SEARCH

SEARCH BY CITATION

Keywords:

  • Pan troglodytes;
  • Mahale;
  • parental care;
  • offspring survival;
  • male-philopatric society

ABSTRACT

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED

If a social-living animal has a long life span, permitting different generations to co-exist within a social group, as is the case in many primate species, it can be beneficial for a parent to continue to support its weaned offspring to increase the latter's survival and/or reproductive success. Chimpanzees have an even longer period of dependence on their mothers' milk than do humans, and consequently, offspring younger than 4.5–5 years old cannot survive if the mother dies. Most direct maternal investments, such as maternal transportation of infants and sharing of night shelters (beds or nests), end with nutritional weaning. Thus, it had been assumed that a mother's death was no longer critical to the survival of weaned offspring, in contrast to human children, who continue to depend on parental care long after weaning. However, in theory at least, maternal investment in a chimpanzee son after weaning could be beneficial because in chimpanzees' male-philopatric society, mother and son co-exist for a long time after the offspring's weaning. Using long-term demographic data for a wild chimpanzee population in the Mahale Mountains, Tanzania, we show the first empirical evidence that orphaned chimpanzee sons die younger than expected even if they lose their mothers after weaning. This suggests that long-lasting, but indirect, maternal investment in sons continues several years after weaning and is vital to the survival of the sons. The maternal influence on males in the male-philopatric societies of hominids may be greater than previously believed. Am J Phys Anthropol, 153:139–143, 2014. © 2013 Wiley Periodicals, Inc.

Parental investment (Trivers, 1972) by animals includes metabolic investment in the primary sex cells, nursing, food sharing, protection against predators or group mates, and in the extreme, education in humans. Primate infants, including humans, born in a relatively helpless, altricial state (Nicolson, 1987), and depend on their mothers not only for nutrition but also for transportation, protection, thermoregulation, and hygiene. Although such maternal investment decreases with the growth of the offspring, it continues for long periods, up to several years, in some species.

Chimpanzees (Pan troglodytes), the closest living species to humans, are no exception. Because a chimpanzee infant depends on the mother's milk for even longer than humans do, it is costly for offspring if the mother dies before weaning. Indeed, it has been reported that wild chimpanzee infants cannot survive when they lose their mothers before they are 4.5–5 years old (Teleki et al., 1976; Goodall, 1983).

Usually, such intense and direct care by the mother ends with the offspring's weaning, especially when the mother resumes estrous and gives birth to the next baby. Almost simultaneously with nutritional weaning, chimpanzee offspring cease to sleep at night with the mother in her bed or nest, are no longer carried by their mothers when traveling, and find and eat food on their own.

Such correspondence of behavioral independence and the end of the requirement for maternal milk in nonhuman primates may suggest that only humans have a “childhood” or a period of post-weaning dependence before adulthood (Bogin, 2009). Consequently, it is often assumed that a weaned chimpanzee, unlike a human, can survive even if it loses its mother (Gibbons, 2008). In fact, most weaned chimpanzees did not die with maternal deaths and showed few obvious changes in their health (Goodall, 1986).

Chimpanzees form a male-philopatric unit-group (or community) in which males stay in the natal group and females transfer between groups on maturity (Nishida and Kawanaka, 1972). After an immigrated female gives birth in the new group, she usually stays in the group until death. This means that a son and his mother typically co-exist in the same group until either of them dies, up to a few decades.

In theory, if a mother and her offspring are in the same social group, it may be beneficial for the mother to support her weaned offspring to increase the latter's fitness, despite some costs. For example, in female-philopatric primate societies, such as those of macaques (Macaca spp.), mothers often support their mature daughters to maintain a high dominance rank (Silk, 2009), and because high dominance rank in females is often related to high fertility (Harcourt, 1987), it can be said that maternal support favors the subsequent reproductive success of the daughter. Similarly, in the male-philopatric society of bonobos (Pan paniscus), mother–son relationships last even after maturation of the son, and the presence of the mother strongly affects dominance relationships among adult males (Furuichi, 1989; Ihobe, 1992). It has also been reported that the presence of bonobo mothers increased the mating success of adult sons (Surbeck et al., 2011). Recent studies (Foster et al., 2012; Andres et al., 2013) show that in some nonprimate mammals, namely killer whales (Orcinus orca) and red deer (Cervus elaphus), offspring had reduced survival when they lost their mothers after weaning, suggesting that maternal support is crucial for offspring survival.

In chimpanzees, maternal support for a mature son is less obvious, and only a few anecdotal cases have been reported to date. At Gombe and Taï, one mother each supported her son in the competition for raising rank, and the sons eventually acquired alpha status (Goodall, 1986; Boesch, 2009). Some benefits of living mothers can also be inferred from stress-related behaviors of orphans; a recent report showed that orphaned chimpanzees at Gombe increased anxiety-related behaviors and played less frequently (Botero et al., 2013). However, little research has quantitatively investigated the long-term effects of the presence of mothers on the survival of offspring in wild chimpanzees. We hypothesize that losing a mother, even after weaning, has significant effects on survival of offspring in the longer term, although it may not immediately cause the deaths of orphans. The effects would be expected to be more apparent in male than female offspring in the male-philopatric society of chimpanzees. Thus, we expect sons who are orphaned after weaning to show a lower survival rate until some age when the mother's presence is no longer vital.

METHODS

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED

We analyzed demographic data for the M group of chimpanzees (Nishida et al., 2003 and unpublished data from the Mahale Mountains Chimpanzee Research Project) inhabiting Mahale Mountains National Park, Tanzania (see Nakamura and Nishida, 2012; Nishida, 2012 for more details of the study site). The M group has been studied since 1968, but complete identification of central individuals was achieved only in 1980 (Hiraiwa-Hasegawa et al., 1984). However, because some individuals and most of the males had been identified in earlier research, data from 1972 to 2012 were used for analyses.

We observed 37 male orphans whose mothers died before their offspring reached 16 years old (i.e., before adulthood) (Table 1). Most of the orphans' mothers and the orphans' ages were known, but when an unknown young chimpanzee was identified with no mother, we assumed that the individual had been orphaned at the age estimated when first observed. For example, a male, Charles, was first identified in 1993 at an estimated age of 8 years old, not accompanied by his mother. It is very unlikely that an 8-year-old chimpanzee male immigrated to the M group by himself. Thus, we assumed that he was a son of a peripheral female who was seldom observed by the researchers, and soon after he lost his mother, he appeared in the central area. Thus, in this case, we assumed that Charles was orphaned at 8 years old.

Table 1. List of chimpanzee male orphans at Mahale
NameMotheraYear of birthbAge when orphaned (t or) (years)Lived untilc (years)Lived longer than expectedd
  1. a

    When mother was unknown, the male was assumed to be orphaned at the time of his first observation with estimated age.

  2. b

    “?” denotes estimated year of birth.

  3. c

    “+” indicates that the individual was still alive at the time of analysis (July 2012).

  4. d

    The expected age of death at each age (current age + average life expectancy at that age) was calculated from accumulated known age of death of M group males (n = 96). “Undetermined” denotes the male had not reached the expected age of death and was still alive at the time of analysis.

VandalViola19850.60.6No
SO88Wasobongo19880.90.9No
TonyTomato19861.11.1No
FJ06Fuji20061.21.2No
OP04Opal20041.71.7No
RB07Ruby20072.02.0No
BrahimBetty19912.42.4No
BrutusWakampompo19923.53.5No
ChopinChausiku19855.48.7No
DarwinDar19885.823.7+Yes
AjiUnknown1973?6.023.0Yes
NickNdilo19826.613.1No
KenjiUnknown1970?7.012.0No
HiroUnknown1976?7.015.0No
MumuMomo1979?7.08.0No
OscarOpal19987.97.9No
LukajaUnknown1965?8.026.0Yes
CharlesUnknown1985?8.014.0No
MtwaleMtimpu1975?8.014.0No
MichioMiya19969.816.0+Undetermined
KalundeUnknown1963?10.049.0+Yes
FancyFanta1978?10.013.0No
HitUnknown1972?11.016.0No
HawaziUnknown1960?12.015.0No
NishidaUnknown1960?12.018.0No
KimaroAdija1971?12.014.0No
SinsiFahari1984?12.013.0No
HanbyHappy1980?12.022.0No
ToshiboWasobongo197612.619.2No
MasudiWantendele197712.928.7Yes
NsabaSada197312.923.2No
BonoboWakampompo198114.130.7+Yes
OrionOpal199115.021.1+Undetermined
MusaUnknown1957?15.036.0Yes
DoguraDodoma1981?15.023.0No
JilbaTango1975?15.021.0No
PrimusPinky199115.121.2+Undetermined

In order to examine the consequences of a mother's death on survival of male offspring, we fitted a Cox proportional hazard model (Fox, 2002):

  • display math

where

h(t) = hazard rate at time t (years);

h0(t) = baseline hazard;

x1(t) = 1 if the mother is dead at time t and tor < 5, otherwise 0, tor denotes offspring's age in years when orphaned;

x2(t) = 1 if the mother is dead at time t and 5 ≤ tor < 13, otherwise 0;

x3(t) = 1 if the mother is dead at time t and 13 ≤ tor < 16, otherwise 0.

In addition to 37 orphan males, the survival/death data of 63 nonorphan males were also used in this analysis.

Direct comparisons between the sexes are not possible because Mahale females emigrate to neighboring groups at about 9 years old, at the earliest, and we do not have subsequent data on the survival/death of those who were assumed to have emigrated into groups that are not habituated to humans. Therefore, we investigated instead whether female orphans died before or lived up to 9 years old. A total of 19 females were orphaned before 9 years of age.

RESULTS

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED

Table 1 shows the observed survival/death of male chimpanzees who were orphaned before they became full adults (16 years old) in the Mahale M group. Among 37 orphaned males observed so far, only 7 lived longer than the expected ages of death. On the other hand, 27 males died before the expected age of death. This difference between observed and expected ages of deaths was statistically significant (Wilcoxon matched-pairs signed-rank test, T = 521, P = 0.00014). The significance still held when we excluded 8 males who were less than 5 years old (i.e., before weaning) at the time they lost their mothers and were thus more susceptible to their mothers' deaths (T = 285, P = 0.0056).

Figure 1 shows the probability of survival derived from a Cox proportional hazard model. Males who lost their mothers before their 5th birthdays (tor < 5) had a 4.07-fold increase in mortality risk (P = 0.00038), and those orphaned between 5 and 13 years (5 ≤ tor < 13) had a 2.38-fold increase (P = 0.013). However, those orphaned after their 13th birthday (13 ≤ tor < 16) did not have a significantly increased mortality risk (hazard ratio = 1.15, P = 0.84).

image

Figure 1. Survival curves derived from a Cox proportional hazards model for male chimpanzees orphaned at different ages (tor).

Download figure to PowerPoint

Figure 2 shows the survival/death for male and female orphans. Although all eight of the infant males that were orphaned before weaning died almost immediately upon their mothers' deaths, only about half of infant females died after their mothers' deaths (five lived, six died); this difference between the sexes was significant (Fisher's exact test, P = 0.044). Furthermore, female orphans had a higher survival rate generally: 10 of 14 females who were orphaned after their 3rd birthdays survived up to the age of possible emigration (9 years old). This ratio did not differ from that of females with live mothers, where 39 of 56 survived (Fisher's exact test, P = 1.0).

image

Figure 2. Age classes of orphaned males and females when they lost their mothers and the consequences. Infant: 0 to <5 years old, from birth to weaning. Juvenile: 5 to <9 years old, from weaning to sexual maturity. Early adol.: 9 to <13 years old. Late adol.: 13 to <16 years old. Although expected ages of death at different ages were calculated for males, those of females could not be calculated because females begin to emigrate at 9 years old (in adolescence); thus, survival/death is shown for females up to 9 years old only.

Download figure to PowerPoint

DISCUSSION

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED

Our results suggest that, in the male-philopatric societies of chimpanzees, the existence of living mothers is important for the survival of sons who stay in their natal group. In particular, it should be noted that the loss of a mother decreased the likelihood of survival not only in infants but also in juveniles and early adolescents in the longer term. These juvenile and adolescent males no longer depended on their mothers' milk and had ceased to receive other direct maternal care, such as bed-sharing or transportation. This indicates that males as juveniles and adolescents receive other types of, presumably indirect and relatively infrequent, benefits from living mothers. Similar to the study of red deer (Andres et al., 2013), a mother's presence affects offspring survival even after weaning.

Male chimpanzees do not become full adults until they are 16 years old (Goodall, 1983; Hiraiwa-Hasegawa et al., 1984), and they often follow the mother for several years after weaning (Pusey, 1983; Hayaki, 1988). By doing so, they may be able to gain benefits by feeding in the same food patch with the mother, sometimes getting shares of meat from the mother, and being groomed more by the mother than vice versa (Nishida, 1988). Staying with mothers is also beneficial to the nonadult offspring because they are less likely to be subject to aggression from others than when they are alone (Hiraiwa-Hasegawa and Hasegawa, 1988). There may also be a psychological benefit to being with mothers; it has been reported that some orphaned chimpanzees suffered from a feeling of loss (Goodall, 1983), and following adult males from earlier ages may also cause psychological stress in young chimpanzees. Although male offspring gradually decrease their association with mothers in their juvenile and early adolescent years (Pusey, 1983; Hayaki, 1988), mother–son bonds do not vanish completely. An independent son, when met by his mother, often grooms with her for a long period (Hayaki, 1988). Although not frequent, a mother may also help an adult son at the time of social conflicts with others, and an injured son may stay with his mother until he recovers (Pusey, 1983). Furthermore, some mature males are known to associate frequently with their mothers (Hayaki, 1988). Such possible help of mothers to adult sons may have some similarity with killer whales, whose mothers maintain strong social relations with their adult sons (Foster et al., 2012). However, there is an apparent difference: orphaning did not affect the survival of older chimpanzee sons (13 years or older), whereas killer whale sons faced even higher risk of mortality than did younger sons when they lost their mothers (ibid.). This may be due to different female reproductive strategies in these two species. Killer whale females have the longest postreproductive life span of all nonhuman animals and continue to support their mature sons throughout their lives. On the other hand, chimpanzee females continue to give birth to new offspring until later in their life span (Emery Thompson et al., 2007). Thus, more investigation is needed on the cost of reduced support to mature offspring due to care of unweaned younger offspring.

The benefits from mothers or the cost to weaned chimpanzee males of being orphaned may not be readily observable because young males gradually separate from their mothers through their juvenile years and into adolescence, at least superficially (Hayaki, 1988). However, despite the declining frequency of interactions between mother and son, mothers' help to sons may sometimes be critical even after weaning, which may, in the long-term, affect the survival of even young male chimpanzees, as shown in this study. We could not incorporate individual characteristics of orphans' mothers into our analyses, because such data are only partially available in our data set. However, it is possible that such parameters as mother's dominance rank, her past reproductive profiles, e.g., whether or not she had successfully raised her older children, maternal health before the death, cause of the death, etc. may also have significant effect on the survivorship of the orphan.

Among male-philopatric hominid species, i.e., the Pan-Homo clade, maternal support of sons is well known in bonobos. Our study suggests that maternal support of sons also exists in chimpanzees, although the extent may be different. In humans, maternal support of mature daughters, rather than sons, has been emphasized in the context of the “grandmother hypothesis” (Hawkes et al., 1998). It may be necessary to also consider the possible maternal contribution to mature sons in the course of human evolution.

ACKNOWLEDGMENTS

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED

We thank the Tanzania Commission for Science and Technology, the Tanzania National Parks, the Tanzania Wildlife Research Institute, the Mahale Mountains National Park, and the Mahale Mountains Wildlife Research Centre for permission to do research in Mahale. We thank the late Prof. T. Nishida and other MMCRP members for their cooperation in maintaining the field site. This study complied with all Japanese institutional requirements and Tanzanian regulations regarding the ethical treatment of primate subjects in the field.

LITERATURE CITED

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED
  • Andres D, Clutton-Brock TH, Kruuk LEB, Pemberton JM, Stopher KV, Ruckstuhl KE. 2013. Sex differences in the consequences of maternal loss in a long-lived mammal, the red deer (Cervus elaphus). Behav Ecol Sociobiol 67:12491258.
  • Boesch C. 2009. The real chimpanzee. Cambridge: Cambridge University Press.
  • Bogin B. 2009. Childhood, adolescence, and longevity: a multilevel model of the evolution of reserve capacity in human life history. Am J Hum Biol 21:567577.
  • Botero M, MacDonald SE, Miller RS. 2013. Anxiety-related behavior of orphan chimpanzees (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania. Primates 54:2126.
  • Emery Thompson M, Jones JH, Pusey AE, Brewer-Marsden S, Goodall J, Marsden D, Matsuzawa T, Nishida T, Reynolds V, Sugiyama Y, Wrangham RW. 2007. Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause. Curr Biol 17:21502156.
  • Foster EA, Franks DW, Mazzi S, Darden SK, Balcomb KC, Ford JKB, Croft DP. 2012. Adaptive prolonged postreproductive life span in killer whales. Science 337:1313.
  • Fox J. 2002. Cox proportional-hazards regression for survival data. Appendix to an R and S-PLUS Companion to Applied Regression. California: Sage Publications. Available at: http://cran.r-project.org/doc/contrib/Fox-Companion/appendix-cox-regression.pdf. Accessed on 11 September, 2013.
  • Furuichi T. 1989. Social interactions and the life history of female Pan paniscus in Wamba, Zaire. Int J Primatol 10:173197.
  • Gibbons A. 2008. The birth of childhood. Science 322:10401043.
  • Goodall J. 1983. Population dynamics during a 15 year period in one community of free-living chimpanzees in the Gombe National Park, Tanzania. Z Tierpsychol 61:160.
  • Goodall J. 1986. The chimpanzees of Gombe. Cambridge, MA: Harvard University Press.
  • Harcourt AH. 1987. Dominance and fertility among female primates. J Zool Lond 213:471487.
  • Hawkes K, O'Connell JF, Blurton Jones NG, Alvarez H, Charnov EL. 1998. Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci USA 95:13361339.
  • Hayaki H. 1988. Association partners of young chimpanzees in the Mahale Mountains National Park, Tanzania. Primates 29:147161.
  • Hiraiwa-Hasegawa M, Hasegawa T. 1988. A case of offspring desertion by a female chimpanzee and the behavioral changes of the abandoned offspring. Primates 29:319330.
  • Hiraiwa-Hasegawa M, Hasegawa T, Nishida T. 1984. Demographic study of a large-sized unit-group of chimpanzees in the Mahale Mountains, Tanzania: a preliminary report. Primates 25:401413.
  • Ihobe H. 1992. Male-male relationships among wild bonobos (Pan paniscus) at Wamba, Republic of Zaire. Primates 33:163179.
  • Nakamura M, Nishida T. 2012. Long-term field studies of chimpanzees at Mahale Mountains National Park, Tanzania. In: Kappeler PM, Watts DP, editors. Long-term studies of primates. Heidelberg: Springer. p 339356.
  • Nicolson NA. 1987. Infants, mothers, and other females. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker T, editors. Primate societies. Chicago: University of Chicago Press. p 330342.
  • Nishida T. 1988. Development of social grooming between mother and offspring in wild chimpanzees. Folia Primatol 50:109123.
  • Nishida T. 2012. Chimpanzees of the lakeshore. Cambridge: Cambridge University Press.
  • Nishida T, Corp N, Hamai M, Hasegawa T, Hiraiwa-Hasegawa M, Hosaka K, Hunt KD, Itoh N, Kawanaka K, Matsumoto-Oda A, Mitani JC, Nakamura M, Norikoshi K, Sakamaki T, Turner L, Uehara S, Zamma K. 2003. Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. Am J Primatol 59:99121.
  • Nishida T, Kawanaka K. 1972. Inter-unit-group relationships among wild chimpanzees of the Mahale Mountains. Kyoto Univ Afr Stud 7:131169.
  • Pusey AE. 1983. Mother-offspring relationships in chimpanzees after weaning. Anim Behav 31:363377.
  • Silk JB. 2009. Nepotistic cooperation in non-human primate groups. Philos Trans R Soc London B Biol Sci 364:32433254.
  • Surbeck M, Mundry R, Hohmann G. 2011. Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). Proc R Soc London B Biol Sci 278:590598.
  • Teleki G, Hunt EE Jr, Pfifferling JH. 1976. Demographic observations (1963–1973) on the chimpanzees of Gombe National Park, Tanzania. J Hum Evol 5:559598.
  • Trivers RL. 1972. Parental investment and sexual selection. In: Campbell B, editor. Sexual selection and the descent of man 1871–1971. Chicago: Aldine. p 136179.