Primates (2007) 48:324–326
DOI 10.1007/s10329-006-0034-x
S H O R T C O M M U N I C A T I O N
A case of infant swapping by wild northern muriquis
(Brachyteles hypoxanthus)
Waldney Pereira Martins Æ Vanessa de Oliveira Guimara˜es Æ
Karen B. Strier
Received: 13 September 2006 / Accepted: 1 December 2006 / Published online: 17 January 2007
Ó Japan Monkey Centre and Springer 2007
Abstract
Allo-parenting has been observed in a
Keywords
Allo-maternal care Á Northern muriquis Á
variety of female primates, and typically infants are
Brachyteles hypoxanthus Á Kin recognition
reunited with their biological mothers assuming that
their mothers are alive. We observed an exception
Introduction
to this pattern when two wild northern muriquis
(Brachyteles hypoxanthus) exchanged infants of dif-
Lactation is known to impose physiological stress, and
ferent sexes and then reared their adopted infants
may reduce survival and future reproductive success
through weaning. The process of this exchange began
for mothers (Altmann 1980; Ko¨nig et al. 1988; Clutton-
when the infants were 4 and 8 days old, respectively.
Brock et al. 1989; Lee 1996). Nonetheless, female
The mother of a 4-day old female carried and nursed
mammals sometimes nurse offspring that are not their
her own daughter and the 8-day old son of a second
own. This behavior has been observed in 68 species,
female. The exchange ended when the second mother
ranging from bats, through carnivores and rodents, to
was first observed carrying the wrong infant 1.5 days
seals (Packer et al. 1992; Roulin 2002). Hypotheses to
later. This observation raises questions about the age
explain why females might nurse offspring other than
and mechanisms of mother–infant recognition in this
their own include misguided parental behavior, reci-
species, and about assumptions of mother–infant
procity, inclusive fitness benefits when the infant is a
relatedness based on behavioral observations alone.
biological relative, evacuation of surplus milk that the
female’s own offspring did not consume, and as prac-
tice or to improve maternal skills (Roulin 2002).
W. P. Martins
Po´s-Graduac¸a˜o em Ecologia,
Kidnapping and adoptions have been reported in
Conservac¸a˜o e Manejo da Vida Silvestre,
some mammals (Riedman and Le Bouef 1982), including
Departamento de Zoologia,
primates (Clarke 1990; Calegaro-Marques and Bicca-
Universidade Federal de Minas Gerais,
Marques 1993; Fortes 2002), and even a cross-genus
Caixa Postal 486, Belo Horizonte,
MG 31270-901, Brazil
adoption has been observed (Izar et al. 2006). We are
e-mail: wpmonkey@yahoo.com.br
not familiar, however, with reports of infant swapping, in
which surviving mothers exchange infants for extended
V. de Oliveira Guimara˜es
periods. Here we report a case of allo-carrying and allo-
Po´s-Graduac¸a˜o em Gesta˜o e Planejamento Ambiental,
Universidade Esta´cio de Sa´, Rua Eduardo Luis Gomes 134,
nursing, and finally infant swapping between two wild
Centro, Nitero´i, RJ, Brazil
female northern muriquis (Brachyteles hypoxanthus).
e-mail: vanessabio@ig.com.br
K. B. Strier (&)
Methods
Department of Anthropology,
University of Wisconsin-Madison, 1180 Observatory Drive,
The observations were made in 2001 while following
Madison, WI 53706, USA
e-mail: kbstrier@wisc.edu
a well habituated group of muriquis that has been
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Primates (2007) 48:324–326
325
studied systematically since 1983 at the 957 ha forest
Table 1 Embraces initiated
Embrace
Time
of
the
Reserve
Particular
Patrimoˆnio
Natural
by BS toward DD while
(24-hour notation)
DD was carrying BS’
(RPPN)-Feliciano Miguel Abdala (previously known
infant on 17 July 2001
as the Estac¸a˜o Biolo´gica de Caratinga), in Minas
1
1139
2
1157
Gerais, Brazil (19°50¢S, 41°50¢W). All group members
3
1222
were fully habituated and accompanied on a near
4
1225
daily basis by trained observers who can recognize
5
1239
individuals by their natural markings (Strier 1999).
6
1247
7
1302
Infants can usually be sexed within a few hours of
8
1331
observation by experienced researchers, but it can
9
1347
take a few weeks before they can be individually
10
1439
recognized when they are apart from their mothers
11
1442
12
1453
unless they have exceptional markings or fur colora-
13
1500
tion at birth.
14
1521
15
1552
16
1632
17
1646
Results and discussion
On 16 July 2001, at 1206 hours, two multiparous fe-
males were observed to descend a tree to drink water
avoidance of extended contact with BS as indicative of
from a stream. One female, identified as DD, was car-
their relative ranks.
rying her 4-day-old daughter, DL, on her ventrum; the
On 18 July 2001, at 0851 hours, both BS and DD
other female, identified as BS, was carrying her 8-day-
were sighted, each carrying one infant. However, it was
old son, BT. When they climbed back up the tree trunk,
immediately clear that their infants had been ‘‘swap-
DD was carrying both infants while BS was carrying
ped’’ because DD was carrying the male BT instead of
none. The moment at which DD acquired BS’s infant
her daughter DL, and BS was carrying DL instead of
was not seen, but no vocalizations or distress calls were
her son BT.
heard while the mothers were out of view so we suspect
We do not know when or how BS re-acquired the
that BT may have crawled onto DD while the two
infant, but based on her persistent efforts the day be-
mothers were drinking alongside one another.
fore we assume that she must have been relieved to
By 1208 hours, both of the infants that DD was
recover a nursing infant after more than 1.5 days of
carrying were observed suckling at the same time, one
milk accumulation. DD may have been equally relieved
from each teat. Throughout the afternoon, BS stayed
to be free of the extra energetic burden that carrying a
within a 2 m radius of DD, although neither of the
second infant had imposed, although it is interesting
females engaged in physical contact with one another,
that she continued to carry both infants instead of
and BS did not appear to be anxious. DD continued
abandoning or relinquishing one to BS sooner.
to carry both infants until observations ceased at
In non-human primates, individual recognition has
1730 hours.
been demonstrated on the basis of visual (Parr et al.
The following day, 17 July 2001, DD was first sigh-
2000), acoustic (Cheney and Seyfarth 1980), and
ted at 0921 hours. She was still carrying both infants.
olfactory cues (Palagi and Dapporto 2006), and kin
At 1139 hours, BS initiated the first observed embrace
recognition among paternal relatives is thought to rely,
with DD since DD began carrying BS’s son. Over the
at least in part, on phenotypic matching (Alberts 1999).
next 5 h, until 1649 hours, BS remained within 2 m of
In our study, however, we could not identify which, if
DD, and initiated a total of 17 embraces with her
any, mechanisms of mother–infant recognition might
(Table 1). During these hugs, BS seemed to be trying
have been operating. Both females continued to carry
to recover her infant, but DD repeatedly terminated
and care for their adopted infants despite ample
the contact by moving away. Given the extra weight
opportunities for both the mother and the infant to
and associated energetic demands of carrying and
correct the error while DD and BS were in proximity
nursing a surplus infant, it is not clear why DD did not
or embracing. This suggests a lack of mother–offspring
relieve herself of BS’s infant at the first opportunity.
recognition, perhaps because of the young age at which
Moreover, the low rates of agonistic interactions and
the exchange occurred. However, we cannot rule out
egalitarian relations among females of this species
the possibility that DD may have deliberately retained
(Strier 1990) make it difficult to interpret DD’s
BT because she preferred to rear an unrelated son over
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326
Primates (2007) 48:324–326
her biological daughter, though why a male infant
E.Veado, J. Gomes, F. Mendes, J. Rı´moli, A.O. Rı´moli, F. Neri,
might be preferred is unclear considering that in mu-
P. Coutinho, A. Carvalho, L. Oliveira, C. Nogueira, S. Neto, W.
Teixeira, R. Printes, and M.Maciel, C.Costa, A. Oliva, L. Dib, D.
riquis, daughters typically disperse from their natal
Carvalho, N. Bejar, C. Damas-Ca¨sar, L. Dias, J.C. da Silva, C. de
groups while sons remain in their natal groups with
Borba Possamai, Regiane R. de Oliveira, F.P. Paim, M.F. Iurck,
their mothers. Also, in contrast to many cercopithe-
K. Tolentino, V. Sousa, D. Guedes, J. Fidelis, F. Tabacow, and
cines and papioines, male muriquis are tolerant toward
M. de Lourenc¸a contributed to the long-term demographic
monitoring of the study group. We also thank Dr. P.C. Lee for
one another’s mating activities and do not compete
helpful comments in her review of an earlier version of this
overtly for rank or priority of access to females (Strier
manuscript.
1990). Consequently, the relative fitness of sons versus
daughters is not clear.
There was no obvious indication that either of the
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Acknowledgments
We thank the Brazilian government and
Strier KB (1990) New world primates, new frontiers: insights
CNPq for permission to conduct research in Brazil, Se´rgio L.
from the wolly spider monkey, or muriqui (Brachyteles
Mendes for his collaboration, E. Veado for providing logistical
arachnoides). Int J Primatol 11:7–19
support, and J.C. da Silva and J. Gomes for their help in the field.
Strier KB (1997) Mating preferences of wild muriqui monkeys
The field work was funded by grants to K.B.S. from the Liz
(Brachyteles arachnoides): reproductive and social corre-
Claiborne and Art Ortenberg Foundation, the National Geo-
lates. Folia primatol 68:120–133
graphic Society, the Margot Marsh Biodiversity Foundation, and
Strier KB (1999) Faces in the Forest: The Endangered Muriqui
the Graduate School of the University of Wisconsin-Madison.
Monkeys of Brazil. Harvard University Press, Cambridge
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Document Outline

• A case of infant swapping by wild northern muriquis (Brachyteles hypoxanthus)
  • Abstract
  • Introduction
  • Methods
  • Results and discussion
  • Acknowledgments
  • References

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