Why Cry Adaptive Significance of Intensive Crying in Human Infants

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Evolution and Human Behavior 19: 193202 (1998)

1998 Elsevier Science Inc. All rights reserved.


655 Avenue of the Americas, New York, NY 10010
1090-5138/98/$19.00
PII S1090-5138(98)00014-2

Why Cry? Adaptive Significance of
Intensive Crying in Human Infants

Virpi Lummaa and Timo Vuorisalo

Section of Ecology, Department of Biology, University of Turku, Turku, Finland

Ronald G. Barr and Liisa Lehtonen

Departments of Pediatrics and Psychiatry, McGill University and the McGill
University-Montreal Childrens Hospital Research Institute, Montreal,
Quebec, Canada

Prolonged crying at the beginning of life in humans appears to be related to a specific
stage of development. We address the possibility that the human infants predisposition
to increased crying might be adaptive in an evolutionary sense by promoting survival
and future reproductive success of the child. We emphasize the evolutionary history of
humans to derive four hypotheses about the benefits of intensive infant crying. First, ac-
cording to an historical hypothesis, crying indicates distress of infants due to physical
separation from their parents. In the evolutionary past of

Homo sapiens

, infants appear
to have been continuously carried by their mothers. In those circumstances, prolonged
physical separation probably meant abandonment by the parent. Second, crying may be
an adaptation to decrease the likelihood of infanticide that has been common in many
human societies during adverse ecological conditions. Assuming that the quality of off-
spring affects the probability of infanticide, intensive crying could enhance an infants
survival by signaling the vigor of the infant. The third hypothesis is that the infant may
utilize his or her crying capacity to psychologically manipulate the parents to provide
more parental care. Finally, the superchild hypothesis posits that crying may be a ma-
nipulation that attempts to avoid the costs of sibling competition by increasing the inter-
val between births. Predictions that follow from each hypothesis are discussed. 1998
Elsevier Science Inc.

KEY WORDS:

Colic; Crying; Infanticide; Honest signaling; Natural selection; Parentoff-

spring conflict; Survival.

Received October 3, 1997; revised February 27, 1998.
Address reprint requests and correspondence to: Dr. Virpi Lummaa, Section of Ecology, Department of
Biology, University of Turku, 20014 Turku, Finland. Fax: 358-2-333-6550; E-mail: Virpi.Lummaa
@utu.fi
194

V. Lummaa et al.

ll babies cry, but some cry a lot more than others. Furthermore, human
infants have been found to cry more during the early weeks of life both
in modern Western (Barr 1990a) and hunter-gatherer societies (Barr et
al. 1991; St. James-Roberts et al. 1994). Soliciting vocalization of neo-
nates is widespread in birds and mammals, and the early crying of human infants
probably corresponds to the pattern observed in other primates (Furlow 1997; New-
man 1985). Although biological determinants very likely account for the universal
patterns of crying, there is considerable variation in how these patterns are mani-
fested. In some populations, babies appear to cry more intensively than in others.
Furthermore, there are large differences in the total amount of crying among infants
raised in the caregiving settings characteristic of modern Western societies and
those raised in more traditional settings (Barr and Elias 1988; Barr et al. 1991;
Bensel 1997; Hunziker and Barr 1986; Lee 1994). Ultimate reasons for this are
rather unknown.
The distribution of the so-called colic syndrome provides an example of such
cross-populational variation. In clinical practice, a baby is said to have colic if it
cries for more than 3 hours per day for more than 3 days per week for a period of at
least 3 weeks (Wessel et al. 1954). It is a common, but probably incorrect, belief that
colic is usually due to organic disease (Miller and Barr 1991). A medical cause for
colic is found only rarely (Gormally and Barr 1997; Miller and Barr 1991). It has
been suggested that, instead of regarding the colicky behavior of human neonates as
a medical syndrome, it should be regarded as continuous with normal crying, and a
predictable consequence of crying being prolonged in the context of caregiving
practices in Western societies (Barr 1997; Miller and Barr 1991). The colic syn-
drome seems to be more common in Western than in hunter-gatherer societies.
A few recent articles have addressed the adaptiveness of different types of in-
fant crying in

Homo sapiens

. According to Barr (1990b, 1997), the predisposition of
human infants to early increased crying in the first few months of life might have
been adaptive in the evolutionary past of our species, and the original functions of
crying should be borne in mind in studies of colicky behavior. Furlow (1997) ana-
lyzed acoustic features of newborn crying as components of parentoffspring com-
munication and argued that cry quality serves as an honest signal of an infants qual-
ity and reproductive value. The acoustic structure of cries as well as the metabolic
cost of crying depend on the phenotypic quality of offspring, and such features need
to be included in evolutionary models of parentoffspring conflict.
This article explores the behavioral and phylogenetic evidence for adaptiveness
of intensive crying in human infants. We present four specific hypotheses address-
ing situations in which early crying in humans could be beneficial, and we compare
them with existing data.

INFANT CRYING: HONEST SIGNALING OF
WHAT AND WHEN?

In principle, only signals that are honest indicators of the signalers quality are
likely to persist in evolutionary time, and the reliability of such signals is maintained
A
Adaptive Signicance of Infant Crying

195

by the costs of signaling (Zahavi 1977, 1987). Further, there should be a direct link
between the signals design and the quality being signaled. There is strong evidence
that crying quality (acoustic characteristics, duration) is correlated with infant vigor
and thus can be considered an honest signal of offspring quality (Furlow 1997).
Capacity for crying demands extra energy. Probably because of the muscular activ-
ity involved, crying increases energy expenditure on the order of 13% in newborns
(Rao et al. 1993). Thus, only vigorous infants can afford to cry intensively.
But in what circumstances is honest signaling of the offsprings quality neces-
sary? Because signaling is costly, it should not be expressed unless necessary. It
seems likely that signaling vigor may be adaptive whenever there is a risk of de-
creased parental care as perceived by the child. The childs decision to cry or not
to cry is likely to be based on changes in parental behavior (e.g., changes in the
length of physical separation, or in feeding frequency). From the parental point of
view, the cost of neglecting or killing the offspring is higher the more vigorous the
child. In the following, we will emphasize the conditions in which signaling of off-
spring quality in our evolutionary past may have been of vital importance, and de-
rive hypotheses for the benefits of infant crying.

HISTORICAL HYPOTHESIS: CRYING AS A SIGNAL OF
SEPARATION DISTRESS

Intensive crying of an infant may indicate emotional stress due to physical separa-
tion from the parents. Sinclair et al. (1986) claim that protohominid quadrupeds
were plant gatherers and occasional scavengers, much like contemporary baboons.
The ability to carry the young in an upright stance enabled hominids to migrate
together with large grazing herbivores in East African savannas and to forage for
carcasses, i.e., to exploit an earlier unfilled niche. Thus, in the evolutionary past of

Homo sapiens

, infants had to be almost continuously carried, leading to persistent
close physical contact between the mother and her young offspring. If true, the
hypothesis of Sinclair et al. (1986) suggests that intensive crying in newborn
humans simply indicates distress of infants who are physically separated from their
parents. The practice of separating the infant from its mother, as occurs when placed
in a cot or infant seat, appears to have become widespread only in modern Western
societies (Barr 1997). In the past, lack of physical contact may have signaled to the
child a risk of desertion. Intensive crying may be a response that evolved to reduce
that risk through restoration of the relationship with the parents or through adoption
by other group members.
As in early hominids, some modern hunter-gatherers, such as the African
!Kung San tribe mothers, carry their infants constantly in their arms or in a sling.
Their caregiving practices differ from those of customary Western societies in many
other respects as well (Barr 1990b; 1997). !Kung San infants are fed continuously
(that is, much more frequently and at briefer intervals) (Konner and Worthman
1980) rather than in the pulse pattern typical of Western societies. !Kung San
mothers also are more likely to respond rapidly to crying than are Western mothers
(Barr et al. 1987). Similarly, infants of some modern pastoralists are in almost con-
196

V. Lummaa et al.

stant physical contact with their mothers during their first 15 to 18 months, e.g., the
Turkana of Kenya (Gray 1996).
The historical hypothesis predicts that prolonged vocalization of infants should
be less common in contemporary societies in which the infants have a closer physi-
cal contact with their mothers, as this appears to be a historically and phylogeneti-
cally more basic caregiving context for young human offspring than the typical
current Western practice (Christensson et al. 1995). The neonatal separation call is
considered to be the most primitive mammalian vocalization (Furlow 1997; Mac-
Lean 1985). Distress calls analogous to human crying are common in many mam-
malian and bird species whose offspring need intensive and prolonged parental care
owing to the high risk of mortality among the more helpless and youngest age
groups (Lorenz 1970; Smotherman et al. 1974). The 50% shorter duration of !Kung
San infant crying time compared to that of American and Dutch infants, as well their
diminished tendency to prolonged crying bouts (Barr et al. 1991), are consistent
with this hypothesis.
There also is some direct evidence suggesting that a number of caregiving
practices affect crying in human infants. Hunziker and Barr (1986) showed experi-
mentally that increased duration of immediate physical contact between parents and
infants affected the length of crying. An increase in the duration of infant carrying
of 1.7 hours per day between 4 and 12 weeks of age resulted in a 43% reduction in
the total daily duration of crying. The frequency of crying did not change, leading
Barr (1997) to conclude that it is the predisposition to frequent but short crying
bouts that may have potentially positive consequences for the infants. The fre-
quency of crying bouts among the !Kung San infants is essentially the same as that
of Western infants (Barr et al. 1991). Thus, the data suggest that the prolonged cry-
ing bouts may be a direct consequence of many of the caregiving practices typical of
contemporary Western societies.

INFANTICIDE HYPOTHESIS: CRYING AS A MEANS
TO INHIBIT INFANTICIDE

Generally, when the reproductive value of the young falls to such a low level that it
is unlikely that even a high investment could save the child, parents may increase
their own fitness by premature termination of parental care for some offspring of the
brood if this enhances either the fitness of surviving offspring or the parents own
future reproductive capacity (OConnor 1978; Parker and Mock 1987). Brood
reduction is most likely to be favored early during the breeding attempt, as the
potential benefits of infanticide to all parties fall as the time of weaning approaches.
Infanticide in humans could contribute to the survival or quality of prior off-
spring or to the total reproductive success of the mother in the case of deliveries that
are spaced too closely, as the brood of humans consists of offspring from sequen-
tial births (Colinvaux 1982) who are still totally dependent on their parents at the
moment of birth of the next child. Indeed, Colinvaux (1982) has suggested that in-
fanticide is an important means for controlling the number and spacing of progeny
Adaptive Signicance of Infant Crying

197

in humans, because continuous sexual activity in humans may lead to exceeding the
number of births that would maximize the number of offspring surviving to adult-
hood. Hence, the rate of offspring production in humans has been selected downward
by natural selection from its current physiological maximum (Alexander 1974).
Infanticide has been common in many human societies (reviewed in Dickeman
1975), possibly dating back to the upper Paleolithic age (Carr-Saunders 1922). Kill-
ing, and sometimes cannibalism, of newborn infants has been widespread, particu-
larly in the contexts of closely spaced babies, twinning, sex preferences, and adverse
ecological conditions leading to famine (Alexander 1974). For example, whereas in
some cases both twins have been destroyed, usually either the male twin or the
stronger of the two twins has been allowed to live (Granzberg 1973). The likelihood
of infanticide also may correlate with the number of earlier offsprings, as the risk of
being killed can depend on whether the child does or does not have siblings. Physi-
cal and mental deformities have been common reasons for infanticide (Montag and
Montag 1979). In most cases, choices have been made to rear only children that are
considered strong enough to begin with. Methods of infanticide vary from deliberate
killing to reduced biological support or outright abandonment (Scrimshaw 1984).
Intensive crying of human infants could be an adaptation to decrease the proba-
bility of infanticide. Crying indicates vigor as it demands extra energy. Assuming
that the quality of the offspring affects the probability of infanticide and that crying
capacity is a reliable measure of quality, the infanticide hypothesis predicts that an
infants predisposition to intensive crying acts to enhance its survival. The hypothe-
sis would gain support if further studies could show reliably that infants that indicate
their vigor by intensive crying have been killed less frequently than more passive
ones, especially under adverse ecological conditions.

BLACKMAILING HYPOTHESIS: CRYING AS A MEANS TO
ATTRACT ATTENTION BY CAUSING HARM TO ONESELF

Whenever parents are not genetically identical to their offspring, they are expected
to disagree with the offspring over how long the period of parental investment
should last, the amount of parental investment that should be given, and the altruis-
tic and egoistic tendencies of the offspring if these tendencies affect other relatives
(Trivers 1974). Consequently, parental level of expenditure may be constrained by
the behavior of their own offspring and, as a consequence of the conflict of interest
between parents and offspring, the mean fitness of both parties may be reduced
(Parker 1985; Trivers 1974). The more an offspring demands from its mother in the
early stages of its postnatal development, the more likely it is to survive in the short
term. However, the overall probability that the offspring will survive might depend
not only on behavior such as nursing, but also on pre- and postweaning maternal
care. Thus, the short- and long-term effects on the probability of survival interact to
give an optimum level of offspring careseeking at each stage of its development
(Bateson 1994). Alternatively, costly begging behavior has been explained as a
means by which offspring communicate their needs, allowing parents at equilibrium
198

V. Lummaa et al.

to provide them with a level of resources equal to that which would be optimal for
the parents in the absence of begging (Godfray 1991, 1995). Thus, the level of off-
spring solicitation could be a true reflection of offspring need as long as solicitation
is costly and the benefits of the extra resources increase with need. However,
Johnstone (1996) has shown that intense solicitation by offspring also may lead par-
ents to allocate more resources than would otherwise be optimal for the parents, as
parental efforts are directed at reducing subsequent levels of costly solicitation by
their young.
Both bird and mammal offspring commonly attempt to persuade their parents
to give them additional food, often in ways that appear to be costly in terms of fit-
ness. Intensive begging calls raise the likelihood that the attention of a predator will
be attracted to the nest (Perrins 1965; Zahavi 1977). If offspring perform temper
tantrums, they could threaten the parent by suggesting that the offspring may actu-
ally harm itself (Trivers 1985). For example, young pelicans can beg vigorously for
their food by grabbing, shaking, and biting their own wings (Burke and Brown
1970), apparently in order to convince the parent that withholding food will have
consequences for the health of the chick. Further, young chimpanzees exhibit tem-
per tantrums involving banging their head on the ground to increase access to breast
milk (Goodall 1986). These tantrums appear to make mothers nervous and tense, of-
ten leading them to give in to their descendants demands.
We propose that intensive crying of human infants could be comparable to so-
licitation by offspring of other species of mammals and birds by making parents ex-
ceed their optimal level of investment to the infant. Noisy solicitation by infants
may attract the attention of both parents and possible predators, and in some condi-
tions the infants may have benefits from this. In fact, by intensive crying a human
infant may try to blackmail the parent with the threat of increased risk of preda-
tion, or dangerous loss of energy, thereby gaining more energy or attention from the
parent than the parent has an evolutionary interest to provide. It has been shown that
excessive crying is associated with clinically significant levels of maternal emo-
tional stress (Miller et al. 1993). However, because blackmailing incurs a higher risk
of mortality for the child itself, it is predicted that the child will exhibit intensive
crying only if there is a real utility to receiving the additional care, and if the real
risk of predation is not excessively high. Thus, the expected positive outcome, i.e.,
more frequent feeding, more effective nursing, or increased birth interval, should be
great enough to more than compensate for the energetic costs of crying and in-
creased risk of predation.
The probability that the parents will respond positively to such blackmailing at-
tempts by the offspring depends on the real risk of predation due to loud vocaliza-
tion by the child. It can be predicted that parents will react rapidly if the child cries
intensively and the predation risk is high. In addition, the quality of the signaling
offspring, as well as the number and quality of its siblings, can be predicted to influ-
ence parental behavior, as the intensive crying of one offspring endangers the whole
brood and the parents, forcing the parents to evaluate the reproductive value of the
whole progeny. The hypothesis would gain support if intensive crying could be
shown to increase care provided by the parents to a greater extent in predator-rich
environments than in average environments.
Adaptive Signicance of Infant Crying

199

SUPERCHILD HYPOTHESIS: CRYING AS A MEANS OF
MINIMIZING THE COSTS OF SIBLING COMPETITION

An exceptionally vigorous child can signal its strength by intensive crying to minimize
costs of sibling competition. Provided that there is (1) a general correlation between
the vigor of the child and its fitness, (2) a general correlation between crying inten-
sity and vigor (Furlow 1997), and (3) a high risk of failure of reproduction for par-
ents, it might be useful for the parents to invest heavily in a superchild when they
manage to produce one. The infant may try to steal investment from its successors
by demanding to suck throughout the night as this may delay the birth of the next
sibling, a likely competitor (Blurton-Jones and da Costa 1987). Parents may volun-
tarily increase the birth interval for the benefit of an exceptionally vigorous child.

DISCUSSION AND CONCLUSIONS

Our hypotheses are based explicitly on the assumption that the capacity of human
infants to vary crying intensity is adaptive, i.e., it has evolved to enhance the sur-
vival and future reproduction of the infant. In our Western culture, the adaptiveness
of the most extreme form of crying, colicky behavior, may appear paradoxical. By
increasing tiredness and stress in the parents, colic seems more likely to pose a risk
to the survival of excessively crying infants. The infanticide and child abuse litera-
ture often highlights excessive crying as a proximate cause of maltreatment. In this
article, we have not considered colic crying as a typical honest signal, but rather as a
manifestation of the way that the most sensitive and vigorous infants respond to
early caregiving conditions and the relative separateness of the motherinfant
relationship. We suggest, following Barr (1997), that colicky behavior is a nonadap-
tive outcome of evolutionarily novel aspects of modern childcare practices. Colicky
infants appear to be a problem only in modern Western countries. We propose that
the crying pattern of these infants could be affected if caretaking conditions were
modified from the beginning of life to more closely approximate those typical of our
evolutionary past.
It is not clear which of the suggested ecological hypotheses is most plausible.
All of them predict an increase in crying in the absence of parents, although for dif-
ferent reasons (Table 1). Also, it is clear that the hypotheses are not mutually exclu-
sive, as an adaptation often serves multiple purposes. Intensive crying of newborn
infants may signal the emotional stress of physical separation from the mother and
indicate vigor of the child at the same time. A general conclusion appears to be that
signaling of vigor is necessary when parental care is threatened (as perceived by the
child). In addition to the adaptiveness of crying, we stress the honesty of crying as a
signal. Intensive crying by human infants has measurable costs, as noted previously.
If nothing else, it gives a reliable measure of the energy the child can invest in cry-
ing. It seems reasonable to assume that vigorous babies can afford more intensive
crying than less vigorous ones.
An unavoidable difficulty in assessing our ecological hypotheses is the scarcity
of information about the lifestyle of our human predecessors (Foley 1987). For ex-
200

V. Lummaa et al.

ample, opinions concerning lifestyles and modes of parental care among early hom-
inids are by no means uniform. Sinclair et al.s model of hominid bipedalism evolu-
tion as a response to selection pressure for long distance travel has been questioned
(Leutenegger 1987; Verhaegen 1987). Moreover, the use of a few modern hunter-
gatherer societies as representative models of past lifestyles has gained deserved
criticism (Dickeman 1975). However, this does not necessarily change our opinions
concerning past caretaking practices. Many of the features of caretaking practice of
!Kung San parents cluster together in other hunter-gatherer societies. This cluster of
behaviors appears to be a typical primate caretaking pattern, and variants of the
!Kung San pattern apparently are strongly associated with hunter-gatherer modes of
existence (Barr 1997). The pediatric medical literature includes reports about a di-
verse range of disease entities that possibly are associated with excessive crying and
colicky behavior of human infants (reviewed by Miller and Barr 1991 and Gormally
and Barr 1997). In order to demonstrate that intensive infant vocalization should be
understood in terms of its adaptive significance rather than strictly as a medical
problem, future work will require more sophisticated cross-cultural (or historical)
studies assessing especially the potential manipulative or infanticide-inhibiting role of
intensive infant vocalization. Further, when studying the effects of a caregiving en-
vironment on crying patterns, more emphasis should be placed on choosing infants
living in different caregiving conditions from within the same human population. To
date, it has been more usual to compare crying behavior of infants born in totally
different cultural and environmental settings. From such comparisons, it is difficult
to distinguish among several possible reasons for crying differences.

We thank Joachim Bensel, Ingemar Jnssn, Antti Kause, Terho Koira, Daniel Leger, Toomas Tammaru,
the editors, and an anonymous reviewer for their valuable help, comments, and efforts to improve this pa-
per. Financial support was generously provided by the Emil Aaltonen Foundation and Section of Ecol-
ogy, University of Turku (V.L.) and the Louis Sessenwein Trust of the Montreal Childrens Hospital
Foundation (R.G.B.).

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Table 1. Summary of the Hypotheses Explaining Intensive Crying in Human Infants

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