Terrestrial predator alarm vocalizations are a valid monitor of stress in captive brown capuchins (Cebus apella)

Zoo Biology

Volumn 18, Issue 4, 1999, Pages 295-312

  Boinski, Sue ^a,b   Gross, Timothy S ^c   Davis, Jerry K ^b  

^a University of Florida ^*  (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c U S GEOLOGICAL SURVEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; AVES; CEBIDAE; CEBUS APELLA; MAMMALIA;

EID: 0033262689     PISSN: 07333188     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2361(1999)18:4<295::AID-ZOO4>3.0.CO;2-5     Document Type: Article

References (75)

1. Alberts SC, Sapolsky RM, Altmann J. 1992. Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Horm Behav 26:167-78.
2. Altmann SA. 1974. Baboons, space, time, and energy. Am Zool 14:221-48.
3. Alvarez F. 1993. Alertness signalling in two rail species. Anim Behav 46:1229-31.
4. Bayart F, Hayashi KT, Faull KF, Barchas J, Levine S. 1990. Influence of maternal proximity on behavioral and physiological responses to separation in infant rhesus monkeys. Behav Neurosci 104:98-107.
5. Bayne KA. 1991. Alternatives to continuous social housing. Lab Anim Sci 41:355-69.
6. Bayne KA, Martin DP. 1998. AAALAC International: using performance standards to evaluate an animal care and use program. Lab Anim 27:32-5.
7. Bergeron RJ, Lin R, McManis JS. 1992. Structural alterations in desferrioxamine compatible with iron clearance in animals. J Med Chem 35:4739-744.
8. Blanchard RJ, Friebel G, Henrie JA, Blanchard DC. 1997. Differentiation of anxiolytic and panicolytic drugs by effects on rat and mouse defense test batteries. Neurosci Biobehav Rev 21:783-9.
9. Blumstein DT, Armitage KB. 1997. Alarm calling in yellow-bellied marmots. 1. The meaning of situationally variable alarm calls. Anim Behav 53:143-71.
10. Boinski S. 1999. Stress responses in primates: proximate mechanisms in the evolution of social organization. In: Foster SA, Endler JA, editors. Geographic variation in behavior: perspectives in evolutionary mechanisms. New York: Oxford University Press. p 95-120.
11. Boinski S. 2000. Social manipulation within and between troops mediates primate group travel. In: Boinski S, Garber PA, editors. On the move: how and why animals travel in groups. Chicago: University of Chicago Press. pp 421-69.
12. Boinski S, Mitchell CL. 1992. The ecological and social factors affecting adult female squirrel monkey vocal behavior. Ethology 92: 316-30.
13. Boinski S, Mitchell CL. 1997. Chuck vocalizations of wild female squirrel monkeys (Saimiri sciureus) contain information on caller identity and foraging activity. Int J Primatol 18: 975-93.
14. Boinski S, Moraes E, Kleiman D, Deitz J, Baker A. 1994a. Infra-group vocal behaviour in wild golden lion tamarins, Leontopithecus rosalia: honest communication of individual activity. Behaviour 130:53-76.
15. Boinski S, Noon C, Stans S, Samudio R, Sammarco P, Hayes A. 1994b. The behavioral profile and environmental enrichment of a squirrel monkey colony: comparisons to wild populations. Lab Primate Newslett 33:1-4.
16. Boinski S, Treves A, Chapman CA. 2000. A critical evaluation of the influence of predators on primates: effects on group travel. In: Boinski S, Garber PA, editors. On the move: how and why animals travel in groups. Chicago: University of Chicago Press. pp 43-72.
17. Boinski S, Swing SP, Gross TP, Davis JK. 1999. Environmental enrichment of brown capuchins (Cebus apella): behavioral and plasma and fecal cortisol measures of effectiveness. Am J Primatol 47:49-68.
18. Brown CH. 1982. Auditory localization and primate vocal behavior. In: Snowdon CT, Brown CH, Peterson MR, editors. Primate communication. New York: Cambridge University Press. p 144-64.
19. Caine NG. 1992. Humans as predators: observational studies and the risk of pseudohabituation. In: Davis H, Balfour D, editors. The inevitable bond: examining scientist-animal interactions. Cambridge: Cambridge University Press. p 357-64.
20. Caine NG, Weldon PJ. 1989. Responses by redbellied tamarins to fecal scents of predatory and non-predatory neotropical mammals. Biotropica 21:186-9.
21. Champoux M, Suomi SJ. 1994. Behavioral and adrenocortical responses of rhesus macaque mothers to infant separation in an unfamiliar environment. Primates 35:191-202.
22. Clarke AS, Boinski S. 1995. Temperament in nonhuman primates. Am J Primatol 37:103-25.
23. Cockram MS, Imlah P, Goddard PJ, Harkiss GD, Waran NK. 1993. The behavioral, endocrine and leukocyte response of ewes to repeated removal of lambs before the age natural weaning. Appl Anim Behav Sci 38:127-42.
24. Cohen J. 1960. A coefficient of agreement for nominal scales. Educ Psych Measure 20:37-46.
25. Committee on the Well-Being of Nonhuman Primates, Institute for Laboratory Animal Research. 1998. The psychological well-being of nonhuman primates. Washington, DC: National Academy Press. 168 p.
26. Cooper BY, Vierck CJ. 1986. Measurement of pain and morphine hypalgesia in monkeys. Pain 26:361-92.
27. Cowlishaw G. 1997. Tradeoffs between foraging and predation risk determine habitat use in a desert population. Anim Behav 53:667-86.
28. Crowell Comuzzie DK. 1993. Baboon vocalizations as a measure of psychological well-being. Lab Primate Newslett 21:5-6.
29. Désautés C, Bidanel JP, Mormede P. 1997. Genetic study of behavioral and pituitary-adrenocortical reactivity in response to an environmental challenge in pigs. Physiol Behav 62:337-45.
30. Emmons LH, Whitney BM, Ross Jr DL. 1997. Sounds of neotropical rainforest mammals: an audio field guide. Ithaca, NY: Cornell Laboratory of Ornithology.
31. Evans CS, Evans L, Marler P. 1993. On the meaning of alarm calls - functional reference in an avian vocal system. Anim Behav 46:23-8.
32. Farabaugh SM, Dooling RJ. 1996. Acoustic communication in parrots: laboratory and field studies of budgerigars, Melopsittacus undulatus. In: Kroodsma DE, Miller EH, editors. Ecology and evolution of acoustic communication in birds. Ithaca, NY: Cornell University Press. p 97-118.
33. Fernandez C, Azkona P. 1994. Human disturbance affects parental care of marsh harriers and nutritional status of nestlings. J Wildlife Manage 57:602-8.
34. Fokkema DS, Smit K, van der Gugten J, Koolhaas JM. 1988. A coherent pattern among social behavior, blood pressure, corticosterone and catecholamine measures in individual male rats. Physiol Behav 42:485-9.
35. Fragaszy DM, Boinski S, Whipple J. 1992. Behavioral sampling in the field: a comparison of focal and group methods. Am J Primatol 26:259-75.
36. Friedman EM, Boinski S, Coe CL. 1995. Interleukin-1 induces sleep-like behavior and alters call structure in juvenile rhesus macaques (Macaca mulatta). Am J Primatol 35:143-55.
37. Goldstein LE, Rasmusson AM, Bunney BS, Roth RH. 1996. Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. J Neurosci 16:4787-98.
38. Goodwin GA, Barr GA. 1997. Evidence for opioid and nonopioid processes mediating adaptive responses on infant rats that are repeatedly isolated. Dev Psychobiol 31:217-27.
39. Grandin T. 1998. The feasibility of using vocalization scoring as an indicator of poor welfare during cattle slaughter. Appl Anim Behav Sci 56:121-8.
40. Greene E, Meagher T. 1998. Red squirrels, Tamiasciureus hudsonicus, produce predator-class specific alarm calls. Anim Behav 55:511-8.
41. Hasson O. 1991. Pursuit-deterrent signals: communication between predator and prey. Trends Ecol Evol 6:325-9.
42. Hennessy MB, Levine S. 1977. Effects of various habituation procedures on pituitary adrenal responsiveness in the mouse. Physiol Behav 18: 799-802.
43. Horn AG, Falls JB. 1996. Categorization and the design of signals: the case of song repertoires. In: Kroodsma DE, Miller EH, editors. Ecology and evolution of acoustic communication in birds. Ithaca, NY: Cornell University Press. p 121-35.
44. Johnstone RA, Grafen A. 1992. The continuous Sir Philip Sidney game: a simple model of biological signalling. J Theor Biol 156:215-34.
45. Kagan J, Reznick JS, Snidman N. 1988. Biological basis of childhood shyness. Science 240:167-71.
46. Krebs JR, Dawkins R. 1984. Animal signals: mind-reading and manipulation. In: Krebs JR, Davies NB, editors. Behavioural ecology: an evolutionary approach. Sunderland, MA: Sinauer Assoc. p 380-402.
47. Krishnamurthy R. 1995. Vocalizations of captive François langurs linked to stereotypy and possible stress. Folia Primatol 63:91-5.
48. Kroodsma DE. 1996. Ecology of passerine song development. In: Kroodsma DE, Miller EH, editors. Ecology and evolution of acoustic communication in birds. Ithaca, NY: Cornell University Press. p 3-19.
49. Laudenslager ML, Boccia ML, Berger CL, Gennaroruggles MM, McFerran B, Reite ML. 1995. Total cortisol, free cortisol, and growth-hormone associated with brief social separation experiences in young macaques. Dev Psychobiol 28:199-211.
50. Lima SL. 1993. Ecological and evolutionary perspectives on escape from predatory attack: a survey of North American birds. Wilson Bull 105:1-47.
51. Levine S, Weiner SG. 1988. Psychoendocrine aspects of mother-infant relationships in non-human primates. Psychoneuroendocrinology 13: 143-54.
52. Marler P, Evans CS. 1996. Bird calls: just emotional displays or something more? Ibis 138: 26-33.
53. Markowitz H. 1982. Behavioral enrichment in the zoo. New York: Van Nostrand and Reinhold.
54. Miczek KA, Weerts EM, Vivian JA, Barros HM. 1995. Aggression, anxiety and vocalizations in animals: GABA(A) and 5-HT anxiolytics. Psychopharmacology 121:38-56.
55. Morton DB, Griffiths PHM. 1985. Guidelines on the recognition of pain, distress and discomfort in experimental animals and an hypothesis for assessment. Vet Reel 16:431-6.
56. Mulligan BE, Baker SC, Murphy MR. 1994. Vocalizations as indicators of emotional state and psychological wellbeing in animals. Anim Welfare Info Center Newslett 5:3-4.
57. Newberry RC. 1995. Environmental enrichment: increasing the biological relevance of captive environments. Appl Anim Behav Sci 44:229-43.
58. Novak MA, Suomi S. 1988. Psychological well-being of primates in captivity. Am Psych 43:765-73.
59. Owren MJ, Bernacki RH. 1998. Applying linear predictive coding (LPC) to frequency-spectrum analysis of animal acoustic signals. In: Hopp SL, Owren MJ, Evans CS, editors. Animal acoustic communication. Berlin: Springer. p129-62.
60. Owren MJ, Rendall D. 1997. An affect-conditioning model of nonhuman primate vocal signalling. In: Owings D et al., editors. Perspectives in ethology, vol. 12. New York: Plenum Press. p 299-346.
61. Randall JM, Matocq MD. 1997. Why do kangaroo rats (Dipodomys spectabilis) footdrum at snakes? Behav Ecol 18:404-13.
62. Ruiz-Miranda CR, Wells SA, Golden R, Seidensticker J. 1998.Vocalizations and other behavioral responses of male cheetahs (Acinonyx jubatus) during experimental separation and reunion trials. Zoo Biol 17:1-16.
63. SchwartzkopfGenswein KS, Stookey JM, Welford R. 1997. Behavior of cattle during hot-iron and freeze branding and the effects on subsequent handling ease. J Anim Sci 75:2064-72.
64. Selye H. 1946. The general adaptation syndrome and the diseases of adaptation. J Clin Endocrinol 6:117-230.
65. Shriner WM. 1998. Yellow-bellied marmot and golden-mantled ground squirrel responses to heterospecific alarm calls. Anim Behav 55: 529-36.
66. Sih A. 1987. Predator and prey lifestyles: an evolutionary and ecological review. In: Kerfoot WC, Sih A, editors. Predation. Hanover: University Press of New England, p 203-224.
67. Snowdon CT. 1994. The significance of naturalistic environments for primate behavioral research. In: Gibbons Jr EF et al., editors. Naturalistic environments for animal behavior research. Albany: State University of New York Press. p 217-35.
68. Thurlow WR. 1971. Audition. In: Kling JW, Riggs LA, editors. Experimental psychology . New York: Holt, Rinehart & Winston. p 223-59.
69. Tilson RL, Norton PM. 1981. Alarm duetting and pursuit deterrence in an African antelope. Am Nat 118:455-62.
70. von Borell E, Ladewig J. 1992. Relationship between behavior and adrenocortical-response pattern in domestic pigs. Appl Anim Behav Sci 34:195-206.
71. Warris PD, Brown SN, Adams SJM. 1994. Relationships between subjective and objective assessments of stress at slaughter and meat quality in pigs. Meat Sci 38:329-430.
72. Weary DM, Ross S, Fraser D. 1997. Vocalizations by isolated piglets: a reliable indicator of piglet need directed towards the sow. Appl Anim Behav Sci 53:249-57.
73. Weary DM, Fraser D. 1995. Signalling need -costly signals and animal-welfare assessment. Appl Anim Behav Sci 44:159-69.
74. White RG, Deshazer JA, Tressler CJ, Borcher GM, Davey S, Waninge A, Parkhurst AM, Milanuk MJ, Clemons ET. 1993. Vocalization and physiological response of pigs during castration with or without a local anesthetic. J Anim Sci 73:381-6.
75. Zuberbuhler K, Noë R, Seyfarth RM. 1997. Diana monkey long-distance calls: messages for conspecifics and predators. Anim Behav 53:589-604.