Comparative analysis of mother–infant interactions between free-ranging and captive rhesus macaques in Kathmandu, Nepal

Smriti Shrestha; Shailendra Sharma; Randall C. Kyes; Laxman Khanal

doi:10.31893/jabb.2024011

Keywords:

Mother-infant interactions

Abstract

Rhesus macaques (Macaca mulatta) are gregarious, social primates whose infants depend on maternal support for survival. This study aimed to compare mother–infant interactions between free-ranging rhesus macaques (Swayambhunath Temple) and those in a captive setting (Central Zoo, Lalitpur) in Kathmandu, Nepal. Interactions such as duration of proximity and duration of contact between the dyads and symmetry, duration of out-of-proximity, duration of carrying or leaving by the mother while moving, and duration of nipple contact were compared. Five-minute focal animal sampling of maternal macaques was used to record the duration of mother–infant interactions. The behavioral state of the mother was also recorded via instantaneous scan sampling at one-minute intervals during focal samples. Our results revealed that the durations of proximity and contact were greater in the free-ranging macaques than in the zoo macaques. Similarly, the duration of carrying or leaving by the mother while moving was also greater in the free-ranging condition. The free-ranging mother–infant dyads spent significantly more time in nipple contact than did those in the captive setting. The infants were found to be primarily responsible for initiating both contact and proximity in the captivity. The symmetry for contact was balanced in free-ranging macaques; however, the infants were more responsible than the mothers for proximity behavior.
References
1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49(3-4):227–266.
2. Bardi M, Bode AE, Ramirez SM, Brent LY (2005) Maternal care and development of stress responses in baboons. American Journal of Primatology 66(3):263–278.
3. Bardi M, Huffman MA (2002) Effects of maternal style on infant behavior in Japanese macaques (Macaca fuscata). Developmental Psychobiology 41(4):364–372. https://doi.org/10.1002/dev.10065.
4. Bardi M, Shimizu K, Barrett GM, Borgognini-Tarli SM, Huffman MA (2003) Peripartum sex steroid changes and maternal style in rhesus and Japanese macaques. General and Comparative Endocrinology 133(3):323–331. https://doi.org/10.1016/s0016-6480(03)00193-x.
5. Bashaw MJ, Tarou LR, Maki TS, Maple TL (2001) A survey assessment of variables related to stereotypy in captive giraffe and okapi. Applied Animal Behaviour Science 73(3):235–247.
6. Bellanca RU, Crockett CM (2002) Factors predicting increased incidence of abnormal behavior in male pigtailed macaques. American Journal of Primatology 58(2):57–69.
7. Berman CM (1980) Early agonistic experience and rank acquisition among free-ranging infant rhesus monkeys. International Journal of Primatology 1:153–170.
8. Berman CM (1980) Mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago: a comparison with captive pairs. Animal Behaviour 28(3):860–873.
9. Boere V (2001) Environmental enrichment for neotropical primates in captivity. Ciência Rural 31:543–551.
10. Brockerhoff EG, Barbaro L, Castagneyrol B, Forrester DI, Gardiner B, González-Olabarria JR, et al (2017). Forest biodiversity, ecosystem functioning and the provision of ecosystem services. Biodiversity and Conservation 26(13):3005–3035. https://doi.org/10.1007/s10531-017-1453-2.
11. Castell R, Wilson C (1971) Influence of spatial environment on development of mother-infant interaction in pigtail monkeys. Behaviour 39(2-4):202–211.
12. Castellano‐Navarro A, Beltrán Francés V, Albiach‐Serrano A, MacIntosh AJJ, Illa Maulany R, Ngakan PO, et al (2022). Maternal and offspring behavior in free‐ranging Japanese and moor macaques: A comparative approach. American Journal of Primatology 85(2):23461. https://doi.org/10.1002/ajp.23461.
13. Chalise MK (2013) Fragmented primate population of Nepal. In Marsh LK, Chapman CA, eds. Primates in fragments: Complexity and resilience. New York: Springer Science+Business Media. Pages 329-356.
14. Clarke AS, Soto A, Bergholz T, Schneider ML (1996) Maternal gestational stress alters adaptive and social behavior in adolescent rhesus monkey offspring. Infant Behavior and Development 19(4):451–461.
15. Clayton JB, Al-Ghalith GA, Long HT, Tuan BV, Cabana F, Huang H, et al (2018) Associations between nutrition, gut microbiome, and health in a novel nonhuman primate model. Scientific Reports 8(1):11159.
16. Crates R, Stojanovic D, Heinsohn R (2023) The phenotypic costs of captivity. Biological Reviews 98(2):434–449.
17. de la Torre A, Coyohua Fuentes A, Rangel Negrin A, Velarde Garcez DA, Canales Espinosa D, Cervantes Acosta P, et al (2021) Maternal care according to offspring sex and maternal physical condition in mantled howler monkeys (Alouatta palliata). Primates 62(2):379–388. https://doi.org/10.1007/s10329-020-00883-6.
18. De Lathouwers M, Van Elsacker L (2004) Comparing maternal styles in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). American Journal of Primatology 64(4):411–423. https://doi.org/10.1002/ajp.20089.
19. Dettmer AM, Kaburu SS, Simpson EA, Paukner A, Sclafani V, Byers KL, et al (2016) Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys. Nature Communications 7(1):11940.
20. Dura, E. 2017. Mother-infant interactions in a free-ranging population of pigtail macaques (Macaca nemestrina). MSc thesis, Central Washington University. Pages: 46.
21. Fairbanks L (1988) Mother-infant behavior in vervet monkeys: response to failure of last pregnancy. Behavioral Ecology and Sociobiology 23:157–165.
22. Fairbanks L, McGuire M (1987) Mother-infant relationships in vervet monkeys: response to new adult males. International Journal of Primatology 8:351-366.
23. Fairbanks L, McGuire M (1988). Long‐term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. Developmental Psychobiology: The Journal of the International Society for Developmental Psychobiology 21(7):711–724.
24. Fairbanks LA (1989) Early experience and cross‐generational continuity of mother‐infant contact in vervet monkeys. Developmental Psychobiology: The Journal of the International Society for Developmental Psychobiology 22(7):669–681.
25. Ferrari PF, Paukner A, Ionica C, Suomi SJ (2009) Reciprocal face-to-face communication between rhesus macaque mothers and their newborn infants. Current Biology 19(20):1768–1772. https://doi.org/10.1016/j.cub.2009.08.055.
26. Gouzoules H (1975) Maternal rank and early social interactions of infant stumptail macaques, Macaca arctoides. Primates 16:405–418.
27. Hinde RA, Spencer-Booth Y (1967) The behaviour of socially living rhesus monkeys in their first two and a half years. Animal Behaviour 15(1):169–196.
28. Holley JM, Simpson MJ (1981) A comparison of primiparous and multiparous mother-infant dyads in Macaca mulatta. Primates 22:379–392.
29. Ilham K, Nurdin J, Tsuji Y (2018) Effect of provisioning on the temporal variation in the activity budget of urban long-tailed macaques (Macaca fascicularis) in West Sumatra, Indonesia. Folia Primatologica 89(5):347–356.
30. Jaman MF, Huffman MA (2013) The effect of urban and rural habitats and resource type on activity budgets of commensal rhesus macaques (Macaca mulatta) in Bangladesh. Primates 54(1):49–59. https://doi.org/10.1007/s10329-012-0330-6.
31. Johnson RL, Southwick CH (1984) Structural diversity and mother-infant relations among rhesus monkeys in India and Nepal. Folia Primatologica 43(4):198–215.
32. Kulik L, Langos D, Widdig A (2016) Mothers make a difference: mothers develop weaker bonds with immature sons than daughters. PLoS ONE 11(5):e0154845.
33. Loudon AS, McNeilly AS, Milne JA (1983) Nutrition and lactational control of fertility in red deer. Nature 302(5904):145–147.
34. Maestripieri D (1993) Maternal anxiety in rhesus macaques (Macaca mulatta) II. Emotional bases of individual differences in mothering style. Ethology 95(1):32–42.
35. Maestripieri D (1994) Mother-infant relationships in three species of macaques (Macaca mulatta, M. nemestrina, M. arctoides). I. Development of the mother-infant relationship in the first three months. Behaviour 131(1-2):75–96.
36. Maestripieri D (1998) Social and demographic influences on mothering style in pigtail macaques. Ethology 104(5):379–385.
37. Maestripieri D (2001) Intraspecific variability in parenting styles of rhesus macaques (Macaca mulatta): The role of the social environment. Ethology 107(3):237–248.
38. Maestripieri D (2005) Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proceedings of the National Academy of Sciences 102(27):9726–9729.
39. Maestripieri D (2018) Maternal influences on primate social development. Behavioral Ecology and Sociobiology 72(8):130. https://doi.org/10.1007/s00265-018-2547-x.
40. Maestripieri D, Georgiev AV (2016) What cortisol can tell us about the costs of sociality and reproduction among free-ranging rhesus macaque females on Cayo Santiago. American Journal of Primatology 78(1):92–105. https://doi.org/10.1002/ajp.22368.
41. Maestripieri D, Hoffman CL, Anderson GM, Carter CS, Higley JD (2009) Mother–infant interactions in free-ranging rhesus macaques: Relationships between physiological and behavioural variables. Physiology and Behavior 96(4-5):613–619. https://doi.org/10.1016/j.physbeh.2008.12.016
42. Maestripieri D, Lindell SG, Ayala A, Gold PW, Higley JD (2005) Neurobiological characteristics of rhesus macaque abusive mothers and their relation to social and maternal behavior. Neuroscience and Biobehavioral Reviews 29(1):51–57.
43. McGrew WC (1981) Social and cognitive capabilities of nonhuman primates: lessons from the wild to captivity. International Journal for the Study of Animal Problems 2(3):138–149.
44. McKenzie VJ, Song SJ, Delsuc F, Prest TL, Oliverio AM, Korpita TM, et al (2017) The effects of captivity on the mammalian gut microbiome. Integrative and comparative biology 57(4):690–704.
45. Meehan CL, Mench JA (2007) The challenge of challenge: can problem solving opportunities enhance animal welfare? Applied Animal Behaviour Science 102(3-4):246–261.
46. Morgan KN, Tromborg CT (2007) Sources of stress in captivity. Applied Animal Behaviour Science 102(3-4):262–302.
47. Newberry RC (1993) The space-time continuum, and its relevance to farm animals. Etologia 3:219–234.
48. NTNC (2021) Annual Report 2021. National Trust for Nature Conservation, Kathmandu, Nepal. Pp.
49. Power ML, Verona CE, Ruiz-Miranda C, Oftedal OT (2008) The composition of milk from free-living common marmosets (Callithrix jacchus) in Brazil. American Journal of Primatology 70(1):78–83. https://doi.org/10.1002/ajp.20459.
50. Raper J, Bush A, Murphy KL, Baxter MG, Alvarado MC (2016) Multiple sevoflurane exposures in infant monkeys do not impact the mother-infant bond. Neurotoxicology and teratology 54:46–51.
51. Rosenblum LA, Paully GS 1984. The effects of varying environmental demands on maternal and infant behavior. Child Development 55(1):305–314. https://doi.org/10.1111/j.1467-8624.1984.tb00293.x
52. Saj T, Sicotte P, Paterson, JD (1999) Influence of human food consumption on the time budget of vervets. International Journal of Primatology 20:977–994.
53. Schwitzer C, Kaumanns W (2003) Foraging patterns of free-ranging and captive primates-implications for captive feeding regimes. Zoo Animal Nutrition 2:247–265.
54. Semple S, Gerald MS, Suggs DN (2009) Bystanders affect the outcome of mother-infant interactions in rhesus macaques. Proceeding of the Royal Society Biological Science 276(1665):2257–2262. https://doi.org/10.1098/rspb.2009.0103.
55. Serres A, Hao Y, Wang D (2020) Body contacts and social interactions in captive odontocetes are influenced by the context: An implication for welfare assessment. Animals 10(6):924.
56. Sha JCM, Ismail R, Marlena D, Lee, JL (2016) Environmental complexity and feeding enrichment can mitigate effects of space constraints in captive callitrichids. Laboratory animals 50(2):137–144.
57. Sharma S, Khanal L, Shrestha S, Pandey N, Bellanca RU, Kyes RC (2023) Zoo visitors as a source of enrichment to reduce abnormal behavior in captive rhesus macaques (Macaca mulatta) in the Central Zoo, Kathmandu, Nepal. Journal of Animal Behaviour and Biometeorology 11(1):e2023005.
58. Sharma S, Shrestha S, Khanal L (2023) Motor Stereotypic Behaviors in Zoo Rhesus Monkeys: a Case Study of the Central Zoo, Kathmandu, Nepal. Zoodiversity 57(3):239–250. https://doi.org/10.15407/zoo2023.03.239.
59. Sharma S, Shrestha S, Pandey N, Khanal L (2022) Determinants of grooming behavior in cvaptive langurs under human disturbance: A case study from the Central Zoo, Kathmandu, Nepal. Punjab University Journal of Zoology 37(2):98–105.
60. Shrestha K, Poudyal PP, Shrestha D, Shrestha P, Khanal B, Shakya S, et al (2006) Swayambhu Environmental Education. Center for Environmental and Educational Development, Nepal, Swayambhu, Kathmandu. p 295.
61. Silk J, Cheney D, Seyfarth R (2013) A practical guide to the study of social relationships. Evol Anthropol 22(5):213–225. https://doi.org/10.1002/evan.21367.
62. Suomi SJ (2005) Aggression and social behaviour in rhesus monkeys. In Bock G, Goodie J (Eds) Novartis Foundation Symposia. https://doi.org/10.1002/0470010703.ch15.
63. Suomi SJ (2005) Mother-infant attachment, peer relationships, and the development of social networks in rhesus monkeys. Human Development 48(1-2):67–79. https://doi.org/10.1159/000083216.
64. Suomi SJ (2007) Early stress and adult emotional reactivity in rhesus monkeys. Ciba Foundation Symposium 156‐The Childhood Environment and Adult Disease: The Childhood Environment and Adult Disease: Ciba Foundation Symposium 156, Wiley Online Library.
65. Tanaka I (1989) Variability in the development of mother-infant relationships among free-ranging Japanese macaques. Primates 30:477–491.
66. Wolfheim JH, Jensen GD, Bobbitt RA (1970) Effects of group environment on the mother-infant relationship in pigtailed monkeys (Macaca nemestrina). Primates 11(2):119–124.
67. Zhao Q, Tan CL, Pan W (2008) Weaning Age, Infant Care, and Behavioral Development in Trachypithecus leucocephalus. International Journal of Primatology 29(3):583–591. https://doi.org/10.1007/s10764-008-9255-8.

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

How to cite

Shrestha, S., Sharma, S., Kyes, R. C., & Khanal, L. (2024). Comparative analysis of mother–infant interactions between free-ranging and captive rhesus macaques in Kathmandu, Nepal. Journal of Animal Behaviour and Biometeorology, 12(2), 2024011. https://doi.org/10.31893/jabb.2024011

[1] Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49(3-4):227–266.

[2] Bardi M, Bode AE, Ramirez SM, Brent LY (2005) Maternal care and development of stress responses in baboons. American Journal of Primatology 66(3):263–278.

[3] Bardi M, Huffman MA (2002) Effects of maternal style on infant behavior in Japanese macaques (Macaca fuscata). Developmental Psychobiology 41(4):364–372. https://doi.org/10.1002/dev.10065.

[4] Bardi M, Shimizu K, Barrett GM, Borgognini-Tarli SM, Huffman MA (2003) Peripartum sex steroid changes and maternal style in rhesus and Japanese macaques. General and Comparative Endocrinology 133(3):323–331. https://doi.org/10.1016/s0016-6480(03)00193-x.

[5] Bashaw MJ, Tarou LR, Maki TS, Maple TL (2001) A survey assessment of variables related to stereotypy in captive giraffe and okapi. Applied Animal Behaviour Science 73(3):235–247.

[6] Bellanca RU, Crockett CM (2002) Factors predicting increased incidence of abnormal behavior in male pigtailed macaques. American Journal of Primatology 58(2):57–69.

[7] Berman CM (1980) Early agonistic experience and rank acquisition among free-ranging infant rhesus monkeys. International Journal of Primatology 1:153–170.

[8] Berman CM (1980) Mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago: a comparison with captive pairs. Animal Behaviour 28(3):860–873.

[9] Boere V (2001) Environmental enrichment for neotropical primates in captivity. Ciência Rural 31:543–551.

[10] Brockerhoff EG, Barbaro L, Castagneyrol B, Forrester DI, Gardiner B, González-Olabarria JR, et al (2017). Forest biodiversity, ecosystem functioning and the provision of ecosystem services. Biodiversity and Conservation 26(13):3005–3035. https://doi.org/10.1007/s10531-017-1453-2.

[11] Castell R, Wilson C (1971) Influence of spatial environment on development of mother-infant interaction in pigtail monkeys. Behaviour 39(2-4):202–211.

[12] Castellano‐Navarro A, Beltrán Francés V, Albiach‐Serrano A, MacIntosh AJJ, Illa Maulany R, Ngakan PO, et al (2022). Maternal and offspring behavior in free‐ranging Japanese and moor macaques: A comparative approach. American Journal of Primatology 85(2):23461. https://doi.org/10.1002/ajp.23461.

[13] Chalise MK (2013) Fragmented primate population of Nepal. In Marsh LK, Chapman CA, eds. Primates in fragments: Complexity and resilience. New York: Springer Science+Business Media. Pages 329-356.

[14] Clarke AS, Soto A, Bergholz T, Schneider ML (1996) Maternal gestational stress alters adaptive and social behavior in adolescent rhesus monkey offspring. Infant Behavior and Development 19(4):451–461.

[15] Clayton JB, Al-Ghalith GA, Long HT, Tuan BV, Cabana F, Huang H, et al (2018) Associations between nutrition, gut microbiome, and health in a novel nonhuman primate model. Scientific Reports 8(1):11159.

[16] Crates R, Stojanovic D, Heinsohn R (2023) The phenotypic costs of captivity. Biological Reviews 98(2):434–449.

[17] de la Torre A, Coyohua Fuentes A, Rangel Negrin A, Velarde Garcez DA, Canales Espinosa D, Cervantes Acosta P, et al (2021) Maternal care according to offspring sex and maternal physical condition in mantled howler monkeys (Alouatta palliata). Primates 62(2):379–388. https://doi.org/10.1007/s10329-020-00883-6.

[18] De Lathouwers M, Van Elsacker L (2004) Comparing maternal styles in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). American Journal of Primatology 64(4):411–423. https://doi.org/10.1002/ajp.20089.

[19] Dettmer AM, Kaburu SS, Simpson EA, Paukner A, Sclafani V, Byers KL, et al (2016) Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys. Nature Communications 7(1):11940.

[20] Dura, E. 2017. Mother-infant interactions in a free-ranging population of pigtail macaques (Macaca nemestrina). MSc thesis, Central Washington University. Pages: 46.

[21] Fairbanks L (1988) Mother-infant behavior in vervet monkeys: response to failure of last pregnancy. Behavioral Ecology and Sociobiology 23:157–165.

[22] Fairbanks L, McGuire M (1987) Mother-infant relationships in vervet monkeys: response to new adult males. International Journal of Primatology 8:351-366.

[23] Fairbanks L, McGuire M (1988). Long‐term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. Developmental Psychobiology: The Journal of the International Society for Developmental Psychobiology 21(7):711–724.

[24] Fairbanks LA (1989) Early experience and cross‐generational continuity of mother‐infant contact in vervet monkeys. Developmental Psychobiology: The Journal of the International Society for Developmental Psychobiology 22(7):669–681.

[25] Ferrari PF, Paukner A, Ionica C, Suomi SJ (2009) Reciprocal face-to-face communication between rhesus macaque mothers and their newborn infants. Current Biology 19(20):1768–1772. https://doi.org/10.1016/j.cub.2009.08.055.

[26] Gouzoules H (1975) Maternal rank and early social interactions of infant stumptail macaques, Macaca arctoides. Primates 16:405–418.

[27] Hinde RA, Spencer-Booth Y (1967) The behaviour of socially living rhesus monkeys in their first two and a half years. Animal Behaviour 15(1):169–196.

[28] Holley JM, Simpson MJ (1981) A comparison of primiparous and multiparous mother-infant dyads in Macaca mulatta. Primates 22:379–392.

[29] Ilham K, Nurdin J, Tsuji Y (2018) Effect of provisioning on the temporal variation in the activity budget of urban long-tailed macaques (Macaca fascicularis) in West Sumatra, Indonesia. Folia Primatologica 89(5):347–356.

[30] Jaman MF, Huffman MA (2013) The effect of urban and rural habitats and resource type on activity budgets of commensal rhesus macaques (Macaca mulatta) in Bangladesh. Primates 54(1):49–59. https://doi.org/10.1007/s10329-012-0330-6.

[31] Johnson RL, Southwick CH (1984) Structural diversity and mother-infant relations among rhesus monkeys in India and Nepal. Folia Primatologica 43(4):198–215.

[32] Kulik L, Langos D, Widdig A (2016) Mothers make a difference: mothers develop weaker bonds with immature sons than daughters. PLoS ONE 11(5):e0154845.

[33] Loudon AS, McNeilly AS, Milne JA (1983) Nutrition and lactational control of fertility in red deer. Nature 302(5904):145–147.

[34] Maestripieri D (1993) Maternal anxiety in rhesus macaques (Macaca mulatta) II. Emotional bases of individual differences in mothering style. Ethology 95(1):32–42.

[35] Maestripieri D (1994) Mother-infant relationships in three species of macaques (Macaca mulatta, M. nemestrina, M. arctoides). I. Development of the mother-infant relationship in the first three months. Behaviour 131(1-2):75–96.

[36] Maestripieri D (1998) Social and demographic influences on mothering style in pigtail macaques. Ethology 104(5):379–385.

[37] Maestripieri D (2001) Intraspecific variability in parenting styles of rhesus macaques (Macaca mulatta): The role of the social environment. Ethology 107(3):237–248.

[38] Maestripieri D (2005) Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proceedings of the National Academy of Sciences 102(27):9726–9729.

[39] Maestripieri D (2018) Maternal influences on primate social development. Behavioral Ecology and Sociobiology 72(8):130. https://doi.org/10.1007/s00265-018-2547-x.

[40] Maestripieri D, Georgiev AV (2016) What cortisol can tell us about the costs of sociality and reproduction among free-ranging rhesus macaque females on Cayo Santiago. American Journal of Primatology 78(1):92–105. https://doi.org/10.1002/ajp.22368.

[41] Maestripieri D, Hoffman CL, Anderson GM, Carter CS, Higley JD (2009) Mother–infant interactions in free-ranging rhesus macaques: Relationships between physiological and behavioural variables. Physiology and Behavior 96(4-5):613–619. https://doi.org/10.1016/j.physbeh.2008.12.016

[42] Maestripieri D, Lindell SG, Ayala A, Gold PW, Higley JD (2005) Neurobiological characteristics of rhesus macaque abusive mothers and their relation to social and maternal behavior. Neuroscience and Biobehavioral Reviews 29(1):51–57.

[43] McGrew WC (1981) Social and cognitive capabilities of nonhuman primates: lessons from the wild to captivity. International Journal for the Study of Animal Problems 2(3):138–149.

[44] McKenzie VJ, Song SJ, Delsuc F, Prest TL, Oliverio AM, Korpita TM, et al (2017) The effects of captivity on the mammalian gut microbiome. Integrative and comparative biology 57(4):690–704.

[45] Meehan CL, Mench JA (2007) The challenge of challenge: can problem solving opportunities enhance animal welfare? Applied Animal Behaviour Science 102(3-4):246–261.

[46] Morgan KN, Tromborg CT (2007) Sources of stress in captivity. Applied Animal Behaviour Science 102(3-4):262–302.

[47] Newberry RC (1993) The space-time continuum, and its relevance to farm animals. Etologia 3:219–234.

[48] NTNC (2021) Annual Report 2021. National Trust for Nature Conservation, Kathmandu, Nepal. Pp.

[49] Power ML, Verona CE, Ruiz-Miranda C, Oftedal OT (2008) The composition of milk from free-living common marmosets (Callithrix jacchus) in Brazil. American Journal of Primatology 70(1):78–83. https://doi.org/10.1002/ajp.20459.

[50] Raper J, Bush A, Murphy KL, Baxter MG, Alvarado MC (2016) Multiple sevoflurane exposures in infant monkeys do not impact the mother-infant bond. Neurotoxicology and teratology 54:46–51.

[51] Rosenblum LA, Paully GS 1984. The effects of varying environmental demands on maternal and infant behavior. Child Development 55(1):305–314. https://doi.org/10.1111/j.1467-8624.1984.tb00293.x

[52] Saj T, Sicotte P, Paterson, JD (1999) Influence of human food consumption on the time budget of vervets. International Journal of Primatology 20:977–994.

[53] Schwitzer C, Kaumanns W (2003) Foraging patterns of free-ranging and captive primates-implications for captive feeding regimes. Zoo Animal Nutrition 2:247–265.

[54] Semple S, Gerald MS, Suggs DN (2009) Bystanders affect the outcome of mother-infant interactions in rhesus macaques. Proceeding of the Royal Society Biological Science 276(1665):2257–2262. https://doi.org/10.1098/rspb.2009.0103.

[55] Serres A, Hao Y, Wang D (2020) Body contacts and social interactions in captive odontocetes are influenced by the context: An implication for welfare assessment. Animals 10(6):924.

[56] Sha JCM, Ismail R, Marlena D, Lee, JL (2016) Environmental complexity and feeding enrichment can mitigate effects of space constraints in captive callitrichids. Laboratory animals 50(2):137–144.

[57] Sharma S, Khanal L, Shrestha S, Pandey N, Bellanca RU, Kyes RC (2023) Zoo visitors as a source of enrichment to reduce abnormal behavior in captive rhesus macaques (Macaca mulatta) in the Central Zoo, Kathmandu, Nepal. Journal of Animal Behaviour and Biometeorology 11(1):e2023005.

[58] Sharma S, Shrestha S, Khanal L (2023) Motor Stereotypic Behaviors in Zoo Rhesus Monkeys: a Case Study of the Central Zoo, Kathmandu, Nepal. Zoodiversity 57(3):239–250. https://doi.org/10.15407/zoo2023.03.239.

[59] Sharma S, Shrestha S, Pandey N, Khanal L (2022) Determinants of grooming behavior in cvaptive langurs under human disturbance: A case study from the Central Zoo, Kathmandu, Nepal. Punjab University Journal of Zoology 37(2):98–105.

[60] Shrestha K, Poudyal PP, Shrestha D, Shrestha P, Khanal B, Shakya S, et al (2006) Swayambhu Environmental Education. Center for Environmental and Educational Development, Nepal, Swayambhu, Kathmandu. p 295.

[61] Silk J, Cheney D, Seyfarth R (2013) A practical guide to the study of social relationships. Evol Anthropol 22(5):213–225. https://doi.org/10.1002/evan.21367.

[62] Suomi SJ (2005) Aggression and social behaviour in rhesus monkeys. In Bock G, Goodie J (Eds) Novartis Foundation Symposia. https://doi.org/10.1002/0470010703.ch15.

[63] Suomi SJ (2005) Mother-infant attachment, peer relationships, and the development of social networks in rhesus monkeys. Human Development 48(1-2):67–79. https://doi.org/10.1159/000083216.

[64] Suomi SJ (2007) Early stress and adult emotional reactivity in rhesus monkeys. Ciba Foundation Symposium 156‐The Childhood Environment and Adult Disease: The Childhood Environment and Adult Disease: Ciba Foundation Symposium 156, Wiley Online Library.

[65] Tanaka I (1989) Variability in the development of mother-infant relationships among free-ranging Japanese macaques. Primates 30:477–491.

[66] Wolfheim JH, Jensen GD, Bobbitt RA (1970) Effects of group environment on the mother-infant relationship in pigtailed monkeys (Macaca nemestrina). Primates 11(2):119–124.

[67] Zhao Q, Tan CL, Pan W (2008) Weaning Age, Infant Care, and Behavioral Development in Trachypithecus leucocephalus. International Journal of Primatology 29(3):583–591. https://doi.org/10.1007/s10764-008-9255-8.

Abstract

References

How to cite