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Brief communication Self-suckling in Barbary macaque (Macaca sylvanus) mothers before and after the death of their infant.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 140:381–383 (2009)
Brief Communication: Self-Suckling in Barbary Macaque
(Macaca sylvanus) Mothers Before and After the Death
of Their Infant
Bonaventura Majolo* and Richard McFarland
Department of Psychology, University of Lincoln, Brayford Pool, Lincoln, LN6 7TS, UK
KEY WORDS
culture; emotion; grief; lactation; maternal behavior; predation; prolactin; stress;
animal tradition
ABSTRACT
We report here self-suckling in four wild
female Barbary macaques (Macaca sylvanus), living in
two troops (i.e. ‘‘Flat face’’ and ‘‘Large’’ troop) in the middle-Atlas Mountains, Morocco. The four females lost
their infants due to predation or for unknown causes.
Self-suckling was observed before and after the infants
died in the four females living in the ‘‘Flat face’’ troop.
When the infants were still alive, self-suckling was of
short duration and it was probably a method to improve
milk flow when the infant switched from one nipple to
the other. After the infants died, self-suckling lasted sig-
nificantly longer and the females were apparently drinking their own milk. Self-suckling was never observed
among the four lactating females in the ‘‘Large’’ troop
(including one monkey who lost her infant) and it could
thus represent a cultural difference. Moreover, self-suckling after the death of an infant may be explained by the
energetic and immunological benefits that a monkey
may gain from drinking their own milk. Finally, selfsuckling may have a stress-releasing effect on the mothers who have lost their infants. Am J Phys Anthropol
140:381–383, 2009. V 2009 Wiley-Liss, Inc.
The death of a lactating infant results in various physiological and behavioral changes in the mother. For
example, prolactin plays a key role in parental behavior
and functions to stimulate mammary glands to produce
milk. Given that prolactin is stimulated by suckling, its
level in the blood drops significantly when a female loses
her infant and stops lactating (Ziegler, 2000). The
decrease of prolactin following the death of an infant
results in a concomitant increase in various ovarian
hormones, on which prolactin has an inhibitory role
(Dixon, 1998). These physiological changes favor the
resumption of sexual activity of the mother. Indeed,
depending on the timing of the death (e.g. whether or
not it is close to the mating season, for seasonally-breeding species), a female who has lost her infant may
resume estrus within a few days. Resumption of sexual
activity is considered the main function of infanticide
attacks (van Schaik and Janson, 2000) but can also occur
after deaths due to predation or illness. Conversely, for
deaths due to food shortage the resumption of estrus is
often delayed until food availability has improved
(Loudon et al., 1983).
Mothers who have lost their infants tend to reduce the
time they spend feeding due to the fact that they do not
have the burden to feed and carry their infant (Altmann,
1980). Together with these hormonal and behavioral
changes, the death of an infant may have dramatic
emotional consequences for the mother. For example,
Altmann (1980) observed a baboon mother carrying and
gently touching the body of her dead infant, in an apparent attempt to make it stand up, for some time before
eventually leaving it. Similar observations have also
been reported in other species, including gorillas,
chimpanzees, and elephants (Schaller, 1963; van LawickGoodall, 1968; Moss, 2000). These sparse and anecdotic
observations suggest that various species may react
emotionally to the loss of an infant. The emotional
response that animals experience following the death of
a relative or close companion might thus be evolutionarily linked to grief in humans (Archer, 1998). However,
data so far indicate that animals, including chimpanzees, lack the conceptual level necessary to understand
death (Allen and Hauser, 1991).
Here we report the behavior of five Barbary macaque
(Macaca sylvanus) mothers in the weeks preceding and
following the death of their infants. Data presented in
this study are part of a longitudinal project, started in
January 2008, on the socio-ecology of wild Barbary macaques living in the middle-Atlas Mountains, Morocco.
Four females were living in a group (i.e. ‘‘Flat-face’’
group) composed of 30 monkeys at the beginning of the
study (11 adult/sub-adult males, 8 adult/sub-adult
females, 6 juveniles, and 5 infants). One female was
living in another group (i.e. ‘‘Large’’ group) composed of
19 adult/sub-adult males, 10 adult/sub-adult females,
12 juveniles, and 4 infants. None of the females were
primiparous as suggested by the size of their nipples
before giving birth. The two study groups relied
completely on natural food and were living in cedar and
oak forest near the city of Azrou (35870 N, 238310 E).
C 2009
V
WILEY-LISS, INC.
C
Grant sponsor: University of Lincoln.
*Correspondence to: Bonaventura Majolo, Department of Psychology, University of Lincoln, Brayford Pool, Lincoln, LN6 7TS, UK.
E-mail: bmajolo@lincoln.ac.uk
Received 31 March 2009; accepted 22 May 2009
DOI 10.1002/ajpa.21125
Published online 9 July 2009 in Wiley InterScience
(www.interscience.wiley.com).
382
B. MAJOLO AND R. MCFARLAND
TABLE 1. Details of the study females, their infants, and on the occurrence of self-suckling
Female
Troop
name
Date when infant
died or disappeared
Last day
self-suckling observed
N days observed
self-suckling
Date when first
seen in consorta
Jessica
Laura
Tabby
Amy
Pam
Flat face
Flat face
Flat face
Flat face
Large
15/07/2008
14/10/2008
14/10/2008
14/10/2008
08/09/2008
29/10/2008
31/10/2008
12/11/2008
19/11/2008
–
106
11
22
30
–
21/10/2008
17/11/2008
12/11/2008
12/11/2008
15/10/2008
a
The mating season lasted from 20th October to around 13th January 2009.
The infants of these five mothers all died before the
onset of the mating season (see Table 1). No other infant
was left in the ‘‘Flat-face’’ troop following these deaths.
However, three infants remained in the ‘‘Large’’ troop.
The infant living in the ‘‘Large’’ troop was caught and
killed by a Berber dog (Canis lupus familiaris). In the
‘‘Flat-face’’ troop one infant was seen dead and its
mother (Jessica, see Table 1) was observed to carry her
dead infant for 6 h before eventually leaving it. The
other three infants disappeared and we did not find their
body or any remains. These infants did not show any
sign of malnutrition or wound when last seen nor was
their death temporally linked to any conspicuous social
event, such as the immigration of a new male or group
fission. As such, we are unable to assess the cause of
death of the infants with the exception of the monkey
caught by a dog.
While their infants were still alive, the four mothers
in the ‘‘Flat-face’’ troop (see Table 1) were observed to
display what we define as self-suckling. That is, they put
the right or left nipple in their mouth while apparently
suckling milk. This behavior was of very short duration
(lasting a maximum of 2 s) and it was consistently
observed immediately before the mother switched her
infant from one nipple to the other. For example, a
female who was feeding her infant would put her free
nipple in her mouth for 1 s and then move her infant to
that same nipple. We interpret these short self-suckling
bouts as a way to improve/stimulate milk flow through
the nipple and thus to facilitate feeding the infant. All
the four females in the ‘‘Flat-face’’ troop practiced selfsuckling after their infants’ death. Of course, this
behavior was no longer linked to infant suckling. More
importantly, the duration of each self-suckling bout was
much longer than when the infants were still alive, lasting from 10 s up to 2 min of consecutive self-suckling.
Females displayed self-suckling two to five times per day
and for several consecutive days (i.e. 42.3 6 21.6 mean
days 6 SE; see Table 1) after their infants’ death. One
female (Jessica, who was observed carrying her dead
infant; see above) displayed self-suckling for 106 consecutive days before stopping. The lactating female in our
second study troop (‘‘Large’’ troop) was never observed
self-suckling before or after her infant’s death. The same
was true for the three females whose infants survived in
the ‘‘Large’’ troop (see above). Finally, all five females
were observed consorting and engaging in sexual activity
during the mating season. However, there was no or limited overlap (Table 1) between the end of self-suckling
and the resumption of sexual activity. In summary, selfsuckling lasted significantly longer after the females had
lost their infant, was observed only in one of our two
study troops and was temporally distinct from sexual
behavior during the mating season.
American Journal of Physical Anthropology
While allo-suckling (i.e. a female nursing an infant
that is not her own) has been reported in several mammals (Packer et al., 1992), to our knowledge self-suckling
has only been previously observed in chimpanzees
(Matsumoto-Oda, 1997) and feral goats (O’Brien, 1982).
Our study is, however, the first observation of this
behavior before and after an infant’s death and on more
than one animal. Because of its timing and occurrence
we suggested above that self-suckling when the infant
was still alive is a method to improve milk flow.
Suckling from the nipple stimulates milk production
(Dixon, 1998) and this may be the reason why self-suckling was observed for several days after the infants died.
Both self-suckling and milk production stimulate the
release of prolactin that in turn inhibits the resumption
of estrus in the mother (Loudon et al., 1983; Dixon,
1998). Self-suckling and sexual activity were temporally
distinct in two females and overlapped for no more than
9 days in the other two females. Moreover, the female
who displayed self-suckling significantly longer than the
others (i.e. Jessica; Table 1) had lost her infant 3
months before the start of the mating season. This might
suggest a negative relationship between self-suckling
and resumption of sexual behavior.
Self-suckling (both before and after the infant death)
was only observed in one of the two study troops. Selfsuckling may thus be a troop-specific behavior and be
considered some sort of habit or cultural behavior (Avital
and Jablonka, 2008). If this is the case, self-suckling
may not have any specific adaptive function but simply
be transmitted across females through imitation or social
learning.
Together with viewing self-suckling as a cultural
behavior, four additional and nonmutually exclusive
functional explanations may be proposed for self-suckling displayed after the infant’s death. First, self-suckling could be a way to regain the energetic content of the
produced milk. This explanation is not adaptive as the
energetic balance between milk production and self-suckling may still be costly for a female (Clutton-Brock et al.,
1989). However, self-suckling and milk production might
constitute a self-reinforcing system that a female is
‘‘unable’’ to stop even though it may bear negative fitness consequences (e.g. milk production or delayed
resumption of sexual activity). Second, self-suckling
could be a mechanism to reduce pain by relieving
engorged breasts (Roulin, 2002). This mechanism would
explain self-suckling at the proximate level but it does
not solve the question of why females are affording the
energetic cost of milk production. A third explanation is
related to the immunological benefits that a female
would gain from prolactin release through self-suckling.
Prolactin improves immuno-competence in the lactating
mother and also milk immunology (Yu-Lee, 1997; Roulin,
SELF-SUCKLING IN THE BARBARY MACAQUE
2003). Self-suckling could thus be beneficial as it would
allow the female to not waste and regain the immunological components she has produced and released in
the milk. Finally, self-suckling could be related to the
emotional consequences of losing an infant. We know
from studies on both humans and animal models (e.g.
rats) that breast-feeding reduces stress and that this
effect is modulated by prolactin (Fischer et al., 1995;
Groer et al., 2006). We may therefore speculate that the
stress releasing function of self-suckling may be particularly beneficial for a monkey who has lost her infant,
given that this loss seems to be stress inducing in various animal species (Archer, 1998). This stress-releasing
function does not require taking into account any energetic benefit that the female may gain (or regain)
through self-suckling. Indeed, stress-releasing factors
may drive primate behavior even when these factors
differ from energetic benefits. For example, infant rhesus macaques separated from their mothers spend more
time attached to a surrogate nonfeeding cloth mother
than to a wire mother furnished with a milk dispenser,
as the former is considered to give emotional security
and stability through physical contact (Harlow and
Harlow, 1962).
In conclusion, self-suckling may be driven by a
combination of cultural, physiological, energetic, and
emotional factors. The hypothesis that self-suckling is a
cultural behavior is supported by the fact that this
behavior has only been observed in one of our study
troop and never, to our knowledge, in any zoo or park.
All the other four functional hypotheses are to some
extent maladaptive, as self-suckling cannot balance the
cost of milk production, but they may be explained by
self-reinforcing
mechanisms.
The
stress-releasing
function is potentially the most beneficial for the female
emotional state.
ACKNOWLEDGMENTS
The authors are grateful to Professor Mohammed
Qarro (Ecole Nationale Forestière d’Ingénieurs, Morocco)
for his support in the field and for research permission.
They thank Professor Harriet Gross, Dr. Ruff and two
anonymous reviewers for useful comments on the MS.
This study complies with Moroccan and UK regulations
regarding the ethical treatment of research subjects.
383
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American Journal of Physical Anthropology
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