Mothers and Others

by Sarah Blaffer Hrdy

  21. Carter 1998.

  22. Allman 2000:111–112.

  23. Carter, Ahnert, et al. 2005.

  24. Silk 1999; Maestripieri 2001.

  25. Hrdy 1977a, ch. 7.

  26. Hrdy 1999:207–217 and references therein.

  27. Silk, Alberts, and Altmann 2003.

  28. Ahnert, Pinquart, and Lamb 2006:665; this report is consistent with earlier observations by Gunnar and Donahue (1980).

  29. Gunnar and Donahue 1980. For an even stronger statement of this position see Simon Baron-Cohen (2003), who argues that “the female brain is predominantly hard-wired for empathy” (p. 1). For a general review and critical evaluation of the evidence, see Brody 1999, ch. 7.

  30. Radke-Yarrow et al. 1994.

  31. Stallings et al. 2001.

  32. The idea can be traced back to Darwin but has been richly developed by Eibl-Eibesfeldt in his 1989 classic Human Ethology as well as by Babchuk et al. 1985; Taylor 2002. For updates and further empirical demonstrations see Baron-Cohen 2003 and esp. Hampson et al. 2006, who demonstrate that young women are quicker and more accurate at reading facial expressions than young men, controlling for their subjects’ prior theatrical and childcare experience.

  33. For the clearest statement of the mind-reading mums hypothesis see Brockway 2003:95ff.; see also Chisholm 2003; Allman 2000; Panksepp 2000; Preston and de Waal 2002 (esp. their reply to commentaries).

  34. Caro and Hauser 1992; Thornton and McAuliffe 2006.

  35. Boesch and Boesch-Achermann 2000:202. On maternal modeling of nut-cracking, see also Gagneux 1993 and Matsuzawa 2001.

  36. Byrne and Whiten’s edited volume on Machiavellian Intelligence (1988) includes reprints of the classic early papers on this subject by Alison Jolly, Nicholas Humphrey, and David Premack. For some of the most interesting recent nonhuman primate research see Hauser et al. 2003 on identification of reciprocators. See Silk 2003 or Cheney and Seyfarth 2007 on identification and choice of allies.

  37. See esp. Harcourt 1988 on the role of alliance formation in the evolution of social intelligence; quotation appears on p. 144.

  38. De Waal 2006 and references therein.

  39. For a sensible, highly readable overview, see Dunbar 2003.

  40. Byrne and Whiten 1988; Boesch and Boesch-Achermann 1990.

  41. According to one of several alternate explanations for apparent coordination, higher success rates during group hunting might just be an artifact of something else, such as the fact that the chances of capturing prey go up as more males participate in the hunt. See Gilby et al. 2006 for overview; also Mitani et al. 2000.

  42. See Flinn et al. 2005 for an overview of how human “ecological dominance and social competition” shaped the evolution of the human neocortex. To avoid confusion, however, note that in order for humans to achieve ecological domination over other species (a prerequisite of the version of the Machiavellian intelligence hypothesis that Flinn et al. advocate) I assume that early hominins must already have been cooperating at a higher level than is typical of other apes. Thus, Flinn et al.’s ideas about ecological dominance combined with social competition cannot solve the specific problem we are addressing here.

  43. Once again, I am indebted to the observations of the developmental psychologist Andrew Meltzoff (2002). See also Trevarthen 2005 and references to the earlier literature therein. For general introduction to social intelligence, see Goleman (2006).

  44. This includes infanticide by males and by female competitors of the mother as well as intergroup raids. See Goodall 1986; Nishida et al. 1985; Wrangham and Peterson 1996; Watts and Mitani 2000; Pusey, Williams, and Goodall 1997; Townsend et al. 2007.

  45. Papousek et al. 1991.

  46. For the discovery of “mirror neurons,” see Rizzolatti et al. 1996.

  47. Rizzolatti et al. 2006; see also Gallese et al. 2002; Preston and de Waal 2002; Gomez 2004, ch. 9.

  48. Meltzoff and Moore replicated their famous 1977 experiment with much younger babies in 1989. These experiments are reviewed in Meltzoff 2002; quotation appears on p. 11.

  49. Tsao, Freiwald, et al. 2006.

  50. Meltzoff 2002:24; see also Quinn et al. 2002.

  51. Meltzoff 2002:10.

  52. Meltzoff 2002:24; see also Preston and de Waal 2002.

  53. Meltzoff 2002:24.

  54. Holden 2006:25.

  55. Eibl-Eibesfeldt 1989; Emery 2000. I am indebted to Karen Bales (personal communication, January 2008) for pointing out that marmosets and tamarins do not find stares to be aversive.

  56. I have never seen a chimpanzee, gorilla, or bonobo with white sclera in the visible part of the eyes, though the white on the sides is sometimes visible when an ape “rolls” its eyes wide, as I once observed in an orangutan at a zoo in Perth, Australia. However, primatologist Kim Bard informs me that very rarely one encounters a chimpanzee with white sclera (personal communication 2005).

  57. On human responsiveness to fearful eye whites, see Whalen, Kagan, et al. 2004.

  58. This logic, sometimes referred to as the cooperative-eye hypothesis, is beautifully laid out by Tomasello (2007).

  59. See Leavens 2004 and literature cited therein.

  60. Darwin 1874.

  61. For overview of primate parenting, see Bard 2002.

  62. Papousek et al. 1991; Konner 1991.

  63. Quotation from Farroni et al. 2002:9602.

  64. Estimates and quotation from Bard 2002:104.

  65. Bard 2002, esp. page 107; Hobson 2004:268. Bard’s ideas are echoed by cultural anthropologists like Alma Gottlieb (2004:315, n. 31) who stress cross-cultural differences in how long mothers spend looking into their infants’ faces or talking to them.

  66. Bard 2002 and esp. Leavens, Hopkins, and Bard 2008.

  67. Bard et al. 2005.

  68. Matsuzawa 2003, and references therein; also Inoue and Matsuzawa 2007.

  69. Matsuzawa 2006.

  70. Hobson 1989:200.

  71. Farroni et al. 2002.

  72. Hobson (2004:195), for example, reports that the proportion of empathy-deficient children is much higher among children blind from birth than among sighted children.

  73. Whiten and Byrne 1997, and for further discussion Boesch and Boesch-Achermann 1990, 2000; and brief review in Matsuzawa 2003. For a readable introduction to the topic see de Waal 2001.

  74. Tomasello 1999; Gomez 2004:252ff.

  75. Myowa 1996; Myowa-Yamakoshi et al. 2004. Myowa’s results have subsequently been replicated by Bard, who further found that previous experience with human faces was not necessary for facial imitation by chimpanzee neonates (2007).

  76. Tetsuro Matsuzawa, personal communication, 2006; Bard 2007.

  77. Ferrari et al. 2006.

  78. See pioneering work along these lines by Wood, Glynn, Phillips, and Hauser 2007.

  79. Want and Harris 2002.

  80. Jones 2007, quotation on p. 598; Want and Harris 2002.

  81. Hare et al. 2002.

  82. See Dennis 1943, esp. Table 1, for the developmental chronology of Del and Rey, twins reared in social deprivation.

  83. See Cole and Cole’s text on The Development of Children (1993:171) for smiling in a 2.5-month-old blind baby.

  84. Dennis 1943.

  85. From Stern 2002.

  3. WHY IT TAKES A VILLAGE

  1. For an excellent overview of the relevant anatomical research and how recent discoveries of the FOXP2 gene help date the origins of language, see Lieberman 2007. For the (still controversial) argument about click languages, see Knight et al. 2003.

  2. See Leavens 2006, and literature cited therein; refer back to Chapter 2.

  3. See Eibl-Eibesfeldt 1971 for classic ethological account of maternal bonds as roots of “love.”

  4. On this occasion the old female Flo allowed her daughter Fifi to take baby Flint (Goodall 1969:388).

  5. Van Noordwijk and van Schaik 2005. According to Fossey (1979), gorillas fall in the same range, though there are a few reports
of transfers after just a few months.

  6. Primate taxonomies are in constant flux. Since I was a graduate student, the commonly accepted number of living primates has risen from 175 species to 276, the number I use in this book. This does not mean that many new species were actually discovered. The principal reason for the increase is that existing classifications are continuously being rearranged and split apart in an effort to better characterize the genetic, morphological, and ecological diversity within the order Primates and to more accurately reflect their phylogenetic relationships. Species names are constantly changing as well as being added. To keep abreast of such changes, I relied on the 1996 edition of Noel Rowe’s The Pictorial Guide to the Living Primates, a favorite among primate behaviorists and conservationists. Rowe includes capsule summaries of the distribution and natural history of each species next to vivid color photos, and it makes a handy reading companion. The forthcoming edition of Rowe’s book will list closer to 400 species. An up-to-date taxonomy will eventually be available at a website located at www.alltheworldsprimates.com.

  7. For anxiety in pregnant mice approaching term, see D’Amato, Rizzi, and Moles 2006. For birth in wild orangutans, see Galdikas 1982.

  8. Van Schaik 2004:102.

  9. Quotation from Schaller 1972:54; Hrdy 1999:177ff.

  10. See Turner et al. 2005 and references therein.

  11. Sarah Turner writing from the Awajishima Monkey Center, personal communication 2007.

  12. For up-to-date authoritative overview by one of the pioneers in the field, see Fleming and Gonzalez 2009; Gray and Ellison 2009 and references therein.

  13. Elsewhere (Hrdy 1999, chs. 12 and 14) I examine in some depth the historical and cross-cultural evidence for infant abandonment as well as criteria (sex, viability, local conditions) that enter into such painful decisions.

  14. Varki and Altheide 2005.

  15. Reed et al. 2007.

  16. For example, Bugos and McCarthy 1984.

  17. Howell 1979; Schiefenhövel 1989; reviewed in Hrdy 1992, Table 1ff.

  18. The foundations for this argument are laid out in Hrdy 1999, esp. chs. 9–14.

  19. See Leckman et al. 1999, 2005 for studies with primarily Western mothers.

  20. See Hill and Hurtado 1989 for intergroup variation in hunter-gatherer lifestyles. See Small 1998 or Konner 2005 for more on indulgence toward infants.

  21. Konner 1972; 1976:306; Lee 1979:310.

  22. See Hewlett, Lamb, et al. 1998 for comparisons across foragers, farmers, and Western postindustrial societies. See esp. Konner 2005 for a detailed reexamination of the literature on hunter-gatherer infant care highlighting how much shared care was actually going on among the !Kung.

  23. Hill and Hurtado 1989; Hewlett and Lamb 2005.

  24. Lancaster 1978; Wall-Scheffler et al. 2007.

  25. Konner 1972:292.

  26. Blurton Jones 1993:316. See esp. overview of this literature in Konner 2005.

  27. Based on observations by Blurton Jones’s coworker Frank Marlowe (2005b:182).

  28. For the Mbuti see Turnbull 1965; quotation from Turnbull 1978:172, cited in Hewlett 1991b:13.

  29. Tronick et al. 1987, writing about the Efe.

  30. Hewlett 1989a, 1989b; Rosenberg and Trevathan 1996. For more on placentas, see Chapter 7.

  31. Morelli and Tronick 1991; Hewlett, Lamb et al. 2000. In the majority of human societies mothers wait for several days before initiating breastfeeding (Hewlett 1989a).

  32. Morelli and Tronick 1991:47.

  33. Hewlett 1989a.

  34. For Agta case, see Peterson 1978:16, cited by Hewlett 1991a:13.

  35. Crittenden and Marlowe 2008.

  36. Konner 2005; Hewlett 2001.

  37. See Rosenberg and Trevathan 1996.

  38. For overview and recent summary of the !Kung data, see Konner 2005. For Efe fieldwork, see Ivey 2000 and Morelli and Tronick 1991. For Aka, Hewlett 2001. I have focused here on foraging societies, but cross-cultural surveys suggest that across many types of human societies it is usual for allomothers to be the first to touch and hold the baby. According to Hewlett 1989a, this applies in some 92 percent of the world’s cultures.

  39. Ivey 2000, Figs. 3, 4, and 5, Tables 4 and 5.

  40. Eibl-Eibesfeldt 1989:138–145; personal communication from Alyssa Crittenden, 2006.

  41. Hewlett, Lamb, et al. 2000, Table 1. This allomaternal provisioning included breastfeeding as well as kiss-feeding. The amount of allomaternal provisioning among these foragers was much higher than among neighboring agriculturalists, the Ngandu.

  42. Goodall 1969:398.

  43. Stern 2002.

  44. Watson 1928.

  45. Bowlby 1971:319.

  46. For infantile preferences for attractive faces see Langlois et al. 1987. For experiments on gaze-following see Farroni et al. 2004. For smells see Porter 1999.

  47. See overview in van IJzendoorn and Sagi 1999 and references therein.

  48. Bowlby 1971:228–229 and elsewhere. Subsequently Konner incorporated Bowlby’s continuous-care-and-contact model as a key component of “the Catarrhine Mother-Infant Complex” (see, e.g., Konner 2005:39–41).

  49. Both vervet and patas monkeys spend about as much time on the African savannas as baboons do, yet in both species mothers allow other females (often nulliparous females gaining practice for motherhood) to take their babies (Lancaster 1971; Hrdy 1976; Nicolson 1987) as early as the first or second day after birth (2007 personal communications from Janice Chism for patas and Lynne Isbell for vervets). Similarly, there is a lot of infant-sharing among some of the more tolerant, albeit less-well-studied semiterrestrial macaque species, including Macaca sylvanus (mostly involving male caretakers) and Macaca tonkeana, where other females, esp. juveniles or subadults, take and carry infants as young as a few days old (Thierry 2007 and personal communication, 2008).

  50. By the time volume 1 of Bowlby’s trilogy on Attachment and Loss was published (1969), we had early field reports of infant-sharing among langurs and titi monkeys (Jay 1963; Mason 1966).

  51. See Pereira et al. 1987 for Varecia variegata. For V. rubra see Pereira and Izard 1989; Vasey 2008. Pereira and Izard (1989) report a rare case in which an unrelated ring-tailed lemur female spontaneously lactated and nursed twins born to a groupmate. In the vast majority of primates, mothers fiercely resist attempts to suckle by infants not their own.

  52. Eberle 2008 for Microcebus murinus; Kessler and Nash 2008 for Galago senegalensis.

  53. Radhakrishna and Singh 2004.

  54. Assunção et al. 2007.

  55. For detailed early observations of biparental care among wild titi monkeys (Callicebus molloch) and grey-necked owl (also called “night”) monkeys (Aotus trivirgatus), see Wright 1984. For wild Aotus azarai, see Wolovich et al. 2007. For gibbons see Nettelbeck 1998.

  56. Fernandez-Duque 2007; Wolovich et al. 2007. For titi infants more upset by separation from fathers than mothers, see Hoffman, Mendoza, et al. 1995.

  57. Small 1990 (and personal communication 2006) regarding infant transfers on their first day postpartum.

  58. Taub 1984.

  59. Reviewed in Paul et al. 2000. Although this assertion was highly controversial when first proposed (Hrdy 1977b, 1979), it is now increasingly clear that infanticide by males occurs in prosimians, Old and New World monkeys, and apes, and can be a major source of infant mortality (see for example van Schaik and Janson 2000). In some of the best-documented cases, infanticide accounts for 30 to 50 percent or more of all deaths in infancy (for example, Sommer 1994; Palombit 1999, 2001; Cheney and Seyfarth 2007), swamping other sources of variance in maternal reproductive success (Fedigan et al. 2007).

  60. For calculations explaining why I am convinced that female langurs have a roughly 0.16 chance of sharing a gene by common descent, see Seger 1977. Recent genetic findings are consistent with Seger’s initial calculation based on behavioral evidence (Little, Sommer, and Bruford 2002).

  61. Hrdy 1976, 1977a.
Even in continuous-care-and-contact species like chimpanzees, nulliparous females are the most interested in babies, though they do not gain much access to them before babies are older than six months (Nishida 1983).

  62. Struhsaker 1975:65–66.

  63. Pusey and Packer 1987.

  64. This 20 percent estimate derives from Wright 2008 and from an ongoing classification of infant care among primates by Stacey Tecot, Patricia Wright, Noel Rowe, and myself.

  65. Primates with shared suckling can be found in a number of genera, including Galago, Lemur, Microcebus, Propithecus, Varecia, and Cebus.

  66. For shared care and suckling in the genus Cebus see Perry 1996; Manson 1999; Baldovino and Bitetti 2008. For hunting and sharing of even high-value food items, see Carnegie et al. 2008 and esp. Rose 1997, Table 6.

  67. My use of the term cooperative breeding in this way dates from Hrdy 1999, 2005a, although I have since learned that alloparental provisioning is more widespread in primates than I then realized. For more on the history of the term and definitional confusion surrounding the way cooperative breeding is applied, see Chapter 6.

  68. Garber 1997.

  69. Ross et al. 2007.

  70. French 2007.

  71. According to calculations by Ross et al. 2007 (“Supporting Information” available online), the degree of relatedness between marmoset brothers may be on the order of 57 percent.

  72. See calculations by Haig (1999), a Harvard evolutionary geneticist who anticipated the discovery of chimeric germ lines in marmosets.

  73. Primate breast milk tends to be quite dilute compared with the very rich milk of other mammals whose babies spend more time away from their mothers, as among tree shrews or rabbits, where “absentee” mothers leave their young behind in dens for long periods. Regardless of whether they are continuous-care-and-contact or infant-sharing mothers (Hrdy 1999:127–129ff., and references therein), primate mothers tend to produce milk that is low in fat and low in carbohydrates. In the case of infant-sharing species, babies can make up at night for time away from the lactating mother during the day. Marmoset milk is an exception, far richer than that of other infant-sharing monkeys with on the order of four times more protein. One possible explanation is that the richness of marmoset milk has more to do with rapid early growth than with time off the mother. (Mother seals, for example, produce very rich milk, not because of shared care but because their babies need to grow fast.) At present, we do not have sufficiently detailed comparative data on mother’s milk in primates to assess the various possibilities.