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)

Martina Volfová1, Zuzana Machovcová1, Franz Schwarzenberger2, Eva Voslářová1, Iveta Bedáňová1, Vladimír Večerek1

1University of Veterinary and Pharmaceutical Sciences Brno, Faculty of Veterinary Hygiene and Ecology, Department of Animal Protection, Welfare and Behaviour, Brno, Czech Republic
2University of Veterinary Medicine Vienna, Department of Biomedical Sciences, Austria

Received November 19, 2018
Accepted February 12, 2019

References

1. Baker 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. Bashaw 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. Behringer 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. Bray 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. Broom DM 1986: Indicators of poor welfare. Br Vet J 142: 524-526 <https://doi.org/10.1016/0007-1935(86)90109-0>
6. Brundige 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. Campbell 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. Capiro 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. Cavigelli 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. Cavigelli 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. Clark 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. Dembiec 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. Frigerio 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. Gould 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. Goymann 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. Goymann 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. Grandin T 1997: Assessment of stress during handling and transport. J Anim Sci 75: 249-257 <https://doi.org/10.2527/1997.751249x>
19. Hämäläinen 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. Heistermann 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. Honess 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. King 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. Kelley 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. Keller 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. Krief 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. Laws 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. Malikova 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. Mallapur 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. Möstl 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. Palme 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. Palme 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. Palme 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. Pereira 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. Pirovino 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. Pride 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. Rangel-Negrín 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. Sapolsky 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. Shutt 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. Schwarzenberger 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. Starling 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. Takeshita 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. Tarou 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. Terio 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. Touma 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. Touma 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. Weingrill 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. Whitten 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.
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