Acta Vet. Brno 2019, 88: 85-92
https://doi.org/10.2754/avb201988010085
The effects of transport stress on the behaviour and adrenocortical activity of the black-and-white ruffed lemur (Varecia variegata)
References
1. ML, Gemmell RT 1999: Physiological changes in the brushtail possum (Trichosurus vulpecula) following relocation from Armidale to Brisbane, Australia. J Exp Zool 284: 42-49
<https://doi.org/10.1002/(SICI)1097-010X(19990615)284:1<42::AID-JEZ7>3.0.CO;2-3>
2. MJ, Sicks F, Palme R, Schwarzenberger F, Tordiffe ASW, Ganswindt A 2016: Non-invasive assessment of adrenocortical activity as a measure of stress in giraffe (Giraffa camelopardalis). BMC Vet Res 235: 1-13
3. V, Deschner T 2017: Non-invasive monitoring of physiological markers in primates. Horm Behav 91: 3-18
<https://doi.org/10.1016/j.yhbeh.2017.02.001>
4. J, Samson DR, Nunn ChL 2016: Activity patterns in seven captive lemur species: evidence of cathemerality in Varecia and Lemur catta? Am J Primatol 79: 1-9
5. DM 1986: Indicators of poor welfare. Br Vet J 142: 524-526
<https://doi.org/10.1016/0007-1935(86)90109-0>
6. L, Oleas T, Doumit M, Zanella AJ 1998: Loading techniques and their effect on behavioral and physiological responses of market weight pigs. J Anim Sci 76: 99
7. JL, Eisemann JH, Williams CV, Glenn KM 2000: Description of the gastrointestinal tract of five lemur species: Propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variegata, Hapalemur griseus, and Lemur catta. Am J Primatol 52: 133-142
<https://doi.org/10.1002/1098-2345(200011)52:3<133::AID-AJP2>3.0.CO;2-#>
8. JM, Stoops MA, Freeman EW, Clawson D, Schook MW 2014: Effects of management strategies on glucocorticoids and behavior in Indian rhinoceros (Rhinoceros unicornis): Translocation and operant conditioning. Zoo Biol 33: 131-143
<https://doi.org/10.1002/zoo.21119>
9. SA 1999: Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs, Lemur catta. Anim Behav 57: 935-944
<https://doi.org/10.1006/anbe.1998.1054>
10. SA, Dubovick T, Levash W, Jolly A, Pitts A 2003: Female dominance status and fecal corticoids in a cooperative breeder with low reproductive skew: Ring-tailed lemurs (Lemur catta). Horm Behav 43: 166-179
<https://doi.org/10.1016/S0018-506X(02)00031-4>
11. CITES 2017. Appendices I, II and III. Available at: https://cites.org/sites/default/files/eng/app/2017/E-Appendices-2017-10-04.pdf. Accessed March 10, 2018
12. FE, Fitzpatrick M, Hartley A, King AJ, Lee T, Routh A, Walker SL, George K 2011: Relationship between behavior, adrenal activity, and environment in zoo-housed Western lowland gorillas (Gorilla gorilla gorilla). Zoo Biol 30: 1-16
13. DP, Snider RJ, Zanella AJ 2004: The effects of transport stress on tiger physiology and behavior. Zoo Biol 23: 335-346
<https://doi.org/10.1002/zoo.20012>
14. D, Dittami J, Möstl E, Kotrschal K 2004: Excreted corticosterone metabolites co-vary with ambient temperature and air pressure in male greylag geese (Anser anser). Gen Comp Endocrinol 137: 29-36
<https://doi.org/10.1016/j.ygcen.2004.02.013>
15. L, Ziegler TE, Wittwer DJ 2005: Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Nahafaly Reserve, Madagascar. Am J Primatol 67: 5-23
<https://doi.org/10.1002/ajp.20166>
16. W, Möstl E, Van't Hof T, East ML, Hofer H 1999: Noninvasive fecal monitoring of glucocorticoids in spotted hyenas, Crocuta crocuta. Gen Comp Endocrinol 114: 340-348
<https://doi.org/10.1006/gcen.1999.7268>
17. W 2012: On the use of non-invasive hormone research in uncontrolled, natural environments: the problem with sex, diet, metabolic rate and the individual. Methods Ecol Evol 3: 757-765
<https://doi.org/10.1111/j.2041-210X.2012.00203.x>
18. T 1997: Assessment of stress during handling and transport. J Anim Sci 75: 249-257
<https://doi.org/10.2527/1997.751249x>
19. A, Heistermann M, Fenosoa ZSE, Kraus C 2014: Evaluating capture stress in wild gray mouse lemurs via repeated fecal sampling: method validation and the influence of prior experience and handling protocols on stress responses. Gen Comp Endocrinol 195: 68-79
<https://doi.org/10.1016/j.ygcen.2013.10.017>
20. M, Palme R, Ganswindt A 2006: Comparison of different enzymeimmunoassays for assessment of adrenocortical activity in primates based on fecal analysis. Am J Primatol 68: 257-273
<https://doi.org/10.1002/ajp.20222>
21. PE, Marin CM 2006: Enrichment and aggression in primates. Neurosci Biobehav Rev 30: 413-436
<https://doi.org/10.1016/j.neubiorev.2005.05.002>
22. IUCN 2018: Varecia variegata. Available at: http://www.iucnredlist.org/details/22918/0. Accessed March 10, 2018
23. T, Rasolofoharivelo T, Chamberlan C 2013: Conserving the critically endangered black-and white ruffed lemur Varecia variegata through integrating ex situ and in situ efforts. Wild Conservation 1: 25-30
24. EA, Jablonski NG, Chaplin G, Sussman RW, Kamilar JM 2016: Behavioral thermoregulation in Lemur catta: The significance of sunning and huddling behaviors. J Am Primatol 78: 745-754
<https://doi.org/10.1002/ajp.22538>
25. KL, Fritz RS, Zoubek CM, Kennedy EH, Cronin KA, Rothwell ES, Serfass TL 2014: Effects of transport on fecal glucocorticoid levels in captive-bred cotton-top tamarins (Sanguinus oedipus). J Pa Acad Sci 88: 84-88
26. S, Jamart A, Hladik CM 2004: On the possible adaptive value of coprophagy in free-ranging chimpanzees. Primates 45: 141-145
<https://doi.org/10.1007/s10329-003-0074-4>
27. N, Ganswindt A, Heistermann M, Harris M, Harris S, Sherwin C 2007: A case study: Fecal corticosteroid and behavior as indicators of welfare during relocation of an Asian elephant. J Appl Anim Welf Sci 10: 349-358
<https://doi.org/10.1080/10888700701555600>
28. M, Voslarova E, Vecerek V 2018: Non-invasive faecal monitoring of stress in captive and free-ranging wild animals. Berl Münch Tierärztl Wechenschr 131: 150-158
29. A, Choudhury BC 2003: Behavioral abnormalities in captive nonhuman primates. J Appl Anim Welf Sci 6: 275-284
<https://doi.org/10.1207/s15327604jaws0604_2>
30. E, Maggs JL, Schrötter G, Besenfelder U, Palme R 2002: Measurement of cortisol metabolites in faeces of ruminants. Vet Res Commun 26: 127-139
<https://doi.org/10.1023/A:1014095618125>
31. R, Möstl E 1997: Measurement of cortisol metabolites in faeces of sheep as a parameter of cortisol concentration in blood. Z Saugetierkd 62: 192-197
32. R, Robia C, Baumgartner W, Möstl E 2000: Transport stress in cattle as reflected by an increase in faecal cortisol metabolite concentrations. Vet Rec 146: 108-109
<https://doi.org/10.1136/vr.146.4.108>
33. R 2005: Measuring fecal steroids: guidelines for practical application. Ann N Y Acad Sci 1046: 75-80
<https://doi.org/10.1196/annals.1343.007>
34. ME, Seelingson ML, Macedonia JM 1988: The behavioral repertoire of the black-and-white ruffed lemur, Varecia variegata variegata (Primates: Lemuridae). Folia Primatol 51: 1-32
<https://doi.org/10.1159/000156353>
35. M, Heistermann M, Zimmermann N, Zingg R, Clauss M, Codron D, Kaup FJ, Steinmetz HW 2011: Fecal glucocorticoid measurements and their relation to rearing, behavior, and environmental factors in the population of pileated gibbons (Hylobates pileatus) held in European zoos. Int J Primatol 32: 1161-1178
<https://doi.org/10.1007/s10764-011-9532-9>
36. Porton I 1989: International studbook for the ruffed lemur Varecia variegata. St. Louis: St. Louis Zool Park
37. RE 2005: Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta). Behav Ecol 16: 550-560
<https://doi.org/10.1093/beheco/ari025>
38. A, Flores-Escobar E, Chavira R, Canales-Espinosa D, Dias PAD 2014: Physiological and analytical validations of fecal steroid hormone measures in black howler monkeys. Primates 55: 459-465
<https://doi.org/10.1007/s10329-014-0432-4>
39. RM, Romero LM, Munck AU 2000: How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21: 55-89
40. K, Setchell JM, Heistermann M 2012: Non-invasive monitoring of physiological stress in the western lowland gorila (Gorilla gorila gorila): validation of fecal glucocorticoid assay and methods for practical application in the field. Gen Comp Endocrinol 179: 167-177
<https://doi.org/10.1016/j.ygcen.2012.08.008>
41. F and Brown JL 2013: Hormone monitoring: An important tool for the breeding management of wildlife species. Wien Tierarztl Monatsschr 100: 209-225
42. Schwitzer C, King T, Robsomanitrandrasana E, Chamberlan C, Rasolofoharivelo T 2013: Integrating ex situ and in situ conservation of lemurs. In: Schwitzer C et al. (Eds) 2013: Lemurs of Madagascar: A Strategy for their conservation 2013-2016. Bristol, UK: IUCN SSC Primate Specialist Group, Bristol Conservation and Science Foundation, and Conservation International, pp. 146-152
43. AP, Charpentier MJE, Fitzpatrick C, Scordato ES, Drea CHM 2010: Seasonality, sociality, and reproduction: long-term stressors of ring-tailed lemurs (Lemur catta). Horm Behav 57: 76-85
<https://doi.org/10.1016/j.yhbeh.2009.09.016>
44. RSC, Bercovitch FB, Huffman MA, Kinoshita K 2018: Development and validation of an enzyme immunoassay for fecal dehydroepiandrosterone sulfate in Japanese macaques (Macaca fuscata). Int J Primatol 39: 208-221
<https://doi.org/10.1007/s10764-018-0026-x>
45. LR, Bloomsmith MA, Maple TL 2005: Survey of stereotypic behavior in prosimians. Am J Primatol 65: 181-196
<https://doi.org/10.1002/ajp.20107>
46. KA, Citino SB, Brown JL 1999: Fecal cortisol metabolite analysis for noninvasive monitoring of adrenocortical function in the cheetah (Acinonyx jubatus). J Zoo Wildl Med 30: 484-491
47. CH, Palme R, Sachser N 2004: Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Horm Behav 45: 10-22
<https://doi.org/10.1016/j.yhbeh.2003.07.002>
48. CH, Palme R 2005: Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann N Y Acad Sci 1046: 54-74
<https://doi.org/10.1196/annals.1343.006>
49. Vasey N 2006: Impact of seasonality and reproduction on social structure, ranging patterns, and fission-fusion social organization in red ruffed lemurs. In: Gould L, Sauther ML (Eds). Lemurs: ecology and adaptation. New York: Springer. 275-304
50. T, Willems EP, Zimmermann N, Steinmetz H, Heistermann M 2011: Species-specific patterns in fecal glucocorticoid and androgen levels in zoo-living orangutans (Pongo spp.). Gen Comp Endocrinol 172: 446-457
<https://doi.org/10.1016/j.ygcen.2011.04.008>
51. PL, Stavisky R, Aureli F, Russel E 1998: Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes). Am J Primatol 44: 57-69
<https://doi.org/10.1002/(SICI)1098-2345(1998)44:1<57::AID-AJP5>3.0.CO;2-W>
52. Zar JH 1999. Biostatistical Analysis. 4th edn. Prentice-Hall, Inc., New Jersey, 663 p.
