Mothers and Others

by Sarah Blaffer Hrdy

  The rise of attachment theory in the postindustrial West not only ushered in more humane treatment of babies, it also led to practical benefits for parents. A baby confident of a rapid response by a mother committed to his well-being is likely to become a child who will be quicker to soothe and adapt to new situations, and likely to grow up to feel confident about human relations generally. In a complete reversal of Watsonian logic, over the long haul babies with more responsive mothers are going to cry and cling to their parents less, not more.

  Today, the main outlines of attachment theory are widely accepted. Developmental psychologists have fanned out around the world to test its major tenets among babies in Africa, Europe, Japan, and Israel, as well as Central, South, and North America.47 The Handbook of Attachment Theory published in 1999 runs 925 pages, weighs in at just under four pounds, and already has a new edition in the works. It summarizes hundreds of studies, most of them from Western societies, elucidating how and why a baby’s felt need for a “warm, intimate, and continuous” relationship turns out to be as addictive as opium. It also lays out compelling evidence for how and why the infant’s confidence in his or her caretakers contributes to emotional security and sets up expectations (or “internal working models”) about the social world that lay the groundwork for subsequent relationships.

  By the late 1990s, however, an explosion of new information concerning the demography and behavior of other apes along with new information about childcare among hunter-gatherers and other traditional peoples began to call into question the applicability of Bowlby’s homology between maternal behavior in humans and our closest ape relations. For Bowlby, the continuous-care-and-contact mothering so readily apparent among the nonhuman Great Apes was not only appealing and consistent with Western presumptions about how “good mothers” ought to behave, it fit with his assumptions about the homologies between infant needs in human and nonhuman primates. What Bowlby overlooked was the many alternative modes of infant care found among primates.

  In his classic 1969 book Attachment, Bowlby singled out chimpanzees, gorillas, and two species of cercopithecine Old World monkeys—baboons and rhesus macaques—as the primate templates for how our African savanna-dwelling ancestors must have cared for babies. Bowlby specifically chose them because, as he put it, “All four species, and especially baboon and gorilla, are adapted to a terrestrial existence.” Among primates who traveled and spent a lot of time feeding on the ground, a baby would need to be continuously held by his mother, Bowlby reasoned, in order to be safe from predators.

  The discipline of primatology was still fairly new, and these four species did happen to be among the first ones studied. Furthermore, experimental studies of captive chimpanzees and rhesus monkeys supplemented information from the wild. Nevertheless, Bowlby’s choice was probably also influenced by an additional criterion that he may not have been conscious of. Each of these species conformed to preconceived Western ideals of how a mother should care for her infant.48 Mothers belonging to primate species that also spent a lot of time on the ground but happened not to remain in continuous tactile contact with their babies went unremarked.

  The continuous contact between mother and infant that seemed so self-evident and so natural to Bowlby, as well as to Darwin, in fact characterizes only a slim majority (if that) of the living primates. Exclusively maternal infant care is scarcely the whole story. It leaves out the other 40 to 50 percent of some 276 species. These include such notably terrestrial African savanna-dwelling catarrhine Old World monkeys as vervet monkeys and patas monkeys, as well as various semiterrestrial north African and Southeast Asian species of macaques.49 Mothers in these species freely allow other group members to hold their babies, presumably saving energy and sparing themselves the awkwardness of carrying new babies while they feed. Detailed studies of infant-sharing species only became available later, but preliminary observations of infant sharing in some species were known, albeit accorded little significance by early attachment theorists.50

  When Bowlby’s 1969 classic Attachment was republished in paperback, the cover photo of an Amazonian Indian emphasized the then-prevailing assumption of continuous skin-to-skin contact between mothers and their infants in nomadic hunter-gatherer societies. (Basic Books/Perseus Book Group)

  To correct the record, join me on a brief tour of how mothers among this overlooked half of the primate order deal with infants in the period after birth. Three points will emerge. First, there is no one, universal pattern of infant care among primates. Second, far from being a hardwired primate-wide trait, continuous-care-and-contact mothering is a last resort for primate mothers who lack safe and available alternatives. Third, and perhaps most important so far as primates are concerned, there is nothing evolutionarily out of the ordinary about mothers cutting corners or relying on shared care.

  A simple guide to the prosimians, monkeys, and apes mentioned in the text. For additional detail I recommend Noel Rowe’s Pictorial Guide to the Living Primates.

  HOW THE OTHER HALF LIVES

  Our survey of maternal shortcuts begins with prosimians. Of all extant primates, the ones that most closely resemble ancient primates from the fossil record of 50 million years ago are lemurs, lorises, and bushbabies. It is assumed that their now-extinct primate precursors gave birth to multiple young, like many prosimians today. If so, mothers probably left them in nests when they went off to forage, just as some of their modern lemur descendants do. Among mouse lemurs, dwarf lemurs, and bushbabies (or “galagos”), mothers nonchalantly leave entire litters in their sleeping nests while they forage. “Stay put, see you later.”

  Among the ruffed lemurs of Madagascar, one of the few primates that can actually be said to have a nesting instinct, pregnant females close to parturition build nests specifically for use as nurseries. These mothers share care of their infants (often twins) with the father and perhaps another lactating mother. When the mother goes off to forage, one of these allomothers stays behind, and if the babies get hungry before their mother returns, a lactating co-mother may suckle them.51 Galago and mouse lemur babies may similarly be co-suckled as well as kept warm by allomothers who are usually aunts, sometimes grandmothers.52

  With neither nests nor allomothers, some prosimians simply stash babies as best they can, the way bamboo lemur and many lorisid mothers do. Parking babies this way is risky. Indian slender loris mothers often hedge their bets by hiding one twin in one spot and the other someplace else. If a predator stumbles on one, the mother still has an heir to spare.53 Monkey mothers with singleton young are understandably more cautious. Nevertheless, in a pinch, woolly spider monkeys (the rare and endangered Brazilian muriquis) may park older babies. In one rare instance when a mother’s own mother was available (unusual because muriqui mothers typically leave home before breeding), the maternal grandmother carried her grandson for extended periods.54

  Pretty clearly, leaving a baby with someone else is preferable to parking it, as long as a caregiver is available, willing, competent, and well-disposed and the mother trusts him or her to return the infant unharmed. Not surprisingly, the best primate caregiver on offer will often be the father. In most mammals, fathers would not be anywhere nearby. But primates are unusual. Instead of decamping after they mate, fathers in most species in the order Primates remain year-round in the same social group as the mothers of their offspring (about which much more in Chapter 5).

  Nowhere in mammaldom do fathers behave in a more exemplary fashion than among two types of New World monkeys, the sixteen monogamously mating titi monkey species belonging to the genus Callicebus, and the various wide-eyed species of night monkeys in the genus Aotus. These fathers not only carry babies about but provide them with food.55 New mothers are followed everywhere by a mate whose top priority in all the world, day in and day out, is to remain nearby and carry her baby whenever it is not nursing. Human mothers can only fantasize about such an unlikely state of affairs. Callicebus and Aotus dads are so attentive that infant titi o
r night monkeys form their primary attachment to the father. While a night monkey baby is more likely to beg food from his dad than his mom, a titi baby becomes more upset (as measured by vocalizations and elevated adrenocortical activity) if the father is removed than if the infant is separated from his mother.56 I know of no other mammals whose babies are routinely more attached to their fathers than to their mothers.

  By the end of the first week, a titi monkey mother’s daytime contact with her baby is down to just four or five bouts of suckling per day. Her mate carries the baby 90 percent of daytime—with a little help from an older sibling, if there is one. Nevertheless (do some things never change?), mom still does diaper duty, licking her baby’s genitalia clean during the brief periods when the baby is back on board to nurse. Even after the baby starts to move about, around six months of age, the father will be more eager than the mother either to play or to share food, typically fruit and insects. Meanwhile, the no-nonsense titi monkey mom concentrates on her own feeding, preparing herself to gestate and then breastfeed their next baby.

  A titi male’s mate is rarely out of his sight, making him the likeliest sire of any baby born to these typically monogamous primates. This differs from the usual situation where a primate male’s paternity is less certain. But even without the certainty of paternity, males sometimes help, as among the Barbary macaques of North Africa. When in estrus, female Macaca sylvanus eagerly solicit and mate promiscuously with just about every male in their multimale troop. Yet after babies are born, right from day one, males take turns carrying them around.57 Such care by possible or would-be fathers is neither so exclusive nor so costly as the attention lavished on young by the single-minded titi monkey male. Yet without this extra care from males, Barbary macaque infants could not survive the harsh winters of the Atlas Mountains where they evolved.58 To ensure that at least some of his offspring survive, a male Macaca sylvanus errs on the conservative side of the uncertainty that surrounds paternity in this species. The risk to a male’s posterity from caring for another male’s offspring is outweighed by the still graver risk of dying childless.

  This titi monkey baby spends most of his day riding on his father’s back. His older sister (in front) also occasionally helps out. When researchers at the University of California-Davis briefly removed a parent, the baby was more distressed by separation from his father than from his mother. (Mike Nelson/California National Primate Research Center)

  In an overwhelming majority of primates, males remain year-round in the same social group as females with whom they have mated, but their assistance is typically limited to generalized protection of the troop from predation or from marauding males likely to kill infants, since in many populations infanticide by alien males is the major source of infant mortality.59 In extreme emergencies, probable fathers may snatch an infant out of harm’s way or, if the mother should die, adopt a weaned orphan. Nevertheless, as far as direct care is concerned, most primate mothers have to rely on other adult females or on juveniles or subadults eager to practice their mothering skills, rather than on male caregivers. So in which species do mothers voluntarily share access to young infants?

  Old World monkeys are divided into two subfamilies, the cercopithecines and colobines. Most cercopithecine Old World monkeys, including such well-known species as rhesus macaques and savanna baboons, exhibit quintessentially continuous-care-and-contact mothering. Interested allomothers might be allowed to briefly touch, but not take, a new infant. Relatively few cercopithecine monkeys behave like Barbary macaque mothers, who freely hand over their newborns to others. Among colobine Old World monkeys, however, this pattern is reversed. Infant-sharing occurs in most of them. In only a few species (such as the Central African red colobus monkeys) do mothers refuse access.

  Aside from humans, few primate mothers are more willing to share their newborns than the beautiful gray Hanuman langurs that I studied in India. I originally chose this species because I was interested in finding out why males among these colobine monkeys were sometimes killing infants. Subsequently, even though I knew a bit about shared care from having watched babysitting behavior among African patas monkeys, I was surprised to find how big a role infant sharing played in langur lives.

  Throughout life, a female langur remains in the same group in which she is born, in the company of her mother, maternal grandmother, aunts, and other kin. On average, females in this highly matrilocal group are related as closely as first or second cousins.60 Since dominance relations between females in the same group are relatively flexible and relaxed, mothers do not need to worry (as they do among more rigidly hierarchical rhesus macaques or baboons) that an allomother will harm an infant or prevent the mother from retrieving it—which, when it happens, may end with the baby starving to death. Baby langurs are passed among their cousins and older siblings, held briefly by aunts or grandmother, and may be off their mothers for up to half a day as early as their first day of life. Yet babies are always safely retrieved by the mother. Young and inexperienced females are the most eager to hold babies.61 Yet, like most other primates (titi and night monkeys being important exceptions), a baby Hanuman langur’s primary attachment remains to his mother.

  Although it is often assumed that continuous contact with the mother would be essential for infant survival among primates that spend time on the ground, langur monkeys are the most terrestrial of the colobines and are also inveterate infant-sharers. The female langur on the left is taking the infant (who resists the transfer) from the allomother on the right. (S. B. Hrdy/AnthroPhoto)

  Family daycare is found across the far-flung colobine subfamily, among black-and-white colobus monkeys of Africa, dusky leaf monkeys of Thailand and Malaysia, ebony langurs of Java and Bali, silver leaf monkeys of Burma and Borneo, and purple-faced leaf monkeys of Sri Lanka, to name just a few. Only a handful of colobine mothers refuse to let others hold new babies, and the exceptions are revealing. They include species like the red colobus monkeys of Central Africa (Procolobus badius) among whom babies are three or four months old before their mothers let them approach another female.62 The reason these mothers are so possessive is that they do not ordinarily have close matrilineal kin nearby when they give birth. Like chimpanzees or gorillas, red colobus females leave their natal troops and move to another troop before reproducing.63 Not having kin that she can trust constrains a mother’s childcare options. These options are further constrained by the fact that the mother is usually the only one providing her baby with food. Other than humans, the most important exceptions to this primate rule are found among fairly distant primate relations rather than among our fellow apes. These cooperatively breeding monkeys are worth considering in some detail.

  FULL-FLEDGED COOPERATIVE BREEDERS (DAYCARE PLUS SNACKS)

  Alloparental care of infants is widespread across the order Primates. However, only in some 20 percent of species do alloparents ever provision as well as care for young, and for the most part this provisioning does not amount to much.64 As mentioned above, some prosimian co-mothers will suckle one another’s young, as will New World monkeys in the genus Cebus, among whom a lactating female may provide a brief pick-me-up to another female’s older but still suckling three-to-six-month-old infant when that infant approaches her and clamps onto her nipple.65 In addition to such suckling, cebus monkeys occasionally allow someone else’s infant to take food. Even though meat is not a big component of Cebus diets, all species in this genus are avid hunters, and allomothers may permit older infants to scrounge bits of baby squirrel or coatis that they have caught. This tolerated scrounging of highly desired items goes beyond the rare instances of tolerated taking of food seen in bonobos. Among capuchin monkeys (Cebus capucinus) as many as one fifth of all instances of food sharing involved food actively offered by an older monkey to an immature.66

  More extensive provisioning is of course commonly observed in titi and night monkeys, but since the provisioner is almost always the mother’s monogamously mated partner, this behav
ior qualifies as biparental care rather than cooperative breeding. So far the only nonhuman primates among whom alloparents frequently bring food to the young of others, doing so regularly, spontaneously, and voluntarily, fall into four genera (Callithrix, Leontopithecus, Saquinus, and Callimico) belonging to the family Callitrichidae—mostly marmosets and tamarins. Even though roughly a fifth of all primates exhibit some degree of shared care and provisioning, these marmosets and tamarins, along with humans, are the only ones I consider to be “full-fledged cooperative breeders.”67

  Famous for breeding fast and for their rapid colonization of new habitats, some 39 species of Callitrichidae are currently deployed across Central and South America. Babies in these species, typically twins, are carried most of the day by one or more adult males. Usually, only the group’s most dominant female breeds, although groups with two breeding females have been observed. Males attempt to defend access to breeding females, but females have their own predilections and may copulate with several partners.

  Since a male marmoset or tamarin is no bigger than his mate, it is hard for him to exercise much control over her. Instead of expending energy growing weaponry and duking it out tooth-and-claw in a vain effort to defend exclusive sexual access to his mate, males compete for paternity by other means—specifically, by ejaculating more sperm than a competitor does. Relative to their body size, callitrichid testicles are enormous. There can be as much as a 45 percent difference in size between one male’s testes and another’s.68 Energy conserved by avoiding direct competition can be channeled into caretaking. This also means that in the absence of DNA testing, it is impossible to know who the father is.