss D, Li J, Schmidt B, Angerer P, Jarczok MN. Measuring allostatic load in the workforce: a systematic review. Ind Health. 2015;53:5–20.
Mayer J. Use of behavior analysis to recognize pain in small mammals. Lab Anim. 2007;36:43.
McClelland DC, Cheriff AD. The immunoenhancing effects of humor on secretory IgA and resistance to respiratory infections. Psychol Health. 1997;12:329–44.
McCraty R, Atkinson M, Tiller WA, Rein G, Watkins AD. The effects of emotions on short-term power spectrum analysis of heart rate variability. Am J Cardiol. 1995;76:1089–93.
McCraty R, Atkinson M, Rein G, Watkins AD. Music enhances the effect of positive emotional states on salivaryIgA. Stress Med. 1996;12:167–75.
McCraty R, Barrios-Choplin B, Rozman D, Atkinson M, Watkins AD. The impact of a new emotional self-management program on stress, emotions, heart rate variability, DHEA and cortisol. Integr Physiol Behav Sci. 1998;33:151–70.
McDade TW, Hawkley LC, Cacioppo JT. Psychosocial and behavioral predictors of inflammation in middle-aged and older adults: the Chicago health, aging, and social relations study. Psychosom Med. 2006;68:376–81.
McEwen BS. Protective and damaging effects of stress mediators. N Engl J Med. 1998a;338:171–9.
McEwen BS. Stress, adaptation, and disease. Allostasis and allostatic load. Ann N Y Acad Sci. 1998b;840:33–44.
McEwen BS. Allostasis and allostatic load: implications for neuropsychopharmacology. Neuropsychopharmacology. 2000;22:108–24.
McEwen BS. From molecules to mind: stress, individual differences, and the social environment. Ann N Y Acad Sci. 2001;935:42–9.
McEwen BS. Early life influences on life-long patterns of behavior and health. Ment Retard Dev Disabil Res Rev. 2003;9:149–54.
McEwen BS. Protective and damaging effects of the mediators of stress and adaptation: allostasis and allostatic load. In: Schulkin J, editor. Allostatis, homeostasis, and the costs of physiological adaptation. Cambridge: Cambridge University Press; 2004. p. 65–98.
McEwen BS. Brain on stress: how the social environment gets under the skin. Proc Natl Acad Sci U S A. 2012;109:17180–5.
McEwen BS, Seeman T. Protective and damaging effects of mediators of stress: elaborating and testing the concepts of allostasis and allostatic load. Ann N Y Acad Sci. 1999;896:30–47.
McEwen BS, Stellar E. Stress and the individual: mechanisms leading to disease. Arch Intern Med. 1993;153:2093–101.
McEwen BS, Wingfield JC. The concept of allostasis in biology and biomedicine. Horm Behav. 2003;43:2–15.
McGuire M, Vonk J, Fuller G, Allard S. Using an ambiguous cue paradigm to assess cognitive bias in gorillas (Gorilla gorilla gorilla) during a forage manipulation. Anim Behav Cogn. 2017a;4:70–83.
McGuire M, Vonk J, Johnson-Ulrich Z. Ambiguous results when using the ambiguous-cue paradigm to assess learning and cognitive bias in gorillas and a black bear. Behav Sci. 2017b;7:51.
McLeay D. Effects of ACTH on the pituitary-interrenal axis and abundance of white blood cell types in juvenile coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol. 1973;21:431–40.
McManamon R, Lowenstine L. Cardiovascular disease in great apes. In: Miller RE, Fowler ME, editors. Fowler’s zoo and wild animal medicine: current therapy. St. Louis: Elsevier; 2012. p. 408–15.
Meehan CL, Mench JA. The challenge of challenge: can problem solving opportunities enhance animal welfare? Appl Anim Behav Sci. 2007;102:246–61.
Meijs-Roelofs H, Kramer P. Effects of adrenalectomy on the release of follicle-stimulating hormone and the onset of puberty in female rats. J Endocrinol. 1977;75:419–26.
Meillère A, Brischoux F, Bustamante P, Michaud B, Parenteau C, Marciau C, Angelier F. Corticosterone levels in relation to trace element contamination along an urbanization gradient in the common blackbird (Turdus merula). Sci Total Environ. 2016;566:93–101.
Mellor D, Beausoleil N. Extending the ‘Five Domains’ model for animal welfare assessment to incorporate positive welfare states. Anim Welf. 2015;24:241–53.
Mellor D, Reid C. Concepts of animal well-being and predicting the impact of procedures on experimental animals. In: Improving the well-being of animals in the research environment. Glen Osmond: Australian and New Zealand Council for the Care of Animals in Research and Teaching; 1994. p. 3–18.
Mellor DJ, Hunt S, Gusset M, editors. Caring for wildlife: the world zoo and aquarium animal welfare strategy. Gland: WAZA Executive Office; 2015.
Menargues A, Urios V, Mauri M. Welfare assessment of captive Asian elephants (Elephas maximus) and Indian rhinoceros (Rhinoceros unicornis) using salivary cortisol measurement. Anim Welf. 2008;17:305–12.
Menargues A, Urios V, Liminana R, Mauri M. Circadian rhythm of salivary cortisol in Asian elephants (Elephas maximus): a factor to consider during welfare assessment. J Appl Anim Welf Sci. 2012;15:383–90.
Mendl M, Burman OH, Parker RM, Paul ES. Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms. Appl Anim Behav Sci. 2009;118:161–81.
Mendl M, Burman OH, Paul ES. An integrative and functional framework for the study of animal emotion and mood. Proc R Soc Lond B. 2010;277:2895–904.
Mendonça-Furtado O, Edaes M, Palme R, Rodrigues A, Siqueira JÉ, Izar PÍ. Does hierarchy stability influence testosterone and cortisol levels of bearded capuchin monkeys (Sapajus libidinosus) adult males? A comparison between two wild groups. Behav Processes. 2014;109:79–88.
Metzler AE, Ossent P, Guscetti F, R übel A, Lang EM. Serological evidence of herpesvirus infection in captive Asian elephants (Elephas maximus). J Wildl Dis. 1990;26:41–9.
Meyer JM, Walker SL, Freeman EW, Steinetz BG, Brown JL. Species and fetal gender effects on the endocrinology of pregnancy in elephants. Gen Comp Endocrinol. 2004;138:263–70.
Michael AE, Papageorghiou AT. Potential significance of physiological and pharmacological glucocorticoids in early pregnancy. Hum Reprod Update. 2008;14:497–517.
Miller RE, Fowler M, editors. Fowler’s zoo and wild animal medicine current therapy, vol. 7. St. Louis: Elsevier Saunders; 2012.
Mitsui S, Yamamoto M, Nagasawa M, Mogi K, Kikusui T, Ohtani N, Ohta M. Urinary oxytocin as a noninvasive biomarker of positive emotion in dogs. Horm Behav. 2011;60:239–43.
Miyakawa M, Matsui T, Kishikawa H, Murayama R, Uchiyama I, Itoh T, Yoshida T. Salivary chromogranin A as a measure of stress response to noise. Noise Health. 2006;8:108.
Mizoguchi K, Ishige A, Takeda S, Aburada M, Tabira T. Endogenous glucocorticoids are essential for maintaining prefrontal cortical cognitive function. J Neurosci. 2004;24:5492–9.
Moberg GP. How behavioral stress disrupts the endocrine control of reproduction in domestic animals. J Dairy Sci. 1991;74:304–11.
Moberg G. Biological responses to stress: implications for animal welfare. In: Moberg GP, Mench JA, editors. The biology of animal stress basic principles and implications for animal welfare. Oxon: CABI publishing; 2000. p. 1–21.
Moberg GP, Mench JA, editors. The biology of animal stress. Basic principles and implications for animal welfare. Oxon: CABI Publishing; 2000.
Moe RO, Stubsjøen SM, Bohlin J, Flø A, Bakken M. Peripheral temperature drop in response to anticipation and consumption of a signaled palatable reward in laying hens (Gallus domesticus). Physiol Behav. 2012;106:527–33.
Moll RJ, Millspaugh JJ, Beringer J, Sartwell J, Woods RJ, Vercauteren KC. Physiological stress response of captive white-tailed deer to video collars. J Wildl Manage. 2009;73:609–14.
Mommersteeg PM, Heijnen CJ, Kavelaars A, van Doornen LJ. Immune and endocrine function in burnout syndrome. Psychosom Med. 2006;68:879–86.
Monclús L, Ballesteros-Cano R, De La Puente J, Lacorte S, Lopez-Bejar M. Influence of persistent organic pollutants on the endocrine stress response in free-living and captive red kites (Milvus milvus). Environ Pollut. 2018;242:329–37.
Montali RJ, Mikota SK, Cheng LI. Mycobacterium tuberculosis in zoo and wildlife species. Rev Sci Tech Off int Epiz. 2001;20:291–303.
Monti F, Duriez O, Dominici JM, Sforzi A, Robert A, Fusani L, Grémillet D. The price of success: integrative long-term study reveals ecotourism impacts on a flagship species at a UNESCO site. Anim Conserv. 2018;21:448–58.
Moodie EM, Chamove AS. Brief threatening events beneficial for captive tamarins? Zoo Biol. 1990;9:275–86.
Moore IT, Jessop TS. Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Horm Behav. 2003;43:39–47.
Moreira N, Brown JL, Moraes W, Swanson WF, Monteiro ELA. Effect of housing and environmental enrichment on adrenocortical activity, behavior and reproductive cyclicity in the female tigrina (Leopardus tigrinus) and margay (Leopardus wiedii). Zoo Biol. 2007;26:441–60.
Moreno J, Merino S, Martínez J, Sanz J, Arriero E. Heterophil/lymphocyte ratios and heat-shock protein levels are related to growth in nestling birds. Ecosci. 2002;9:434–9.
Morgan KN, Tromborg CT. Sources of stress in captivity. Appl Anim Behav Sci. 2007;102:262–302.
Morgan CA, Southwick S, Hazlett G, Rasmusson A, Hoyt G, Zimolo Z, Charney D. Relationships among plasma dehydroepiandrosterone sulfate and cortisol levels, symptoms of dissociation, and objective performance in humans exposed to acute stress. Arch Gen Psychiatry. 2004;61:819–25.
Morgan D, Mundry R, Sanz C, Ayina CE, Strindberg S, Lonsdorf E, Kühl HS. African apes coexisting with logging: comparing chimpanzee (Pan troglodytes troglodytes) and gorilla (Gorilla gorilla gorilla) resource needs and responses to forestry activities. Biol Conserv. 2018;218:277–86.
Morici LA, Elsey RM, Lance VA. Effects of long-term corticosterone implants on growth and immune function in juvenile alligators, Alligator mississippiensis. J Exp Zool. 1997;279:156–62.
Mormède P, Andanson S, Aupérin B, Beerda B, Guémené D, Malmkvist J, Manteca X, Manteuffel G, Prunet P, van Reenen CG, Richard S, Veissier I. Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare. Physiol Behav. 2007;92:317–39.
Morrison S, Shenassa ED, Mendola P, Wu T, Schoendorf K. Allostatic load may not be associated with chronic stress in pregnant women, NHANES 1999-2006. Ann Epidemiol. 2013;23:294–7.
Morrow-Tesch J, McGlone J, Norman R. Consequences of restraint stress on natural killer cell activity, behavior, and hormone levels in rhesus macaques (Macaca mulatta). Psychoneuroendocrinology. 1993;18:383–95.
Mostl E, Palme R. Hormones as indicators of stress. Domest Anim Endocrinol. 2002;23:67–74.
Muehlenbein MP, Watts DP. The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. Biopsychosoc Med. 2010;4:1–12.
Müllner A, Linsenmair KE, Wikelski M. Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin). Biol Conserv. 2004;118:549–58.
Mumby HS, Mar KU, Hayward AD, Htut W, Htut-Aung Y, Lummaa V. Elephants born in the high stress season have faster reproductive ageing. Sci Rep. 2015;5:1–11.
Munck A, Koritz SB. Studies on the mode of action of glucocorticoids in rats I. Early effects of cortisol on blood glucose and on glucose entry into muscle, liver and adipose tissue. Biochim Biophys Acta. 1962;57:310–7.
Muneta Y, Yoshikawa T, Minagawa Y, Shibahara T, Maeda R, Omata Y. Salivary IgA as a useful non-invasive marker for restraint stress in pigs. J Vet Med Sci. 2010;72:1295–300.
Muneta Y, Minagawa Y, Nakane T, Shibahara T, Yoshikawa T, Omata Y. Interleukin-18 expression in pig salivary glands and salivary content changes during acute immobilization stress. Stress. 2011;14:549–56.
Munson L, Nesbit JW, Meltzer DGA, Colly LP, Bolton L, Kriek NPJ. Diseases of captive cheetahs (Acinonyx jubatus jubatus) in South Africa: a 20-year retrospective survey. J Zoo Wildl Med. 1999;30:342–7.
Murphy HW, Danforth MD, Clyde VL. The Great Ape Heart Project. Int Zoo Yearb. 2018;52:1–10.
Murray CM, Stanton MA, Wellens KR, Santymire RM, Heintz MR, Lonsdorf EV. Maternal effects on offspring stress physiology in wild chimpanzees. Am J Primatol. 2018;80:1–12.
Nakane H, Asami O, Yamada Y, Harada T, Matsui N, Kanno T, Yanaihara N. Salivary chromogranin A as an index of psychosomatic stress response. Biomed Res. 1998;19:401–6.
Nakayama K, Goto S, Kuraoka K, Nakamura K. Decrease in nasal temperature of rhesus monkeys (Macaca mulatta) in negative emotional state. Physiol Behav. 2005;84:783–90.
Narayan E, Molinia F, Christi K, Morley C, Cockrem J. Urinary corticosterone metabolite responses to capture, and annual patterns of urinary corticosterone in wild and captive endangered Fijian ground frogs (Platymantis vitiana). Aust J Zool. 2010;58:189–97.
Narayan EJ, Cockrem JF, Hero J-M. Urinary corticosterone metabolite responses to capture and handling in two closely related species of free-living Fijian frogs. Gen Comp Endocrinol. 2012;177:55–61.
Nater UM, Rohleder N. Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: current state of research. Psychoneuroendocrinology. 2009;34:486–96.
Nater UM, La Marca R, Florin L, Moses A, Langhans W, Koller MM, Ehlert U. Stress-induced changes in human salivary alpha-amylase activity—associations with adrenergic activity. Psychoneuroendocrinology. 2006;31:49–58.
Nater UM, Rohleder N, Schlotz W, Ehlert U, Kirschbaum C. Determinants of the diurnal course of salivary alpha-amylase. Psychoneuroendocrinology. 2007;32:392–401.
Navarro-Castilla Á, Mata C, Ruiz-Capillas P, Palme R, Malo JE, Barja I. Are motorways potential stressors of roadside wood mice (Apodemus sylvaticus) populations? PLoS One. 2014;9:e91942.
Nelson RJ. An introduction to behavioral endocrinology. 4th ed. Sunderland: Sinauer Associates; 2011.
Nelson KM, Reiber G, Kohler T, Boyko EJ. Peripheral arterial disease in a multiethnic national sample: the role of conventional risk factors and allostatic load. Ethn Dis. 2007;17:669–75.
Neumann I, Johnstone H, Hatzinger M, Liebsch G, Shipston M, Russell J, Landgraf R, Douglas A. Attenuated neuroendocrine responses to emotional and physical stressors in pregnant rats involve adenohypophysial changes. J Physiol. 1998;508:289–300.
Newman AE, Pradhan DS, Soma KK. Dehydroepiandrosterone and corticosterone are regulated by season and acute stress in a wild songbird: jugular versus brachial plasma. Endocrinology. 2008;149:2537–45.
Newton R, Kuitert L, Slater D, Adcock I, Barnes P. Cytokine induction of cytosolic phospholipase A2 and cyclooxygenase-2 mRNA is suppressed by glucocorticoids in human epithelial cells. Life Sci. 1996;60:67–78.
Ng V, Koh D, Chan G, Ong H, Chia S, Ong C. Are salivary immunoglobulin A and lysozyme biomarkers of stress among nurses? J Occup Environ Med. 1999;41:920–7.
Nganvongpanit K, Soponteerakul R, Kaewkumpai P, Punyapornwithawa V, Buddhachat K, Nomsiri R, Kaewmong P, Kittiwatanawong K, Chawangwongsanukun R, Angkawanish T, Thitaram C, Mahakkanukrauh P. Osteoarthritis in two marine mammals and 22 land mammals: learning from skeletal remains. J Anat. 2017;231:140–55.
Niebylski A, Boccolini A, Bensi N, Binotti S, Hansen C, Yaciuk R, Gauna H. Neuroendocrine changes and natriuresis in response to social stress in rats. Stress Health. 2012;28:179–85.
Nisenbaum LK, Zigmond MJ, Sved AF, Abercrombie ED. Prior exposure to chronic stress results in enhanced synthesis and release of hippocampal norepinephrine in response to a novel stressor. J Neurosci. 1991;11:1478–84.
Noda K, Akiyoshi H, Aoki M, Shimada T, Ohashi F. Relationship between transportation stress and polymorphonuclear cell functions of bottlenose dolphins, Tursiops truncatus. J Vet Med Sci. 2007;69:379–83.
Nussey DH, Kruuk LEB, Morris A, Clutton-Brock TH. Environmental conditions in early life influence ageing rates in a wild population of red deer. Curr Biol. 2007;17:R1000–R1.
O’Connor JC, André C, Wang Y, Lawson MA, Szegedi SS, Lestage J, Castanon N, Kelley KW, Dantzer R. Interferon-γ and tumor necrosis factor-α mediate the upregulation of indoleamine 2, 3-dioxygenase and the induction of depressive-like behavior in mice in response to bacillus Calmette-Guérin. J Neurosci. 2009;29:4200–9.
O’Toole D, Grossman A, Gross D, Delle Fave G, Barkmanova J, O’Connor J, Pape U-F, Plöckinger U. ENETS consensus guidelines for the standards of care in neuroendocrine tumors: biochemical markers. Neuroendocrinology. 2009;90:194–202.
Okeson DM, Garner MM, Taus NS, Li H, Coke RL. Ibex-associated malignant catarrhal fever in a bongo antelope (Tragelaphus euryceros). J Zoo Wildl Med. 2007;38:460–4.
Olefsky JM, Kimmerling G. Effects of glucocorticoids on carbohydrate metabolism. Am J Med Sci. 1976;271:202–10.
Olster DH, Ferin M. Corticotropin-releasing hormone inhibits gonadotropin-secretion in the ovariectomized rhesus monkey. J Clin Endocrinol Metab. 1987;65:262–7.
Onderka DK, Finlayson MC. Salmonellae and salmonellosis in captive reptiles. Can J Comp Med. 1985;49:268–70.
Ordóñez-Gómez JD, Cristóbal-Azkarate J, Arroyo-Rodríguez V, Santillán-Doherty AM, Valdez RA, Romano MC. Proximal and distal predictors of the spider monkey’s stress levels in fragmented landscapes. PLoS One. 2016;11:e0149671.
Orr TE, Taylor MF, Bhattacharyya AK, Collins DC, Mann DR. Acute immobilization stress disrupts testicular steroidogenesis in adult male rats by inhibiting the activities of 17-alpha-hydroxylase and 17,20-lyase without affecting the binding of LH/HCG receptors. J Androl. 1994;15:302–8.
Ott S, Soler L, Moons C, Kashiha M, Bahr C, Vandermeulen J, Janssens S, Gutiérrez A, Escribano D, Cerón J. Different stressors elicit different responses in the salivary biomarkers cortisol, haptoglobin, and chromogranin A in pigs. Res Vet Sci. 2014;97:124–8.
Otten W, Puppe B, Kanitz E, Schön PC, Stabenow B. Physiological and behavioral effects of different success during social confrontation in pigs with prior dominance experience. Physiol Behav. 2002;75:127–33.
Palagi E, Norscia I. Bonobos protect and console friends and kin. PLoS One. 2013;8:e79290.
Palagi E, Chiarugi E, Cordoni G. Peaceful post-conflict interactions between agressors and bystanders in captive lowland gorillas (Gorilla gorilla gorilla). Am J Primatol. 2008;70:949–55.
Palme R. Measuring fecal steroids: guidelines for practical application. Ann N Y Acad Sci. 2005;1046:75–80.
Palme R. Monitoring stress hormone metabolites as a useful, non-invasive tool for welfare assessment in farm animals. Anim Welf. 2012;21:331.
Palme R. Non-invasive measurement of stress hormones: advances and problems. Physiol Behav. 2019;199:229–43.
Papargiris MM, Rivalland ETA, Hemsworth PH, Morrissey AD, Tilbrook AJ. Acute and chronic stress-like levels of cortisol inhibit the oestradiol stimulus to induce sexual receptivity but have no effect on sexual attractivity or proceptivity in female sheep. Horm Behav. 2011;60:336–45.
Paramastri Y, Royo F, Eberova J, Carlsson HE, Sajuthi D, Fernstrom AL, Pamungkas J, Hau J. Urinary and fecal immunoglobulin A, cortisol and 11-17 dioxoandrostanes, and serum cortisol in metabolic cage housed female cynomolgus monkeys (Macaca fascicularis). J Med Primatol. 2007;36:355–64.
Parga ML, Pendl H, Forbes NA. The effect of transport on hematologic parameters in trained and untrained Harris’s hawks (Parabuteo unicinctus) and peregrine falcons (Falco peregrinus). J Avian Med Surg. 2001;15:162–9.
Park SE, Park D, Song K-I, Seong J-K, Chung S, Youn I. Differential heart rate variability and physiological responses associated with accumulated short-and long-term stress in rodents. Physiol Behav. 2017;171:21–31.
Parker VJ, Douglas AJ. Stress in early pregnancy: maternal neuro-endocrine-immune responses and effects. J Reprod Immunol. 2010;85:86–92.
Parrott R, Hall S, Lloyd D. Heart rate and stress hormone responses of sheep to road transport following two different loading procedures. Anim Welf. 1998;7:257–67.
Pearce G, Paterson A, Hughes P. Effect of short-term elevations in plasma cortisol concentration on LH secretion in prepubertal gilts. J Reprod Fertil. 1988;83:413–8.
Penfold LM, Powell D, Traylor-Holzer K, Asa CS. “Use it or lose it”: characterization, implications, and mitigation of female infertility in captive wildlife. Zoo Biol. 2014;33:20–8.
Peppler R, Jacobs JJ. The effect of adrenalectomy on ovulation and follicular development in the rat. Biol Reprod. 1976;15:173–8.
Pereia RJG, Granzinolli MAM, De Barros FM, Duarte JMB. Influence of radiotransmitters on fecal glucocorticoid levels of free-ranging male American kestrels. J Wildl Manage. 2009;73:772–8.
Peric T, Corazzin M, Romanzin A, Bovolenta S, Prandi A, Montillo M, Comin A. Cortisol and DHEA concentrations in the hair of dairy cows managed indoor or on pasture. Livest Sci. 2017;202:39–43.
Peters A, McEwen BS, Friston K. Uncertainty and stress: why it causes diseases and how it is mastered by the brain. Prog Neurobiol. 2017;156:164–88.
Petrovic D, Pivin E, Ponte B, Dhayat N, Pruijm M, Ehret G, Ackermann D, Guessous I, Younes SE, Pechére-Bertschi A, Vogt B, Mohaupt M, Martin P-Y, Paccaud F, Burnier M, Bochud M, Stringhini S. Sociodemographic, behavioral and genetic determinants of allostatic load in a Swiss population-based study. Psychoneuroendocrinology. 2016;67:76–85.
Phillips DM, Lakshmi V, Monder C. Corticosteroid 11-beta-dehydrogenase in rat testis. Endocrinology. 1989;125:209–16.
Piccione G, Casella S, Giannetto C, Giudice E, Fazio F. Utility of acute phase proteins as biomarkers of transport stress in ewes. Small Rumin Res. 2012;107:167–71.
Pihl L, Hau J. Faecal corticosterone and immunoglobulin A in young adult rats. Lab Anim. 2003;37:166–71.
Pineiro M, Pineiro C, Carpintero R, Morales J, Campbell FM, Eckersall PD, Toussaint MJ, Lampreave F. Characterisation of the pig acute phase protein response to road transport. Vet J. 2007;173:669–74.
Piñeiro A, Barja I, Silván G, Illera JC. Effects of tourist pressure and reproduction on physiological stress response in wildcats: management implications for species conservation. Wildl Res. 2012;39:532–9.
Poessel SA, Biggins DE, Santymire RM, Livieri TM, Crooks KR, Angeloni L. Environmental enrichment affects adrenocortical stress responses in the endangered black-footed ferret. Gen Comp Endocrinol. 2011;172:526–33.
Pohlin F, Brabender K, Fluch G, Stalder G, Petit T, Walzer C. Seasonal variations in heart rate variability as an indicator of stress in free-ranging pregnant Przewalski’s horses (E. ferus przewalskii) within Hortobágy National Park in Hungary. Front Physiol. 2017;8:1–11.
Pomerantz O, Terkel J. Effects of positive reinforcement training techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). Am J Primatol. 2009;71:687–95.
Poole TB. Meeting a mammal’s psychological needs: basic principles. In: Shepherdson DJ, Mellen JD, Hutchins M, editors. Second nature: environmental enrichment for captive animals. Washington: Smithsonian Institution Press; 1998. p. 83–94.
Powell DM. Collection planning for the next 100 years: what will we commit to save in zoos and aquariums? Zoo Biol. 2019;38:139–48.
Prado NA, Keady M, Oestmann A, Steinbeiser CM, Brown JL. Hyperprolactinemic African elephant (Loxodonta africana) females exhibit elevated dopamine, oxytocin and serotonin concentrations compared to normal cycling and non-cycling, low prolactin elephants. Biol Reprod. 2019; https://doi.org/10.1093/biolre/ioz036.
Pressman SD, Cohen S. Does positive affect influence health? Psychol Bull. 2005;131:925–71.
Price EE, Stoinski TS. Group size: determinants in the wild and implications for the captive housing of wild mammals in zoos. Appl Anim Behav Sci. 2007;103:255–64.
Price K, Kittridge C, Damby Z, Hayes SG, Addis EA. Relaxing life of the city? Allostatic load in yellow-bellied marmots along a rural-urban continuum. Conserv Physiol. 2018;6:coy070.
Prior L, Manley D, Jones K. Stressed out? An investigation of whether allostatic load mediates associations between neighbourhood deprivation and health. Health Place. 2018;52:25–33.
Proctor HS, Carder G. Nasal temperatures in dairy cows are influenced by positive emotional state. Physiol Behav. 2015;138:340–4.
Prunier A, Leterrier C. How should pain in farm animals be assessed? Adv Anim Biosci. 2014;5:310–8.
Pryce CR, Dettling AC, Spengler M, Schnell CR, Feldon J. Deprivation of parenting disrupts development of homeostatic and reward systems in marmoset monkey offspring. Biol Psychiatry. 2004;56:72–9.
Qiu X, Mainka SA. Review of mortality of the giant panda (Ailuropoda melanoleuca). J Zoo Wildl Med. 1993;24:425–9.
Quenby S, Farquharson R, Young M, Vince G. Successful pregnancy outcome following 19 consecutive miscarriages: case report. Hum Reprod. 2003;18:2562–4.
Quenby S, Kalumbi C, Bates M, Farquharson R, Vince G. Prednisolone reduces preconceptual endometrial natural killer cells in women with recurrent miscarriage. Fertil Steril. 2005;84:980–4.
Rabin DS, Johnson EO, Brandon DD, Liapi C, Chrousos GP. Glucocorticoids inhibit estradiol-mediated uterine growth—possible role of the uterine estradiol-receptor. Biol Reprod. 1990;42:74–80.
Radwan J, Kuduk K, Levy E, LeBas N, Babik W. Parasite load and MHC diversity in undisturbed and agriculturally modified habitats of the ornate dragon lizard. Mol Ecol. 2014;23:5966–78.
Raharivololona BM, Ganzhorn JU. Gastrointestinal parasite infection of the gray mouse lemur (Microcebus murinus) in the littoral forest of Mandena, Madagascar: effects of forest fragmentation and degradation. Madag Conserv Dev. 2009;4:103–12.
Rainville P, Bechara A, Naqvi N, Damasio AR. Basic emotions are associated with distinct patterns of cardiorespiratory activity. Int J Psychophysiol. 2006;61:5–18.
Rakotoniaina JH, Kappeler PM, Ravoniarimbinina P, Pechouskova E, Hämäläinen AM, Grass J, Kirschbaum C, Kraus C. Does habitat disturbance affect stress, body condition and parasitism in two sympatric lemurs? Conserv Physiol. 2016;4:cow034.
Ralph C, Tilbrook A. The usefulness of measuring glucocorticoids for assessing animal welfare. J Anim Sci. 2016;94:457–70.
Ramaley JA. Adrenal-gonadal interactions at puberty. Life Sci. 1974;14:1623–33.
Raouf SA, Smith LC, Brown MB, Wingfield JC, Brown CR. Glucocorticoid hormone levels increase with group size and parasite load in cliff swallows. Anim Behav. 2006;71:39–48.
Read S, Grundy E. Allostatic load—a challenge to measure multisystem physiological dysregulation. London: National Centre for Research Methods; 2012. p. 1–9.
Reddacliff LA, Kirkland PD, Hartley WJ, Reece RL. Encephalomyocarditis virus infections in an Australian Zoo. J Zoo Wildl Med. 1997;28:153–7.
Rehbinder C, Hau J. Quantification of cortisol, cortisol immunoreactive metabolites, and immunoglobulin A in serum, saliva, urine, and feces for noninvasive assessment of stress in reindeer. Can J Vet Res. 2006;70:151–4.
Reidarson TH, McBain JF. Hematologic, biochemical, and endocrine effects of dexamethasone on bottlenose dolphins (Tursiops truncatus). J Zoo Wildl Med. 1999;30:310–2.
Richman LK, Montali RJ, Cambre RC, Schmitt D, Hardy D, Hildbrandt T, Bengis RG, Hamzeh FM, Shahkolahi A, Hayward GS. Clinical and pathological findings of a newly recognized disease of elephants caused by endotheliotropic herpesviruses. J Wildl Dis. 2000a;36:1–12.
Richman LK, Montali RJ, Hayward GS. Review of a newly recognized disease of elephants caused by endotheliotropic herpesviruses. Zoo Biol. 2000b;19:383–92.
Riemer S, Assis L, Pike TW, Mills DS. Dynamic changes in ear temperature in relation to separation distress in dogs. Physiol Behav. 2016;167:86–91.
Rimbach R, Link A, Heistermann M, Gómez-Posada C, Galvis N, Heymann EW. Effects of logging, hunting, and forest fragment size on physiological stress levels of two sympatric ateline primates in Colombia. Conserv Physiol. 2013;1:cot031.
Rivier C, Rivest S. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis—peripheral and central mechanisms. Biol Reprod. 1991;45:523–32.
Robbins MM, Gray M, Fawcett KA, Nutter FB, Uwingeli P, Mburanumwe I, Kagoda E, Basabose A, Stoinski TS, Cranfield MR, Byamukama J, Spelman LH, Robbins AM. Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS One. 2011;6:e19788.
Robert KA, Schwanz LE. Monitoring the health status of free-ranging tammar wallabies using hematology, serum biochemistry, and parasite loads. J Wildl Manage. 2013;77:1232–43.
Robertson T, Beveridge G, Bromley C. Allostatic load as a predictor of all-cause and cause-specific mortality in the general population: evidence from the Scottish Health Survey. PLoS One. 2017;12:1–14.
Robinson LM, Altschul DM, Wallace EK, Úbeda Y, Llorente M, Machanda Z, Slocombe KE, Leach MC, Waran NK, Weiss A. Chimpanzees with positive welfare are happier, extraverted, and emotionally stable. Appl Anim Behav Sci. 2017;191:90–7.
Robinson LM, Coleman K, Capitanio JP, Gottlieb DH, Handel IG, Adams MJ, Leach MC, Waran NK, Weiss A. Rhesus macaque personality, dominance, behavior, and health. Am J Primatol. 2018;80:e22739.
Rodriguez EJ, Livaudais-Toman J, Gregorich SE, Jackson JS, Nápoles AM, Pérez-Stable EJ. Relationships between allostatic load, unhealthy behaviors, and depressive disorder in U.S. adults, 2005-2012 NHANES. Prev Med. 2018;110:9–15.
Romero LM, Wikelski M. Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proc Natl Acad Sci U S A. 2001;98:7366–70.
Romero LM, Wikelski M. Severe effects of low-level oil contamination on wildlife predicted by the corticosterone-stress response: preliminary data and a research agenda. Spill Sci Technol Bull. 2002;7:309–13.
Rosen JB, Schulkin J. Adaptive fear, allostasis, and the pathology of anxiety and depression. In: Schulkin J, editor. Allostasis, homeostasis, and the costs of physiological adaptation. Cambridge: Cambridge University Press; 2004. p. 164–227.
Rosenberg N, Park CG, Eldeirawi K. Relationship of serum carotenoid concentrations with allostatic load as a measure of chronic stress among middle-aged adults in the USA. Public Health Nutr. 2014;18:313–21.
Ross SR. Issues of choice and control in the behaviour of a pair of captive polar bears (Ursus maritimus). Behav Processes. 2006;73:117–20.
Rossdale P, Burguez P, Cash R. Changes in blood neutrophil/lymphocyte ratio related to adrenocortical function in the horse. Equine Vet J. 1982;14:293–8.
Rosvall M, Engström G, Janzon L, Berglund G, Hedblad B. The role of low grade inflammation as measured by C-reactive protein levels in the explanation of socioeconomic differences in carotid atherosclerosis. Eur J Public Health. 2006;17:340–7.
Rowden LJ, Rose PE. A global survey of banteng (Bos javanicus) housing and husbandry. Zoo Biol. 2016;35:546–55.
Royo F, Bjork N, Carlsson HE, Mayo S, Hau J. Impact of chronic catheterization and automated blood sampling (Accusampler) on serum corticosterone and fecal immunoreactive corticosterone metabolites and immunoglobulin A in male rats. J Endocrinol. 2004;180:145–53.
Royo F, Lyberg K, Abelson KS, Carlsson HE, Hau J. Effect of repeated confined single housing of young pigs on faecal excretion of cortisol and IgA. Scand J Lab Anim Sci. 2005;32:33–7.
Rubenstein DR, Shen S-F. Reproductive conflict and the costs of social status in cooperatively breeding vertebrates. Am Nat. 2009;173:650–61.
Ruby S, Buchanan-Smith HM. The effects of individual cubicle research on the social interactions of individual behavior of brown capuchin monkeys (Sapajus apella). Am J Primatol. 2015;77:1097–108.
Sabbah W, Watt RG, Sheiham A, Tsakos G. Effects of allostatic load on the social gradient in ischaemic heart disease and periodontal disease: evidence from the Third National Health and Nutrition Examination Survey. J Epidemiol Community Health. 2008;62:415–20.
Salas M, Temple D, Abáigar T, Cuadrado M, Delclaux M, Enseñat C, Almagro V, Martínez-Nevado E, Quevedo MÁ, Carbajal A, Tallo-Parra O, Sabés-Alsina M, Amat M, Lopez-Bejar M, Fernández-Bellon H, Manteca X. Aggressive behavior and hair cortisol levels in captive Dorcas gazelles (Gazella dorcas) as animal-based welfare indicators. Zoo Biol. 2016;35:467–73.
Samaras A, Santo CE, Papandroulakis N, Mitrizakis N, Pavlidis M, Höglund E, Pelgrim TNM, Zethof J, Spanings FAT, Vindas MA, Ebbesson LOE, Flik G, Gorissen M. Allostatic load and stress physiology in European seabass (Dicentrarchus labrax L.) and gilthead seabream (Sparus aurata L.). Front Endocrinol. 2018;9:451.
Sannen A, Van Elsacker L, Heistermann M, Eens M. Urinary testosterone metabolite levels and aggressive behaviors in male and female bonobos (Pan paniscus). Aggress Behav. 2004;30:425–34.
Santymire R, Manjerovic M, Sacerdote-Velat A. A novel method for the measurement of glucocorticoids in dermal secretions of amphibians. Conserv Physiol. 2018;6:coy008.
Sapolsky RM. Stress-induced suppression of testicular function in the wild baboon—role of glucocorticoids. Endocrinology. 1985;116:2273–8.
Sapolsky RM. Individual differences and the stress response. Semin Neurosci. 1994;6:261–9.
Saruta J, Tsukinoki K, Sasaguri K, Ishii H, Yasuda M, Osamura YR, Watanabe Y, Sato S. Expression and localization of chromogranin A gene and protein in human submandibular gland. Cells Tissues Organs. 2005;180:237–44.
Scannapieco FA, Torres G, Levine MJ. Salivary α-amylase: role in dental plaque and caries formation. Crit Rev Oral Biol Med. 1993;4:301–7.
Scarlata CD, Elias BA, Godwin JR, Powell RA, Shepherdson D, Shipley LA, Brown JL. Relationship between fecal hormone concentrations and reproductive success in captive pygmy rabbits (Brachylagus idahoensis). J Mammal. 2012;93:759–70.
Scarlata CD, Elias BA, Godwin JR, Powell RA, Shepherdson D, Shipley LA, Brown JL. Influence of environmental conditions and facility on faecal glucocorticoid concentrations in captive pygmy rabbits (Brachylagus idahoensis). Anim Welf. 2013;22:357–68.
Schaefer SA, Steklis HD. Personality and subjective well-being in captive male western lowland gorillas living in bachelor groups. Am J Primatol. 2014;76:879–89.
Schaftenaar W, Reid C, Martina B, Fickel J, Osterhaus ADME. Nonfatal clinical presentation of elephant endotheliotropic herpes virus discovered in a group of captive Asian elephants (Elephas maximus). J Zoo Wildl Med. 2010;41:626–32.
Scheier MF, Bridges MW. Person variables and health: personality predispositions and acute psychological states as shared determinants for disease. Psychosom Med. 1995;57:255–68.
Schenk HM, Jeronimus BF, van der Krieke L, Bos EH, de Jonge P, Rosmalen JGM. Associations of positive affect and negative affect with allostatic load: a lifelines cohort study. Psychosom Med. 2018;80:160–6.
Schenker JG, Meirow D, Schenker E. Stress and human reproduction. Eur J Obstet Gynecol Reprod Biol. 1992;45:1–8.
Scherer K, Dan E, Flykt A. What determines a feeling’s position in affective space? A case for appraisal. Cognit Emot. 2006;20:92–113.
Schiml PA, Rissman EF. Cortisol facilitates induction of sexual behavior in the female musk shrew (Suncus murinus). Behav Neurosci. 1999;113:166.
Schluessel V. Who would have thought that ‘Jaws’ also has brains? Cognitive functions in elasmobranchs. Anim Cogn. 2015;18:19–37.
Schmid PG, Eckstein JW, Abboud FM. Comparison of effects of deoxycorticosterone and dexamethasone on cardiovascular responses to norepinephrine. J Clin Invest. 1967;46:590–8.
Schoof VAM, Jack KM, Ziegler TE. Male response to female ovulation in white-faced capuchins (Cebus capucinus): variation in fecal testosterone, dihydrotestosterone, and glucocorticoids. Int J Primatol. 2014;35:643–60.
Schreck CB. Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocrinol. 2010;165:549–56.
Schreiber JR, Nakamura K, Erickson GF. Rat ovary glucocorticoid receptor: identification and characterization. Steroids. 1982;39:569–84.
Schultner J, Kitaysky AS, Welcker J, Hatch S. Fat or lean: adjustment of endogenous energy stores to predictable and unpredictable changes in allostatic load. Funct Ecol. 2013;27:45–55.
Schultz R, Isola J, Parvinen M, Honkaniemi J, Wikström A-C, Gustafsson J-Å, Pelto-Huikko M. Localization of the glucocorticoid receptor in testis and accessory sexual organs of male rat. Mol Cell Endocrinol. 1993;95:115–20.
Scott K, Heistermann M, Cant MA, Vitikainen EI. Group size and visitor numbers predict faecal glucocorticoid concentrations in zoo meerkats. R Soc Open Sci. 2017;4:161017.
Seaward BL. Managing stress: principles and strategies for health and well being. 5th ed. Boston: Jones and Bartlett; 2006.
Seeman TE. Social ties and health: the benefits of social integration. Ann Epidemiol. 1996;6:442–51.
Seeman TE, McEwen BS. Impact of social environment characteristics on neuroendocrine regulation. Psychosom Med. 1996;58:459–71.
Seeman TE, Berkman LF, Blazer D, Rowe JW. Social ties and support and neuroendocrine function: the MacArthur studies of successful aging. Ann Behav Med. 1994;16:95–106.
Seeman TE, Singer BH, Rowe JW, Horwitz RI, McEwen BS. Price of adaptation—allostatic load and its health consequences. Arch Intern Med. 1997;157:2259–68.
Seeman TE, McEwen BS, Rowe JW, Singer BH. Allostatic load as a marker of cumulative biological risk: MacArthur studies of successful aging. Proc Natl Acad Sci U S A. 2001;98:4770–5.
Seeman TE, Singer BH, Ryff CD, Love GD, Levy-Storms L. Social relationships, gender, and allostatic load across two age cohorts. Psychosom Med. 2002;64:395–406.
Seeman TE, Crimmins EM, Huang M-H, Singer BH, Bucur A, Gruenewald TL, Berkman LF, Reuben DB. Cumulative biological risk and socio-economic differences in mortality: MacArthur studies of successful aging. Soc Sci Med. 2004a;58:1985–97.
Seeman TE, Glei DA, Goldman N, Weinstein M, Singer BH, Lin Y-H. Social relationships and allostatic load in Taiwanese elderly and near elderly. Soc Sci Med. 2004b;59:2245–57.
Seeman TE, Epel E, Gruenewald TL, Karlamangla AS, McEwen BS. Socio-economic differentials in peripheral biology: cumulative allostatic load. Ann N Y Acad Sci. 2010;1186:223–39.
Seeman M, Merkin SS, Karlamangla A, Koretz B, Teresa S. Social status and biological dysregulation: the “status syndrome” and allostatic load. Soc Sci Med. 2014;118:143–51.
Seplaki CL, Goldman N, Weinstein M, Lin Y-H. How are biomarkers related to physical and mental well-being? J Gerontol A Biol Sci Med Sci. 2004;59A:201–17.
Setchell JM, Smith T, Wickings EJ, Knapp LA. Social correlates of testosterone and ornamentation in male mandrills. Horm Behav. 2008;54:365–72.
Shepherdson DJ. Tracing the path of environmental enrichment in zoos. In: Shepherdson DJ, Mellen JD, Hutchins M, editors. Second nature: environmental enrichment for captive animals. Washington: Smithsonian Institution Press; 1998. p. 1–12.
Shepherdson DJ, Carlstead KC, Wielebnowski N. Cross-institutional assessment of stress responses in zoo animals using longitudinal monitoring of faecal corticoids and behaviour. Anim Welf. 2004;13:S105–S13.
Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R. Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia. 2011;166:869–87.
Shields GS, Lam JCW, Trainor BC, Yonelinas AP. Exposure to acute stress enhances decision-making competence: evidence for the role of DHEA. Psychoneuroendocrinology. 2016;67:51–60.
Shini S, Kaiser P. Effects of stress, mimicked by administration of corticosterone in drinking water, on the expression of chicken cytokine and chemokine genes in lymphocytes. Stress. 2009;12:388–99.
Shini S, Huff GR, Shini A, Kaiser P. Understanding stress-induced immunosuppression: exploration of cytokine and chemokine gene profiles in chicken peripheral leukocytes. Poult Sci. 2010;89:841–51.
Shirotsuki K, Izawa S, Sugaya N, Yamada KC, Ogawa N, Ouchi Y, Nagano Y, Nomura S. Salivary cortisol and DHEA reactivity to psychosocial stress in socially anxious males. Int J Psychophysiol. 2009;72:198–203.
Shively CA, Day SM. Social inequalities in health in nonhuman primates. Neurobiol Stress. 2015;1:156–63.
Shutt K, Heistermann M, Kasim A, Todd A, Kalousova B, Profosouva I, Petrzelkova K, Fuh T, Dicky J-F, Bopalanzognako J-B. Effects of habituation, research and ecotourism on faecal glucocorticoid metabolites in wild western lowland gorillas: implications for conservation management. Biol Conserv. 2014;172:72–9.
Siegel HS. Effects of behavioral and physical stressors on immune responses. In: Wiepkema PR, Van Adrichem PWM, editors. Biology of stress in farm animals: an integrative approach. Dordrecht: Springer; 1987. p. 39–54.
Silk JB, Alberts SC, Altmann J. Social bonds of female baboons enhance infant survival. Science. 2003;302:1231–4.
Silva de Souza Matos L, Palme R, Silva Vasconcellos AÉ. Behavioural and hormonal effects of member replacement in captive groups of blue-fronted amazon parrots (Amazona aestiva). Behav Processes. 2017;138:160–9.
Simpson GM, Fuller G, Lukas KE, Kuhar CW, Fitch-Snyder H, Taylor J, Dennis PM. Sources of morbidity in lorises and pottos in North American zoos: a retrospective review, 1980-2010. Zoo Biol. 2018;37:245–57.
Skandakumar S, Stodulski G, Hau J. Salivary IgA—a possible stress marker in dogs. Anim Welf. 1995;4:339–50.
Smiley T, Spelman L, Lukasik-Braum M, Mukherjee J, Kaufman G, Akiyoshi DE, Cranfield M. Noninvasive saliva collection techniques for free-ranging mountain gorillas and captive eastern gorillas. J Zoo Wildl Med. 2010;41:201–9.
Smith KP, Christakis NA. Social networks and health. Annu Rev Sociol. 2008;34:405–29.
Smith TE, French JA. Psychosocial stress and urinary cortisol excretion in marmoset monkeys (Callithrix kuhli). Physiol Behav. 1997;62:225–32.
Smith AS, Birnie AK, French JA. Social isolation affects partner-directed social behavior and cortisol during pair formation in marmosets, Callithrix geoffroyi. Physiol Behav. 2011;104:955–61.
Smith BK, Remis MJ, Dierenfeld ES. Nutrition of the captive western lowland gorilla (Gorilla gorilla gorilla): a dietary survey. Zoo Biol. 2014;33:419–25.
Snowdon CT. The criteria for successful captive propagation of endangered primates. Zoo Biol. 1989;1:149–61.
Snyder RJ, Perdue BM, Powell DM, Forthman DL, Bloomsmith MA, Maple TL. Behavioral and hormonal consequences of transporting giant pandas from China to the United States. J Appl Anim Welf Sci. 2012;15:1–20.
Snyder-Mackler N, Sanz JÍ, Kohn JN, Brinkworth JF, Morrow S, Shaver AO, Grenier J-C, Pique-Regi R, Johnson ZP, Wilson ME, Barreiro LB, Tung J. Social status alters immune regulation and response to infection in macaques. Science. 2016;354:1041–5.
Sosa C, Forcada F, Meikle A, Abecia J. Increase in ovine plasma cortisol at oestrus and its relation with the metabolic status during the sexual cycle in sheep. Biol Rhythm Res. 2013;44:445–9.
Speeg K Jr, Harrison RW. The ontogony of the human placental glucocorticoid receptor and inducibility of heat-stable alkaline phosphatase. Endocrinology. 1979;104:1364–8.
Spencer KA, Evans NP, Monaghan P. Postnatal stress in birds: a novel model of glucocorticoid programming of the hypothalamic-pituitary-adrenal axis. Endocrinology. 2009;150:1931–4.
Sperry J, Butler L, Romero L, Weatherhead P. Effects of parasitic infection and radio-transmitters on condition, hematological characteristics and corticosterone concentrations in Texas ratsnakes. J Zool. 2009;278:100–7.
Sterling P. Principles of allostasis. In: Schulkin J, editor. Allostasis, homeostasis, and the costs of physiological adaptation. Cambridge: Cambridge University Press; 2004. p. 17–64.
Sterling P. Allostasis: a model of predictive regulation. Physiol Behav. 2012;106:5–15.
Sterling P, Eyer J. Allostasis: a new paradigm to explain arousal pathology. In: Fisher S, Reason J, editors. Handbook of life stress, cognition and health. Chichester: Wiley; 1988. p. 629–49.
Stewart M, Schaefer A, Haley D, Colyn J, Cook N, Stafford K, Webster J. Infrared thermography as a non-invasive method for detecting fear-related responses of cattle to handling procedures. Anim Welf. 2008a;17:387–93.
Stewart M, Stafford K, Dowling S, Schaefer A, Webster J. Eye temperature and heart rate variability of calves disbudded with or without local anaesthetic. Physiol Behav. 2008b;93:789–97.
Støen O-G, 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;152:244–8.
Stoinski TS, Lukas KE, Kuhar CW, Maple TL. Factors influencing the formation and maintenance of all-male gorilla groups in captivity. Zoo Biol. 2004;23:189–203.
Strasser EH, Heath JA. Reproductive failure of a human-tolerant species, the American kestrel, is associated with stress and human disturbance. J Appl Ecol. 2013;50:912–9.
Strong VJ, Grindlay D, Redrobe S, Cobb M, White K. A systematic review of the literature relating to captive great ape morbidity and mortality. J Zoo Wildl Med. 2016;47:697–710.
Strong VJ, Martin M, Redrobe S, White K, Baiker K. A retrospective review of great ape cardiovascular disease epidemiology and pathology. Int Zoo Yearb. 2018;52:113–25.
Sullivan K, van Heugten E, Ange-van Heugten K, Poore MH, Dierenfeld ES, Wolfe B. Analysis of nutrient concentrations in the diet, serum, and urine of giraffe from surveyed North American zoological institutions. Zoo Biol. 2010;29:457–69.
Svec F, Lopez A. Antiglucocorticoid actions of dehydroepiandrosterone and low concentrations in Alzheimer’s disease. Lancet. 1989;334:1335–6.
Svobodova I, Chaloupkova H, Koncel R, Bartos L, Hradecka L, Jebavy L. Cortisol and secretory immunoglobulin A response to stress in German shepherd dogs. PLoS One. 2014;9:e90820.
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;49:963–8.
Takai N, Yamaguchi M, Aragaki T, Eto K, Uchihashi K, Nishikawa Y. Gender-specific differences in salivary biomarker responses to acute psychological stress. Ann N Y Acad Sci. 2007;1098:510–5.
Takatsuji K, Sugimoto Y, Ishizaki S, Ozaki Y, Matsuyama E, Yamaguchi Y. The effects of examination stress on salivary cortisol, immunoglobulin A, and chromogranin A in nursing students. Biomed Res. 2008;29:221–4.
Takeshita RS, Bercovitch FB, Huffman MA, Kinoshita K. Development and validation of an enzyme immunoassay for fecal dehydroepiandrosterone sulfate in Japanese macaques (Macaca fuscata). Int J Primatol. 2018;39:208–21.
Tamashiro KLK, Nguyen MMN, Sakai RR. Social stress: from rodents to primates. Front Neuroendocrinol. 2005;26:27–40.
Tartu S, Gabrielsen GW, Blévin P, Ellis H, Bustnes JO, Herzke D, Chastel O. Endocrine and fitness correlates of long-chain perfluorinated carboxylates exposure in Arctic breeding black-legged kittiwakes. Environ Sci Technol. 2014;48:13504–10.
Taylor SE. Tend and befriend: biobehavioral bases of affiliation under stress. Curr Dir Psychol Sci. 2006;15:273–7.
Taylor J, McFarland MJ, Carr DC. Age, perceptions of mattering, and allostatic load. J Aging Health. 2018:1–20.
Tébar M, Bellido C, Sánchez-Criado JE. Luteinizing hormone (LH) and corticosterone in proestrous afternoon restore the follicle-stimulating hormone secretion at early estrus in adrenalectomized LH-releasing hormone antagonist-treated rats. Biol Reprod. 1995;52:63–7.
Tennessen JB, Parks SE, Langkilde T. Traffic noise causes physiological stress and impairs breeding migration behaviour in frogs. Conserv Physiol. 2014;2:cou032.
Tetsuka M. Actions of glucocorticoid and their regulatory mechanisms in the ovary. Anim Sci J. 2007;78:112–20.
Tetsuka M, Milne M, Simpson GE, Hillier SG. Expression of 11β-hydroxysteroid dehydrogenase, glucocorticoid receptor, and mineralocorticoid receptor genes in rat ovary. Biol Reprod. 1999;60:330–5.
Thatcher HR, Downs CT, Koyama NF. Using parasitic load to measure the effect of anthropogenic disturbance on vervet monkeys. Ecohealth. 2018;15:676–81.
Thayer Z, Barbosa-Leiker C, McDonell M, Nelson L, Buchwald D, Manson S. Early life trauma, post-traumatic stress disorder, and allostatic load in a sample of American Indian adults. Am J Hum Biol. 2017;29:1–10.
Thibier M, Rolland O. The effect of dexamethasone (DXM) on circulating testosterone (T) and luteinizing hormone (LH) in young postpubertal bulls. Theriogenology. 1976;5:53–60.
Thiel D, Jenni-Eiermann S, Braunisch V, Palme R, Jenni L. Ski tourism affects habitat use and evokes a physiological stress response in capercaillie Tetrao urogallus: a new methodological approach. J Appl Ecol. 2008;45:845–53.
Thoma MV, Kirschbaum C, Wolf JM, Rohleder N. Acute stress responses in salivary alpha-amylase predict increases of plasma norepinephrine. Biol Psychol. 2012;91:342–8.
Thompson LA, Spoon TR, Goertz CE, Hobbs RC, Romano TA. Blow collection as a non-invasive method for measuring cortisol in the beluga (Delphinapterus leucas). PLoS One. 2014;9:e114062.
Thompson NA, Higham JP, Heistermann M, Vogel E, Cords M. Energy balance but not competitive environment corresponds with allostatic load during development in an Old World monkey. Horm Behav. 2019;108:30–41.
Tilbrook AJ, Turner AI, Clarke IJ. Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences. Rev Reprod. 2000;5:105–13.
Tilbrook AJ, Turner AI, Clarke IJ. Stress and reproduction: central mechanisms and sex differences in non-rodent species. Stress. 2002;5:83–100.
Tiller WA, McCraty R, Atkinson M. Cardiac coherence: a new, noninvasive measure of autonomic nervous system order. Altern Ther Health Med. 1996;2:52–65.
Toda M, Kusakabe S, Nagasawa S, Kitamura K, Morimoto K. Effect of laughter on salivary endocrinological stress marker chromogranin A. Biomed Res. 2007;28:115–8.
Tokarz RR, Summers CH. Stress and reproduction in reptiles. In: David ON, Kristin HL, editors. Hormones and reproduction of vertebrates. London: Academic Press; 2011. p. 169–213.
Toker S, Shirom A, Shapira I, Berliner S, Melamed S. The association between burnout, depression, anxiety, and inflammation biomarkers: C-reactive protein and fibrinogen in men and women. J Occup Health Psychol. 2005;10:344.
Torner L. Actions of prolactin in the brain: from physiological adaptations to stress and neurogenesis to psychopathology. Front Endocrinol. 2016;7:25.
Touma C, Sachser N, Mostl E, Palme R. Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen Comp Endocrinol. 2003;130:267–78.
Travain T, Colombo ES, Grandi LC, Heinzl E, Pelosi A, Previde EP, Valsecchi P. How good is this food? A study on dogs’ emotional responses to a potentially pleasant event using infrared thermography. Physiol Behav. 2016;159:80–7.
Tress U, Suchodolski JS, Williams DA, Steiner JM. Development of a fecal sample collection strategy for extraction and quantification of fecal immunoglobulin A in dogs. Am J Vet Res. 2006;67:1756–9.
Troïanowski M, Mondy N, Dumet A, Arcanjo C, Lengagne T. Effects of traffic noise on tree frog stress levels, immunity, and color signaling. Conserv Biol. 2017;31:1132–40.
Tsujita S, Morimoto K. Secretory IgA in saliva can be a useful stress marker. Environ Health Prev Med. 1999;4:1–8.
Tung J, Archie EA, Altmann J, Alberts SC. Cumulative early life adversity predicts longevity in wild baboons. Nat Commun. 2016;7:1–7.
Uchino BN. Social support and health: a review of physiological processes potentially underlying links to disease outcomes. Behav Med. 2006;29:377–87.
Uchino BN, Cacioppo JT, Kiecolt-Glaser JK. The relationship between social support and physiological processes: a review with emphasis on underlying mechanisms and implications for health. Psychol Bull. 1996;119:488–531.
Ulrich-Lai YM, Herman JP. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci. 2009;10:397–409.
Upchurch DM, Rainisch BW, Chyu L. Greater leisure time physical activity is associated with lower allostatic load in white, black, and Mexican American midlife women: findings from the national health and nutrition examination survey, 1999 through 2004. Womens Health Issues. 2015a;25:680–7.
Upchurch DM, Stein J, Greendale GA, Chyu L, Tseng C-H, Huang M-H, Lewis TT, Kravitz HM, Seeman TE. A longitudinal investigation of race, socioeconomic status, and psychosocial mediators of allostatic load in midlife women: findings from the study of women’s health across the nation. Psychosom Med. 2015b;77:402–12.
Uphoff Meteyer C, Gonzales BJ, Heuschele WP, Howard EB. Epidemiologic and pathologic aspects of an epizootic of malignant catarrhal fever in exotic hoofstock. J Wildl Dis. 1989;25:280–6.
Uphouse L. Stress and reproduction in mammals. In: David ON, Kristin HL, editors. Hormones and reproduction of vertebrates. London: Academic Press; 2011. p. 117–38.
Valera M, Bartolomé E, Sánchez MJ, Molina A, Cook N, Schaefer A. Changes in eye temperature and stress assessment in horses during show jumping competitions. J Equine Vet Sci. 2012;32:827–30.
Valkanova V, Ebmeier KP, Allan CL. CRP, IL-6 and depression: a systematic review and meta-analysis of longitudinal studies. J Affect Disord. 2013;150:736–44.
van Ree JM, Gerrits MA, Vanderschuren LJ. Opioids, reward and addiction: an encounter of biology, psychology, and medicine. Pharmacol Rev. 1999;51:341–96.
Vidya TNC, Sukumar R. The effect of some ecological factors on the intestinal parasite loads of the Asian elephant (Elephas maximus) in southern India. J Biosci. 2002;27:521–8.
Vigil JM, Geary DC, Granger DA, Flinn MV. Sex differences in salivary cortisol, alpha-amylase, and psychological functioning following Hurricane Katrina. Child Dev. 2010;81:1228–40.
Viijoen JJ, Ganswindt A, du Toit JT, Langbauer WR. Translocation stress and faecal glucocorticoid metabolite levels in free-ranging African savanna elephants. S Afr J Wildl Res. 2008;38:146–52.
Vitazkova SK, Wade SE. Effects of ecology on the gastrointestinal parasites of Alouatta pigra. Int J Primatol. 2007;28:1327–43.
Von Borell E, Langbein J, Després G, Hansen S, Leterrier C, Marchant-Forde J, Marchant-Forde R, Minero M, Mohr E, Prunier A. 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;92:293–316.
von Känel R, Bellingrath S, Kudielka BM. Association between burnout and circulating levels of pro-and anti-inflammatory cytokines in schoolteachers. J Psychosom Res. 2008;65:51–9.
Wade GN, Schneider JE. Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev. 1992;16:235–72.
Walker BG, Boersma PD, Wingfield JC. Field endocrinology and conservation biology. Integr Comp Biol. 2005;45:12–8.
Wallace ME, Harville EW. Allostatic load and birth outcomes among white and black women in New Orleans. Matern Child Health J. 2013;17:1025–9.
Wallace M, Harville E, Theall K, Webber L, Chen W, Berenson G. Neighborhood poverty, allostatic load, and birth outcomes in African American and white women: findings from the Bogalusa Heart Study. Health Place. 2013a;24:260–6.
Wallace M, Harville E, Theall K, Webber L, Chen W, Berenson G. Preconception biomarkers of allostatic load and racial disparities in adverse birth outcomes: the Bogalusa heart study. Paediatr Perinat Epidemiol. 2013b;27:587–97.
Wang F, Riley JCM, Behrman HR. Immunosuppressive levels of glucocorticoid block extrauterine luteolysins in the rat. Biol Reprod. 1993;49:66–73.
Wang X, Byars SG, Stearns SC. Genetic links between post-reproductive lifespan and family size in Framingham. Evol Med Public Health. 2013;2013:241–53.
Waples KA, Gales NJ. Evaluating and minimising social stress in the care of captive bottlenose dolphins (Tursiops aduncus). Zoo Biol. 2002;21:5–26.
Wasserman MD, Chapman CA, Milton K, Goldberg TL, Ziegler TE. Physiological and behavioral effects of capture darting on red colobus monkeys (Procolobus rufomitratus) with a comparison to chimpanzee (Pan troglodytes) predation. Int J Primatol. 2013;34:1020–31.
Watanuki S, Kim Y-K. Physiological responses induced by pleasant stimuli. J Physiol Anthropol Appl Human Sci. 2005;24:135–8.
Watters JV, Powell DM. Measuring animal personality for use in population management in zoos: suggested methods and rationale. Zoo Biol. 2012;31:1–12.
Waylen KA, McGowan PJK, Milner-Gulland EJ, Pawi Study G. Ecotourism positively affects awareness and attitudes but not conservation behaviours: a case study at Grande Riviere, Trinidad. Oryx. 2009;43:343–51.
Webster Marketon JI, Glaser R. Stress hormones and immune function. Cell Immunol. 2008;252:16–26.
Webster JI, Tonelli L, Sternberg EM. Neuroendocrine regulation of immunity. Annu Rev Immunol. 2002;20:125–63.
Webster K, Narayan E, De Vos N. Fecal glucocorticoid metabolite response of captive koalas (Phascolarctos cinereus) to visitor encounters. Gen Comp Endocrinol. 2017;244:157–63.
Weinstein M, Goldman D, Hedley A, Yu-Hsuan L, Seeman TE. Social linkages to biological markers of health among the elderly. J Biosoc Sci. 2003;35:433–53.
Weissenböck NM, Weiss CM, Schwammer HM, Kratochvil H. Thermal windows on the body surface of African elephants (Loxodonta africana) studied by infrared thermography. J Therm Biol. 2010;35:182–8.
Wells SK, Gutter AE, Soike KF, Baskin GB. Encephalomyocarditis virus: epizootic in a zoological collection. J Zoo Wildl Med. 1989;20:291–6.
Wendelaar Bonga SE. The stress response in fish. Physiol Rev. 1997;77:591–625.
West G. Tuberculosis in captive exotic animals. In: Thoen CO, Steele JH, Gilsdorf MJ, editors. Mycobacterium bovis infection in animals and humans. 2nd ed. Ames: Blackwell; 2006. p. 248–57.
Whirledge S, Cidlowski JA. A role for glucocorticoids in stress-impaired reproduction: beyond the hypothalamus and pituitary. Endocrinology. 2013;154:4450–68.
Whitehouse J, Micheletta J, Powell LE, Bordier C, Waller BM. The impact of cognitive testing on the welfare of group housed primates. PLoS One. 2013;8:e78308.
Whitham JC, Wielebnowski N. New directions for zoo animal welfare science. Appl Anim Behav Sci. 2013;147:247–60.
Wielebnowski NC, Fletchall N, Carlstead K, Busso JM, Brown JL. Noninvasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biol. 2002a;21:77–98.
Wielebnowski NC, Ziegler K, Wildt DE, Lukas J, Brown JL. Impact of social management on reproductive, adrenal and behavioral activity in the cheetah (Acinonyx jubatus). Anim Conserv. 2002b;5:291–301.
Wikelski M, Cooke SJ. Conservation physiology. Trends Ecol Evol. 2006;21:38–46.
Wildt DE. Effect of transportation on sexual behavior of cats. Lab Anim Sci. 1980;30:910–2.
Willis SL, Tennstedt SL, Marsiske M, Ball K, Elias J, Koepke KM, Morris JN, Rebok GW, Unverzagt FW, Stoddard AM, Wright E. Long-term effects of cognitive training on everyday functional outcomes in older adults. JAMA. 2006;296:2805–14.
Wilson S, Fell L, Colditz I, Collins D. An examination of some physiological variables for assessing the welfare of beef cattle in feedlots. Anim Welf. 2002;11:305–16.
Wingfield JC, Sapolsky RM. Reproduction and resistance to stress: when and how. J Neuroendocrinol. 2003;15:711–24.
Witeska M. Stress in fish-hematological and immunological effects of heavy metals. Electron J Ichthyol. 2005;1:35–41.
Wittig RM, Crockford C, Weltring A, Deschner T, Zuberbuhler K. Single aggressive interactions increase urinary glucocorticoid levels in wild male chimpanzees. PLoS One. 2015;10:e0118695.
Wojtaszek J, Dziewulska-Szwajkowska D, Łozińska-Gabska M, Adamowicz A, Dżugaj A. Hematological effects of high dose of cortisol on the carp (Cyprinus carpio L.): cortisol effect on the carp blood. Gen Comp Endocrinol. 2002;125:176–83.
Wolf OT. HPA axis and memory. Best Pract Res Clin Endocrinol Metab. 2003;17:287–99.
Wooddell LJ, Hamel AF, Murphy AM, Byers KL, Kaburu SSK, Meyer JS, Suomi SJ, Dettmer AM. Relationships between affiliative social behavior and hair cortisol concentrations in semi-free ranging rhesus monkeys. Psychoneuroendocrinology. 2017;84:109–15.
Woof JM, Kerr MA. IgA function—variations on a theme. Immunology. 2004;113:175–7.
Woolley LA, Millspaugh JJ, Woods RJ, Van Rensburg SJ, Page BR, Slotow R. Intraspecific strategic responses of African elephants to temporal variation in forage quality. J Wildl Manage. 2009;73:827–35.
Yamauchi A, Takei I, Kasuga A, Kitamura Y, Ohashi N, Nakano S, Takayama S, Nakamoto S, Katsukawa F, Saruta T. Depression of dehydroepiandrosterone in Japanese diabetic men—comparison between non-insulin-dependent diabetes mellitus and impaired glucose tolerance. Eur J Endocrinol. 1996;135:101–4.
Yeates JW, Main DC. Assessment of positive welfare: a review. Vet J. 2008;175:293–300.
Yin YJ, Nie CY, Liu WS, Zou Q, Zhai JC, Han HS, Li HP. Non-invasive determination of the immune physiological state of reindeer (Rangifer tarandus) in the Greater Khingan Mountains, China. Genet Mol Res. 2015;14:6664–73.
Yon L, Kanchanapangka S, Chaiyabutr N, Meepan S, Stanczyk FZ, Dahl N, Lasley B. A longitudinal study of LH, gonadal and adrenal steroids in four intact Asian bull elephants (Elephas maximus) and one castrate African bull (Loxodonta africana) during musth and non-musth periods. Gen Comp Endocrinol. 2007a;151:241–5.
Yon L, Kanchanapangka S, Chaiyabutr N, Stanczyk F, Meepan S, Lasley B. ACTH stimulation in four Asian bull elephants (Elephas maximus): an investigation of androgen sources in bull elephants. Gen Comp Endocrinol. 2007b;151:246–51.
Yoshida C, Ishikawa T, Michiue T, Quan L, Maeda H. Postmortem biochemistry and immunohistochemistry of chromogranin A as a stress marker with special regard to fatal hypothermia and hyperthermia. Int J Leg Med. 2011;125:11–20.
Young KM, Walker SL, Lanthier C, Waddell WT, Monfort SL, Brown JL. Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. Gen Comp Endocrinol. 2004;137:148–65.
Zabka T, Goldstein T, Cross C, Mueller R, Kreuder-Johnson C, Gill S, Gulland F. Characterization of a degenerative cardiomyopathy associated with domoic acid toxicity in California sea lions (Zalophus californianus). Vet Pathol. 2009;46:105–19.
Zhang D, Lavaux T, Sapin R, Lavigne T, Castelain V, Aunis D, Metz-Boutigue M-H, Schneider F. Serum concentration of chromogranin A at admission: an early biomarker of severity in critically ill patients. Ann Med. 2009;41:38–44.
Zilioli S, Slatcher RB, Ong AD, Gruenewald TL. Purpose in life predicts allostatic load ten years later. J Psychosom Res. 2015;79:451–7.
Zilioli S, Imami L, Ong AD, Lumley MA, Gruenewald T. Discrimination and anger control as pathways linking socioeconomic disadvantage to allostatic load in midlife. J Psychosom Res. 2017;103:83–90.
Zota AR, Shenassa ED, Morello-Frosch R. Allostatic load amplifies the effect of blood lead levels on elevated blood pressure among middle-aged U.S. adults: a cross-sectional study. Environ Health. 2013;12:1–11.
Zumoff B, Walter L, Rosenfeld RS, Strain JJ, Degen K, Strain GW, Levin J, Fukushima D. Subnormal plasma adrenal androgen levels in men with uremia. J Clin Endocrinol Metab. 1980;51:801–5.
Zwijacz-Kozica T, Selva N, Barja I, Silván G, Martínez-Fernández L, Illera JC, Jodłowski M. Concentration of fecal cortisol metabolites in chamois in relation to tourist pressure in Tatra National Park (South Poland). Acta Theriol. 2013;58:215–22.
Acknowledgments
We thank the technical, veterinary, zoo and research staff who contributed to work described herein. Authors and associated work were funded or supplied with in-kind donations by the AZA Conservation Endowment Fund, Columbus Zoo and Aquarium, Department of Anthropology at The Ohio State University, FBB Capital Partners, Friends of the National Zoo, Institute of Museum and Library Services, International Elephant Foundation, Morris Animal Foundation (D15ZO-403), Siemens Medical Solutions Diagnostics, Shared Earth Foundation, Smithsonian Competitive Grants Program, Smithsonian Institution Fellowship and George E. Burch Fellowship Programs, Smithsonian Women’s Committee, and the Society of Integrative and Comparative Biology.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Edwards, K.L., Edes, A.N., Brown, J.L. (2019). Stress, Well-Being and Reproductive Success. In: Comizzoli, P., Brown, J., Holt, W. (eds) Reproductive Sciences in Animal Conservation. Advances in Experimental Medicine and Biology, vol 1200. Springer, Cham. https://doi.org/10.1007/978-3-030-23633-5_5
Download citation
DOI: https://doi.org/10.1007/978-3-030-23633-5_5
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-23632-8
Online ISBN: 978-3-030-23633-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)