SOCIAL ORGANIZATION AND BEHAVIOR
Troop size is variable, but a general trend follows that groups are larger in
semideciduous habitats and smaller in evergreen areas. Also, group size
variation at a single site over extended periods of time is comparable to that
between different habitats (Crockett & Eisenberg 1988). In one thirty-year
study, troop size averaged annually between 6 and 10.5 individuals but could be
as small as 4 individuals and as large as 18 (Rudran & Fernandez-Duque
2003). The group sizes reported by Rudran & Fernandez-Duque approximate the
range of group sizes that are found in the wild between study sites (see
Crockett & Eisenberg 1988 and Chapman & Balcomb 1998 for lit reviews).
Photo: Roy Fontaine
Group composition can be either unimale or multimale up to (rarely) 6 males.
Multimale groups are usually larger than unimale groups and average 2.2 adult
males however both types of groups have comparable numbers of adult females.
Among the adults, there are more females than males in the population and per
group there are usually 2 or 3 adult females within a range of 1 to 4 (Soini
1986; Crockett & Eisenberg 1988; Rudran & Fernandez-Duque 2003). All
adult males in a group are dominant to all group females (Neville et al. 1988).
There are never more than four breeding females in a group (Crockett 1996).
Within multi-male groups there is a hierarchy of males, with an alpha male
dominant to the other males in the group as well as being the only male within
the group that is able to reproduce (Kimura 1997; Pope 1990; Crockett 2003).
The alpha male is usually physically larger than the subordinate group males and
challenges of alpha male status by other males can be violent and result in
injuries to one or both parties (Rudran personal communication cited in Jones
1983; Izawa 1997a; Kimura 1997). Breeding males will not leave a group
voluntarily and only leave if forced by challengers (Pope personal communication
cited in Jack 2003). When first established, groups are usually unimale (Crockett 1996; Rudran
& Fernandez-Duque 2003).
Both sexes of red howlers emigrate from their natal troops, but in different
proportions. Around 70-80% of females will breed outside of their natal group
while for males the figure is 98% (Crockett 1996). If a female breeds within a
group, she will remain in that group for the rest of her or the group's life
(Pope 2000). Females rarely are able to integrate into established troops and
must form new troops while males are usually able to join existing troops, often
by challenging resident males with another non-group male (Crockett 1984;
Crockett & Pope 1993; Crockett 1996; Crockett 1998b; Pope 2000). Indeed,
males are usually not able to join or invade an established group without the
help of another male individual, often a relative (Pope 1990; Agoramoorthy &
Rudran 1993). Over half of males disperse before or at sexual maturity
(Agoramoorthy & Rudran 1993).
Solitary females are actively prevented from joining established groups by
group females and as a result, non-troop females have a relatively high rate of
physical injuries (Rudran 1979; Sekulic 1982a; Crockett & Pope 1988). As a
result, females must emigrate farther than males to establish new groups while
males are able to join existing groups, often adjacent to their natal group
(Pope 2000). In addition, after emigration from the natal troop, a significant
amount of time can be spent solitary (Crockett 1996). Most females emigrate
from their natal group between 2-4 years old while males emigrate between 4-6
years old (Crockett & Pope 1993).
Vocalization by a howler group is common in the early mornings and serves to
discourage other howlers who are not members of a group from approaching over
the course of the day (Sekulic 1982c). If a different group or troop approaches
over the course of the day, usually in areas of home range overlap, males will
coalesce and begin roaring, joined soon after by the group females (Sekulic
1982d; Crockett 1998b). Both groups will then face one another for a time and roar, but not
chase, for a time and then begin to rest (Sekulic 1982d).
Rates of allogrooming vary widely between groups and individuals. Allogrooming is infrequent
and of short duration and primarily serves social purposes (Sánchez-Villagra et al. 1998).
Rates of physical injuries resulting from aggression among red howlers is
high, with over a third of individuals in one study population exhibiting scars and
physical injuries from encounters with other red howlers (Crockett & Pope
1988). However, rates of actual aggressive behaviors are quite low, even if
they can be quite violent when they do occur (Crockett 1984). Agonistic
conflicts between males most often elicit piloerection, throat-rubbing, growling
and roaring from those involved (Sekulic 1982d).
Red howlers are best described as having a single or multi-male polygynous
breeding system in which in the multi-male troops, the dominant male has almost
exclusive breeding access to troop females (Crockett & Rudran 1987b; Pope
1990; Kimura 1992). However, following infanticide and male status changes
within a troop, females will mate with several males (Crockett 2003). In
addition, extra-group copulations have been observed in which females mate with
the dominant male of a neighboring group in addition to the dominant male of
their group (Agoramoorthy & Hsu 1999). Often, females must emigrate from their natal groups because
of competition between females for breeding position. In fact, only around 20% of females will
breed in their natal groups and the others emigrate, either to found new troops,
join existing troops, or simply disappear (Crockett 1998b). Females may emigrate because larger female
group size may be attractive to infanticidal males (Crockett and Janson 2000).
Solicitation and copulatory behavior can consist of tongue-flicking,
genital-sniffing and inspection, and genital and body licking (Izawa &
Lozano 1989; Agoramoorthy & Hsu 1999). Copulation is short in duration, and
the male mounts the female from behind, as if covering her (Izawa & Lozano
1989). In one study, copulations within a group were common, and occurred on
average once every three hours (Sekulic 1982a).
Photo: Roy Fontaine
Red howler monkeys do not breed in a strictly seasonal fashion; however there
are consistent, annual dips and peaks in births. In semi-deciduous habitats in
Venezuela, a reduction but not cessation in births is seen early in the wet
season and among troops a synchrony of births is sometimes observed (Crockett
& Rudran 1987a). Similarly, in evergreen tropical forests in Peru, breeding
occurs year-round but with fewer births in June-September and most between
October and April (Soini 1986).
Females first give birth at around 4 or 5 years of age while males usually do
not father offspring until they are around 7 (Crockett & Rudran unpub cited
in Crockett & Eisenberg 1987; Crockett 1998b). Average gestation length in
wild red howler monkeys is 191 days (6.3 months) (with an inter-birth interval
after a surviving infant of an average of 517.1 days (17.0 months) (Crockett
& Sekulic 1982; Crockett & Rudran 1987b). Based on hormonal studies,
estrous cycle length is estimated at 29.5 days (.97 months) (Herrick et al.
2000). Estrous is sometimes externally visible in females, although the
indications are often only slight and unreliable in addition to being variable
between individuals (Crockett & Sekulic 1982; Sekulic 1982a).
Births in red howlers occur at night and during the day and usually it takes
only one or two minutes for the mother to give birth. Shortly after
parturition, the mother will consume the placenta (Sekulic 1982b). The newborn
infant is tiny, and is born with eyes closed and pale hair (Izawa 1997a). In
general, group females both adult and immature spend a lot of time near infants,
and dominant males spend more time than other group males near new mothers and their infants than other
group males (Sekulic 1983b).
Adoption is documented in the species with wild kin, group and non-group
females having adopted abandoned infants or the infants of others, and in some
cases nursing and raising them until weaning (Izawa 1989; Agoramoorthy &
One of the most marked features of red howler ecology is the prevalence of
infanticide by males which significantly raises infant mortality in the species.
Infanticide occurs in two contexts in the red howler, during invasions of a
group by external males and during breeding status changes among resident males
(Crockett & Sekulic 1984; Agoramoorthy & Rudran 1995). Infanticide in
this and other howler species is proposed to be the result of sexual selection and
shortens the inter-birth interval of a female (Crockett 2003). According to Crockett (2003),
there is less evidence supporting the hypothesis that infanticide is related to food
competition within a group (Agoramoorthy & Rudran 1995). Often, females attempt to resist infanticide
but are not usually successful. After the death of an infant, a female will
usually conceive 1-3 months later and solicit copulations as soon as one week
after the death of a previous infant (Crockett & Sekulic 1984; Agoramoorthhy
& Rudran 1995). In one study, overall mortality was about 20% in the first year
and more than 44% of infant mortality was attributable to infanticide (Crockett & Rudran 1987a).
Red howler mothers overall give the impression of only vague or passive
interest in their infants however they will groom them and actively defend them
from threats (Neville 1972b). For the first month after birth, the
infant is carried ventrally by the mother, after which, it will ride on the
mother's back (Mack 1979; Soini 1986). During both ventral and dorsal carrying,
the infant will wrap its tail around the base of the mother's tail (Mack 1979;
Izawa & Lozano 1992). During group movement until the fourth month, ventral
carrying occasionally is still used. Up to four months old, the infant remains within 2
meters (6.6 ft) of the mother but in the fifth and six months, more time is
spent away from the mother. During the fifth and six months, the occurrence of
carrying is limited to nursing and travel and by the seventh through ninth
month; the infant is carried less than a quarter of the time (Mack 1979). In
the second month, quadrupedal movement and use of the prehensile tail is first
seen and by month four, adult locomotion is attained and the infants will move
about on their own (Mack 1979; Soini 1986). Independence, but not weaning, occurs between seven or
eight months of age (Izawa & Lozano 1992). Males either never or rarely
carry infants (Mack 1979; Soini 1986). Play with adults is also rare and
usually occurs between the infant and other infants or juveniles. However, in
general, group members, especially females, are very interested in the infant
and spend a lot of time near them (Mack 1979; Sekulic 1983b). Most weaning occurs between 10.5 and 14 months
(Crockett & Pope 1993). Nursing can persist into the 17th or 18th month of age, especially while resting (Mack 1979).
Photo: Roy Fontaine
Vocal communication in howler monkeys is highlighted by its loud calls, the
"roars" or "howls" from which the genus gains its common name (Drubbel &
Gautier 1993). The loud calls are amplified by a large hyoid that resonates
vocalizations as part of a specialized vocal apparatus that allows the species
to produce single roar emissions for as long as 8 seconds (Sekulic & Chivers
1986; Schön Ybarra 1988). Loud calls have been classified into two general
types by different researchers, either "barks" and "roars" or "short" and "long"
calls (Schön Ybarra 1986; Drubbel & Gautier 1993). "Barks" are
typically short, harsh, and low-pitched vocalizations, often uttered in
syllables or rhythms. "Roars" are very loud, low-pitched, long calls which are
uttered together with other group members and can be heard up to a kilometer
away (Schön Ybarra 1986). While roaring mostly occurs in the morning
(timing highly variable, but as early as 169 minutes before dawn), it also
occurs during the night and over the course of the day as well (Schön
Ybarra 1986; Sekulic 1981; 1982c; 1983a; Sekulic & Chivers 1986). Roaring
is usually heard in encounters with non-group individuals, especially when they
are visible, and may repel males from other troops that might try to enter
the group (Sekulic 1981; 1982d). In addition, roaring is heard in intra-group
situations as well (Sekulic 1982d). Experimental evidence hints that female
howling serves to incite male competition (Sekulic 1983a). Soft growlings are heard
during feeding and play (Crockett pers. comm.)
Except for howling, the species is surprisingly silent, but the species does
have a canon of other vocalizations (Defler 2004). Aggressive vocalizations
include the "incipient roar", the "roar accompaniment" and the "oodel." The
"male woof", "female woof" or "bark", "incipient woof"and the "whimper" are
heard when disturbed. Infant vocalizations are the "eh", the "squeeking hinge",
the "infant bark", and the "purr" (Defler 2004). Other vocalizations include
the "nGot", heard before howling in a threatening sense and the "ngut", a tense
vocalization (Izawa 1997a).
Throat-rubbing has been observed in wild red howlers. This is apparently
scent-marking and is usually performed on a large branch or tree trunk in which the
animal moves its throat back and forth for several minutes. Male red howler
monkeys throat-rub at higher rates than females and in most cases, the behavior
is associated with hostility with other red howlers and sometimes is accompanied
by howling and piloerection (Sekulic & Eisenberg 1983). There are throat
glands in both sexes which points to a scent-marking role in muzzle and chin
rubbing (Epple & Lorenz 1967 cited in Neville et al. 1988). Other marking
activities include the rubbing of the anus on a branch after defecation, the
rubbing of the muzzle and the beard on branches, back rubbing, and communal
defecation (Braza et al. 1981; Defler 2004).
Red howlers use several visual signals. Sexual signals are tongue flicking
and lip smacking. Aggressive and agonistic signals are back-arching,
lip-pursing, and genital displays. When alarmed, they will branch-shake and
yawn. To show submission, red howlers crouch (Defler 2004).
Content last modified: November 26, 2007
Written by Kurt Gron. Reviewed by Carolyn Crockett.
Cite this page as:
Gron KJ. 2007 November 26. Primate Factsheets: Red howler (Alouatta seniculus) Behavior . <http://pin.primate.wisc.edu/factsheets/entry/red_howler/behav>. Accessed 2014 July 28.