Life history

Prenatal development

Gestation lasts approximately 5.5 months in macaques (rhesus: 146 to 180 days; cynomolgus: 153 to 179 days). Maternal health has a profound influence on infant development. Stress and poor health in pregnant females may lead to permanent developmental and behavioural abnormalities in their offspring.

Infancy

Typically a single infant is born, usually at night. Birth is preceded by behavioural signs, such as touching the vagina, squatting, body shakes, tail wagging and frequent position changing. Labour lasts 1 to 3 hours. The infant begins to suckle at 1 hour. By 2 weeks of age the mother will have begun to introduce solid foods into the diet. At 4 weeks infant weight is around 0.65 kg (rhesus), and by 6 weeks the infant is able to move independently and starts to explore away from the mother. Nutritional weaning begins gradually at 4 months.

Yearlings and juveniles

Nutritional weaning is complete around 12 to 14 months (earlier in captivity). Yearlings weigh around 1 to 1.3 kg. Juveniles usually remain close to their mother until the birth of a sibling (1 to <2 years). Juveniles develop social skills, through sex-specific patterns of play. Their diet now resembles that of adults; both cynomolgus and rhesus macaques are omnivorous frugivores.

Adolescence and sexual maturity

Rhesus macaque females reach sexual maturity at 3 years, and males at 4 years. Cynomolgus macaque females reach sexual maturity at 4 years, and males at 7 years or earlier. Maturity may be reached sooner in captivity. Oestrus is accompanied by reddening of the sexual skin on the rump and face. Peak fertility (ovulation) occurs 11 to 14 days after onset of menstruation in both species regardless of cycle length (26 to 29 days in rhesus; 26 to 38 days in cynomolgus). On reaching sexual maturity, males may become more aggressive and begin exploring away from the natal group.

Adulthood

The breeding season in macaques varies in timing and length between species, locations and over time; breeding seasonality is less pronounced in cynomolgus than rhesus macaques. Macaques mate promiscuously. Females give birth approximately every 1 to 2 years, from 3 to 20 years of age. Higher-ranked females reproduce more often, from an earlier age, and have higher infant survival rates.

Senescence

The median lifespan of macaques in the wild is less than 15 years (<5% reach 25 years). In captivity, macaques can live for over 25 years (maximum recorded is 40 years). Females over 25 years of age experience menopause. Geriatric illnesses are rarely seen in wild populations, but geriatric captive macaques exhibit illnesses such as arthritis, atherosclerosis, cataracts, gum disease, cancer, diabetes and obesity. Low ranking macaques are at higher risk of chronic psychosocial stress, leading to more health problems in old age.

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Life history timeline

Prenatal development | Infancy |Yearlings and juveniles |Adolescence and sexual maturity | Adulthood |Senescence

 

Prenatal development

  • Gestation – Gestation lasts approximately 5.5 months in macaques (rhesus: 146 – 180 days; cynomolgus: 153 – 179 days).1
  • Maternal health –  Maternal health has a profound influence on infant development. Stress and poor health in pregnant females may lead to permanent developmental and behavioural abnormalities in their offspring.2

Infancy

  • Birth – Typically a single infant is born, usually at night.3 Infant weight at birth is 0.4 – 0.55 kg (rhesus) 0.33 – 0.35 kg (cynomolgus).4
  • 1 hour – Infant begins to suckle.
  • 2 weeks – Mother begins introducing solid foods into the diet.5
  • 4 weeks – Infant weight is ~0.65 kg (rhesus).
  • 6 weeks – Infant is able to move independently and starts to explore away from the mother.
  • 1 to 3.5 months – Milk composition is 4.6% fat, 1.8% protein and 7.6% sugar.6 Breast milk contains a higher energy density for male infants than for female infants.7
  • 4 months – Nutritional weaning begins gradually.8
  • 5 months – Infant weight is ~1 kg.9

Images: Alexander Georgiev. Click to enlarge the image.

Rhesus macaque infant sucklingRhesus macaque infant exploringRhesus macaque infant playing with a leafRhesus macaque infant carried on mother's backInfant rhesus macaques playing

 

Male infant care from NC3Rs on Vimeo. In this video, an adult male rhesus macaque protects a young infant.

 

Yearlings and juvenilesRhesus macaque mother with juvenile

  • 12 months – Yearlings weigh ~1.3 kg.10
  • 12-14 months – Nutritional weaning is complete.11 In captivity, nutritional weaning can occur as early as 8 months of age in cynomolgus macaques.
  • Artificial weaning (permanent separation of infants from their mothers) should not occur before 10-14 months of age.12 Infants separated early from the mother show development abnormalities, including impaired cognition, altered physiology, disrupted endocrine response to stress, behavioural abnormalities and inability to function in a social group.13 These effects can be life-long and impact negatively on the suitability of such animals as research models.
  • 18 months – Juveniles usually remain close to their mother until the birth of a sibling ~1 – <2 years14 Juveniles develop social skills, through sex-specific patterns of play. Their diet now resembles that of adults. Both cynomolgus and rhesus macaques are omnivorous frugivores, with dietary composition varying greatly with location and season.

Weaning tantrum from NC3Rs on Vimeo. In this video, the infant on the left tries to suckle from its mother, but is rejected. (Video: MRC Centre for Macaques)

Auntying from NC3Rs on Vimeo. In this video, a yearling carries its infant sibling, which cries and is then taken by their mother. (Video: MRC Centre for Macaques)

Juveniles playing from NC3Rs on Vimeo. In this video, juvenile cynomolgus macaques are seen playing on the forest floor.

 

Adolescence and sexual maturity

  • 3 years – Rhesus macaque females reach sexual maturity.15 Maturity may be reached sooner in captivity.16
  • 4 years – Rhesus macaque males and cynomolgus macaque females reach sexual maturity.17
  • 7 years – Cynomolgus macaque males reach sexual maturity; can be earlier in some captive colonies18
  • Sexual maturity – Increases in sex hormones influence secondary sexual characteristics and behaviour.19
    • Female oestrous cycle is 26-29 days in rhesus macaques20 26-38 days in cynomolgus macaques21. Accompanied by reddening of the sexual skin on the rump and face. Peak fertility (ovulation) occurs 11-14 days after onset of menstruation in both species regardless of cycle length.22
    • Males may become more aggressive and begin exploring away from the natal group.
    • Females may reproduce from 3-4 years of age. In the wild males are unlikely to sire young until they reach full adult size.23

Adulthood

  • ~8 years – Rhesus macaque males reach full body size.
  • Breeding – Rhesus macaques are seasonal breeders, with births in the wild coinciding with the end of the rainy season, or during the period of highest food abundance24. Breeding season varies in timing and length between locations and over time (e.g. in the mid-1980s, the rhesus macaque mating season on Cayo Santiago lasted from July to December;25 today the mating season runs from January to June, with variation on a year-to-year basis). Breeding seasonality is less pronounced in cynomolgus macaques and varies across their range.26
  • Mating – Macaques mate promiscuously.27 The testes of male macaques increase up to twice their normal size during the breeding season.28
  • Birth – Single young are born approximately every 1-2 years29 from 3 – 20 years of age30. Higher-ranked females reproduce more often, from an earlier age, and have higher infant survival rates31. Birth usually occurs at night, preceded by behavioural signs, such as touching the vagina, squatting, body shakes, tail wagging and frequent position changing. Labour lasts 1 – 3 hours.32

Images: Alexander Georgiev and Michael Gumert. Click image to enlarge.

Rhesus macaque female with cheek pouches visibleRhesus macaques copulatingRhesus macaque female with umbilical cord visibleCynomolgus macaque mount

Senescence

  • Old age – Geriatric illnesses are rarely seen in wild populations, but geriatric captive macaques exhibit illnesses such as arthritis, atherosclerosis, cataracts, gum disease, cancer, diabetes and obesity.33 Low ranking macaques are at higher risk of chronic psychosocial stress, leading to more health problems in old age.34
  • It is important that captive enclosures meet the physical needs of geriatric animals, with lower platforms and easy access to food and resting areas. Softer foods should be supplied to geriatric macaques with gum disease and weakened or missing teeth; failure to eat hard foods, or observation of the animal soaking dry foods in water, may indicate teeth or gum problems.
  • <15 years – Median lifespan in the wild; <5% reach 25 years.35
  • >25 years – Median lifespan in captivity; maximum recorded is 40 years.36 Females >25 years of age go through menopause.37

Geriatric macaque using stairs from NC3Rs on Vimeo. At this cynomolgus macaque breeding facility, wooden stairs have been installed to enable geriatric animals to more easily climb up to the shelving platforms. For more information, see Waitt et al. 2010 Designing environments for aged primates. (Video: BFC)

  1. Wolfensohn & Honess 2005; Primate Products Inc. ↩

  2. Bauman et al. 2014 ↩

  3. Fooden 2000; van Schaik & van Noordwijk 1988 ↩

  4. cynomolgus: Nowak 1991; Wolfensohn & Honess 2005 ↩

  5. Maestripieri & Hoffman 2012 ↩

  6. Hinde et al. 2009 ↩

  7. Hinde et al. 2007 ↩

  8. Fooden 2000; Semple et al. 2009 ↩

  9. Hinde et al. 2009 ↩

  10. Bowman & Lee 1995 ↩

  11. Fooden 2000 ↩

  12. Prescott et al. 2012 ↩

  13. Boyce et al. 1995; Capitanio et al. 2005; Champoux et al. 1989, 2002; Kinnally et al. 2008; Rawashdeh & Dubocovich 2014 ↩

  14. Maestripieri & Hoffman 2012; Fooden 2000 ↩

  15. Rawlins & Kessler 1986; de Jong et al. 1994 ↩

  16. Catchpole & van Wagenen 1975 ↩

  17. Rawlins & Kessler 1986; de Jong et al. 1994 ↩

  18. Rawlins & Kessler 1986; de Jong et al. 1994 ↩

  19. Dixson 1998 ↩

  20. Catchpole & van Wagenen 1975; Kumar et al. 2011 ↩

  21. Nawar & Hafez 1972; Yoshida et al. 1982 ↩

  22. Dobutsu 1982 ↩

  23. Dixson & Nevison 1997 ↩

  24. Lindburg 1971; Wenyuan et al. 1993 ↩

  25. Chapais 1986 ↩

  26. van Noordwijk & van Schaik 1999; Engelhardt et al. 2004 ↩

  27. Lindburg 1971; Du et al. 2010 ↩

  28. Bercovitch 1993; Nowak 1991; Parker 1990 ↩

  29. Fooden 2000; Gomendio 1990; van Schaik & van Noordwijk 1988; de Jong et al. 1994 ↩

  30. Rawlins & Kessler 1986; van Noordwijk & van Schaik 1999 ↩

  31. Gomendio 1990 ↩

  32. Brandt & Mitchell 1973 ↩

  33. Coe et al. 2012; Didier et al. 2012; Pritzker & Kessler 2012 ↩

  34. Maestripieri & Hoffman 2011; Sapolsky 2004 ↩

  35. Johnson & Kapsalis 1995 ↩

  36. Roth et al. 2004; Maestripieri & Hoffman 2011 ↩

  37. Gilardi et al. 1997; Walker 1995 ↩

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