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Contexts of rubbing behavior in Alouatta guariba clamitans a scent-marking role.

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American Journal of Primatology 70:575–583 (2008)
RESEARCH ARTICLE
Contexts of Rubbing Behavior in Alouatta guariba clamitans:
A Scent-Marking Role?
ZELINDA MARIA BRAGA HIRANO, ISABEL COELHO CORREA, AND DILMAR ALBERTO GONC- ALVES DE OLIVEIRA
Centro de Pesquisas Biológicas de Indaial, Departamento de Cieˆncias Naturais, Universidade Regional de Blumenau,
Blumenau, Brazil
Rubbing behaviors are well known in several primate species and are usually seen as scent-marking
behaviors, with several functions proposed but still widely debated. The genus Alouatta is highly
sexually dimorphic and a suitable subject for the study of sexual and hierarchical divergences associated
with rubbing behavior: males should mark more than females, and dominant individuals more than
subordinate ones. Three wild groups of Southern brown howler monkeys, Alouatta guariba clamitans,
were studied at Morro Geisler, Indaial, Brazil, from September 2004 to February 2005. One hundred
and twenty-three rubbing episodes were registered; data on performers and associated contexts showed
that anogenital, dorsum and hyoid regions were the most often rubbed. Adult males rubbed
significantly above expected levels, whereas subordinated females and juveniles tended to rub below
the expected levels. Females were the main performers of anogenital rubbing, often preceded by
defecation. The predominance of rubbing in males probably serves an important function in intrasexual
communication and social interactions. Intrasexual competition can also lead to a relationship between
rubbing and social status in females. Hyoid and sternum rubbing by males are probably agonistic
signals associated with extragroup conflict. The possible cleaning function of anogenital rubbing does
not preclude a communicative function. Whether rubbing behavior in howlers is solely for the function
of scent marking or can also be a visual signal (e.g. as a display or to color the substrate with pigment)
c 2008 Wiley-Liss, Inc.
requires further study. Am. J. Primatol. 70:575–583, 2008.
Key words: Alouatta guariba; marking behavior; hierarchy; territoriality
INTRODUCTION
Rubbing is a well-known behavior in many
mammalian species, including primates, in which a
scent-marking function is frequently assumed, as
body surfaces used in rubbing usually have skin
glands with a putative odoriferous function [Epple,
1986]. Rubbing as a scent-marking mechanism is
most studied in strepsirrhines and platyrrhines
[Epple, 1986; Heymann, 2006], primate groups in
which both multiple skin glands and functional
accessory (vomeronasal) olfaction are found [Evans,
2006]. Chemical analyses have been carried out on
primate scent marks, indicating the potential for the
identification of species, sex, reproductive status and
even individual signatures [Hayes et al., 2004; Smith,
2006].
Mammalian scent-marking behavior is usually
related to territorial and social functions. A territorial role is assumed when marking behavior is related
to intergroup encounters and home range boundaries, with marks used to signal the use of resources
or area by a group [Gorman, 1990; Mertl-Millhollen,
2006]. However, when home ranges are so large as to
preclude group members from the effective marking
of boundaries, territorial marking can predominate
r 2008 Wiley-Liss, Inc.
in core areas [‘‘hinterland marking’’: Gorman, 1990;
Heymann, 2000]. Social functions of skin glands are
either related to hierarchic signaling, with dominant
individuals using marks to reinforce their status over
subordinates [Miller et al., 2003; Ralls, 1971;
Walraven & van Elsacker, 1992], or sexual signaling
[Di Fiore et al., 2006; Epple, 1986; Heymann,
2003a,b, 2006; Setz & Gaspar, 1997] or both
functions.
In Neotropical primates, rubbing behavior is
well known, and a direct relationship between social
rank and rubbing frequency has been found in some
species [Kleiman & Mack, 1980; Miller et al., 2003;
Contract grant sponsor: CNPq; Contract grant number: 305372/
2002-5; FURB.
Correspondence to: Zelinda Maria Braga Hirano, Centro de
Pesquisas Biológicas de Indaial, Departamento de Ciências
Naturais, Universidade Regional de Blumenau, Rua Antônio da
Veiga, 140, 89102-900 Blumenau, SC, Brazil.
E-mail: bugio@furb.br
Received 2 July 2007; revised 5 December 2007; revision
accepted 13 January 2008
DOI 10.1002/ajp.20531
Published online 5 March 2008 in Wiley InterScience (www.
interscience.wiley.com).
576 / Hirano et al.
Rylands, 1990; Walraven & van Elsacker, 1992].
Sexual selection plays a role in platyrrhine scent
marking, as there is a general trend for the sex
having the lesser degree of parental care to mark
more, which is associated with a greater level of
intrasexual competition [Heymann, 2003a, 2006].
Additionally, the rubbing behavior of Neotropical
primates may be related to an intersexual signaling
function [Di Fiore et al., 2006; Setz & Gaspar, 1997],
although a territorial function is still controversial
[Gosling & Roberts, 2001; Heymann, 2000, 2006].
The described patterns of rubbing behaviors in
Alouatta are assumed to serve scent-marking functions [Neville et al., 1988]. Of these behaviors, throat
rubbing is usually associated with conflicts, as in
intergroup encounters in Alouatta seniculus [Sekulic
& Eisenberg, 1983]. Anal rubbing has been linked to
social signaling in A. seniculus [Braza et al., 1981].
Neville [1972] observed dorsal, perineal, chin, facial
and neck (throat) rubbing modes in A. seniculus, but
judged these behaviors to be more likely just
scratching. Shoemaker [1979] noticed the same
behaviors in captive A. caraya of all ages and both
sexes and considered hygienic and marking functions
to be equally possible. Eisenberg [1976], studying
captive A. palliata, considered chin and chest
(sternum) rubbing to be a male behavior associated
with high arousal, whereas anogenital rubbing to be
a female behavior without a clear context. He also
described a ‘‘back-roll’’ behavior that resembles
dorsal rubbing, relating it as possible artifact of
captivity. Altmann [1959] also observed genital
rubbing in females of this species and suggested that
it could be considered masturbation. However, neck
and chest rubbing by a former solitary male A.
palliata was associated with changes in his social
status—access to females and group membership
[Young, 1982]. Clearly, most forms of rubbing in
Alouatta have not been systematically studied and
are still poorly understood.
Other forms of chemical communication in
Alouatta involve urine washing and sniffing in
A. palliata [Eisenberg, 1976; Jones, 2003; Milton,
1975] and anogenital sniffing and licking in
A. palliata [Altmann, 1959; Eisenberg, 1976] and
A. seniculus [Neville, 1972]. Anogenital investigation
was observed to be a behavior performed by both
sexes [Eisenberg, 1976] or just by males [Altmann,
1959; Neville, 1972].
Some authors also considered the acts of
collective defecation in howlers as a likely scentmarking behavior, related to territoriality [Braza et
al, 1981; Emmons & Feer, 1990; Shoemaker, 1979].
Recent research indicates that howler monkeys
have fully functional vomeronasal sensory organs,
being genetically able to perceive pheromones [Webb
et al., 2004]. Even so, responses to pheromone
signals are no longer considered to be exclusively
dependent on vomeronasal structures, but are also
Am. J. Primatol.
believed to be perceived by the main olfactory
epithelium, and the integration between both systems enhances the associative and learning capacities related to chemical communication in
mammals [Brennan & Zufall, 2006]. Therefore, there
is a wide potential for chemosignaling in Alouatta.
As howlers are highly sexually dimorphic animals, we hypothesize that sexual divergence in
rubbing activity can be predicted. Males should be
the main performers, according to Heymann’s [2006]
schema, as they are the most competitive sex. If a
hierarchical function is served by howler’s rubbing
behavior, dominant individuals should mark more
often than subordinate ones. We can also test
hypotheses of associations between some forms of
rubbing and particular contexts, based on what has
been previously described in howlers. Therefore, we
examine whether rubbing occurs principally in the
context of intergroup conflict, particularly when the
hyoid (throat) region was used, and we explore the
possibility that anal rubbing is linked to defecation.
To test these hypotheses, we investigated rubbing behavior in three wild groups of A. guariba
clamitans. Specifically, we focused on individuals
performing rubbing behavior, body parts rubbed and
the contexts of rubbing behavior.
METHODS
Study Site
This research was conducted at Morro Geisler, a
forested hill located at (261540 S, 401130 W) in Indaial,
Santa Catarina State, in Southern Brazil. It is a
40 ha fragment of essentially secondary growth
forest that is part of the Atlantic Rainforest.
Deforestation occurred at this site approximately
60 years ago, and it contains some ancient remnant
trees and several clearings occupied by bamboo,
grasses, lianas and chayote (Sechium edule). Height
varies from 80 to 285 m above sea level. The research
area is connected by forest corridors to neighboring
hills still covered by similar forest as part of the hilly
surroundings of the Itajai-Ac- ú River Valley.
Subjects
The Southern brown howler monkey, A. guariba
clamitans, is the only primate species at Morro
Geisler, albeit the tufted capuchin monkey, Cebus
nigritus, is also a member of the native fauna of the
region and can occur in neighboring areas. The local
population of howlers is estimated at 30–40 individuals, with at least six groups known in the area.
Three groups, named Huebes, Pedreira and Licurana, were observed from September 2004 to February 2005. The composition of the groups and the
changes that occurred in these groups are given in
Table I. In the two groups with two adult females,
one (AF1) was probably dominant to the other (AF2)
Rubbing Behavior in Howlers / 577
TABLE I. Composition of Study Groups at Morro Geisler
Adult male
Huebes
Pedreira
Licurana
Population
a
1
1
1
3
Adult female
1
2
2
5
Subadult male
Juvenile
a
1
1
2
Infant
1
2
3
1
1b
1
1–3
Total
3–4
4–5
7
14–16
Born in October 2004.
Born in January 2005.
b
based on larger body size and the predominance of a
leading position in group progression. The single
female in the Huebes Group was also denominated as
AF1. Each group was followed 12 hr/day for 2–4 days/
month. Thirty-two complete days of observation
were obtained as follows: Huebes Group, 13 days
(September 2004–January 2005); Pedreira Group, 15
days (September–December 2004, February 2005);
Licurana Group, 4 days (January–February 2005).
Rubbing Behavior
All rubbing behavior episodes (repeated contact of any body part on a substrate) were recorded
[‘‘all occurrences’’ sampling method; Altmann,
1974]. These episodes constituted single acts of
rubbing by a subject. When other individuals
rubbed at the same time, or the same individual
rubbed another body part, it was considered as
another episode. For each episode the following
data were registered: hour; performer; body part
rubbed (hyoid, mandible, dorsum, abdomen, sternum, anogenital region); substrate (vertical trunk,
branch); context preceding the episode (intergroup
conflict, defecation, play, locomotion, rain, feeding,
grooming, vocalization, movement in the forest,
researcher’s approach, no apparent reason); context after the episode (same as the previous ones);
position of performer (sitting, lying on back,
ventral contact, suspended by tail); body reactions
of performer (piloerection, none); looking direction
(other group members, human observers, other
howler group or no target identified). To preserve
mutual exclusivity of context categories, rain was
considered as a context only when any other
context category was not observed.
Statistical Analysis
The data were compiled into contingency tables
and analyzed by Pearson’s w2 tests. When a
significant result was found (a 5 0.05), the standardized adjusted residuals [STAR; Agresti, 2002] of
each cell in a table were calculated, to show which
differences were responsible for the significance.
When w2 calculations involved a single column, the
simpler adjusted residuals [AR; Agresti, 2002] were
calculated. For an a 5 0.05, residual values higher
than 1.96 indicate a frequency significantly greater
than that expected in the cell; values lower than
1.96 indicate a frequency significantly below the
expected one. As multiple tests are done within a
single contingency table, false significant results
could occur just by chance. To prevent type I errors
(incorrect rejection of the null hypothesis 5 false
positive), a Bonferroni-like correction was made in
multiple comparisons within each contingency table.
The a level is recalculated with a 5 0.05/N, where N
is the number of cells in the contingency table.
Therefore, a critical modular value for residuals was
calculated in each w2 table, corresponding to the
corrected a-value, and denominated as critical
residual (CR). Residual values above positive CR or
below negative CR were considered significant.
We calculated the expected frequencies of rubbing episodes by each sex–age category from the
number of individuals within each category in the
three groups and from the time (number of days)
spent with each group.
Fisher exact tests were performed to show any
associations between the most frequent forms of
contexts (intergroup conflict and defecation) and the
kind of rubbing most frequently associated with each
context (respectively, hyoid rubbing and anogenital
rubbing).
A w2 test of adherence was used to test the
hypothesis that rubbing in intergroup conflicts
diverged from the expected. The time spent in
intergroup conflicts by focal groups was divided by
total time of observation to provide the expected
proportion. Intergroup conflict duration was measured as the time from the beginning of the first loud
call emission between the focal groups and other
groups to the end of the last emission, in any series of
successive emissions involving the same groups with
less than 1 hr of interval between consecutive
emissions. Other signs of intergroup conflicts, such
as chasing and physical aggression, were not
observed in this study.
This study is in compliance with animal
care regulations applicable in Brazil. All research
protocols reported in this article were reviewed
and approved by the Ethics Committee on Animal
Experimentation of the Regional University
of Blumenau at Blumenau, Brazil (Ethics Committee
on Animal Experimentation protocol number
016/04).
Am. J. Primatol.
578 / Hirano et al.
TABLE II. Rubbing Episodes According to Body Part Rubbed in Three Groups at Morro Geisler
Hyoid
Sternum
Anogenital
Dorsum
Abdomen
Mandible
Total
5
4
1
4
2
1
29
24
0
30
10
5
2
3
0
3
0
0
73
43
7
10
7
53
45
5
3
123
Huebes
Pedreira
Licurana
Total
TABLE III. Percentage of Rubbing Episodes (n 5 123) According to Body Part in Groups at Morro Geisler
Hyoid
Sternum
Anogenital
Dorsum
Abdomen
Mandible
Total
AM
AF1
AF2
SM
JU
6.5
0.0
0.0
0.0
0.8
4.9
0.8
0.0
0.0
0.0
13.0
11.4
4.9
9.8
4.1
15.4
8.9
1.6
8.9
1.6
1.6
1.6
0.0
0.0
0.8
1.6
0.8
0.0
0.8
0.0
43.1
23.6
6.5
19.5
7.3
Total
7.3
5.7
43.1
36.6
4.1
3.3
100.0
AM, adult male; AF1 and AF2, adult females; SM, subadult male; JU, juvenile.
RESULTS
One hundred and twenty-three episodes of
rubbing behavior were recorded for the three howler
groups at Morro Geisler (0.32 episode/hr). The data
by group are summarized in Table II, with the
Huebes Group comprising 59.5% of the rubbing
events observed, followed by Pedreira Group (34.7%)
and Licurana Group (5.8%). The anogenital region
was the most often rubbed (43.1%), followed by the
dorsum (36.6%) and hyoid (7.3%). Adult males
performed rubbing behaviors more often than other
group members, with 43.1% of records (Table III).
The adult females were second (30.1%), followed by
subadult males (19.5%) and juveniles (7.3%). The
proportion that each sex–age category performed
rubbing varied significantly (w2 5 24.5, df 5 3,
Po0.001), with significant residuals (N 5 4,
CR 5 2.50) for adult males performing above the
expected (AR 5 3.59) and juveniles performing below
the expected (AR 5 2.67). Dominant females performed most female rubbing episodes (AF1 5 23.6%,
AF2 5 6.5%), and the separation of female data into
these two categories also results in significant
variation in rubbing between sex–age categories
(w2 5 26.5, df 5 4, Po0.001), and adds a negative,
but not significant residual to AF2 (AR 5 2.23,
N 5 5, CR 5 2.58), indicating that subordinate
females tend to rub below the expected.
Adult males were the main performers of dorsal,
hyoid and sternal rubbing, whereas adult females
were the main performers of anogenital rubbing
(Table III). Other forms of rubbing behaviors were
infrequent, preventing a global analysis of rubbing
according to body part rubbed in relation to sex–age
categories. However, a partial analysis of this table,
limited to the most frequent performers (adult males
Am. J. Primatol.
and females) and body parts rubbed (anogenital,
dorsum and hyoid1sternum), showed a significant
difference in the body parts most used by each sex
(w2 5 10.5, df 5 2, Po0.01). The residuals (N 5 6,
CR 5 2.64) indicated a significantly greater amount
of hyoid and sternal rubbing by adult males
(STAR 5 7.92) and a significantly greater amount of
anogenital rubbing by adult females (STAR 5 3.20).
Hyoid and sternal rubbing were grouped together in
this analysis as they are usually performed by adult
males and occur in similar contexts (see below).
Substrate Rubbed
Howlers only rubbed on tree branches (horizontal substrates) or tree trunks (vertical substrates). In
113 recordings of rubbing behavior, the tree part
rubbed was identified, and branches represented
59.3% of these records. The difference in the use of
these two substrates was not significantly different
from equality (binomial test, P40.05), but anogenital rubbing was more asymmetrical, with 36 records
on branches and 12 on trunks.
Position While Rubbing
Rubbing behaviors were most frequently
performed while howlers were in sitting postures
(51.5%), followed by rubbing behaviors in ventral
lying positions (33.3%), upright postures (13.1%) and
while hanging by the tail (2%).
Body Reactions by Performers
The only corporal reactions observed in howlers
performing rubbing behaviors were piloerection
(11 episodes), sneezing (one episode: sternum rubbing by the adult male in Licurana Group) and rump
Rubbing Behavior in Howlers / 579
TABLE IV. Contexts Preceding Rubbing Episodes According to Body Part Rubbed in Groups at Morro Geisler
Hyoid
Sternum
Anogenital
Dorsum
Abdomen
Mandible
Total
Intergroup conflict
Defecation
Play
Movement in the forest
Rain
Feeding
Grooming
Locomotion
Vocalization
Researcher’s approach
No apparent reason
4
1
0
1
0
1
0
0
0
0
1
3
1
0
0
0
1
0
0
0
0
1
0
39
0
1
0
0
0
0
0
2
4
6
5
1
4
6
1
2
2
1
0
7
0
1
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
1
0
13
47
1
6
6
3
2
2
1
4
14
Total
8
6
46
35
3
1
99
TABLE V. Contexts After Rubbing Episodes According to Body Part Rubbed in Groups at Morro Geisler
Hyoid
Sternum
Anogenital
Dorsum
Abdomen
Mandible
Total
Intergroup conflict
Defecation
Movement in the forest
Locomotion
Rain
Feeding
Grooming
Vocalization
No apparent reason
3
0
0
1
0
0
0
0
2
3
0
0
1
0
0
0
0
2
0
13
0
3
0
2
0
0
11
6
3
1
5
4
0
2
2
5
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
12
16
1
10
4
2
2
2
21
Total
6
6
29
28
1
0
70
elevation in relation to performer’s forepart (one
episode: hyoid rubbing by the adult male in Huebes
Group). Piloerection was most frequent in hyoid
(four records) and dorsal (three episodes) rubbing
episodes.
Contexts
Contexts preceding and after rubbing behaviors
are given, respectively, in Tables IV and V. A large
number of rubbing behaviors occurred in undetermined contexts. The relationship between preceding
extragroup conflicts with hyoid and sternum rubbing
showed significant results (hyoid: Fisher test,
Po0.01; sternum: Fisher test, Po0.05), indicating
that these forms of rubbing behavior are significantly associated with intergroup encounters when
compared with other rubbing modes. Intergroup
conflicts accounted for 2% of the time spent with
howler groups. The w2 test of adherence showed an
overall frequency above the expected of rubbing
preceded by intergroup conflict (w2 5 59.2, df 5 2,
Po0.001). The same pattern was found for hyoid
rubbing alone (w2 5 90, df 5 2, Po0.001) and hyoid
plus sternum rubbing (w2 5 157.6, df 5 2, Po0.001).
A significant positive relationship also was found
in the frequency of anogenital rubbing behavior
during both the period preceding and the period after
defecation (Fisher test, Po0.001, in both cases). We
noted two observations of anogenital rubbing in the
Pedreira Group after we had completed data collection for this study. In both episodes, the performer
adult female engaged in copulatory behavior with the
resident adult male of her group soon after anogenital rubbing.
Dorsal rubbing was the only form of rubbing
associated with rainfall, being also associated with
other contexts. The only possible overmarking
episode observed occurred after the study period
and involved dorsal rubbing by the adult female and
subadult male in Huebes Group along with a
recently emigrated adult female. During group
progression initiated by the subadult male, he was
observed to rub against a tree trunk immediately
upon arrival at the tree. He then continued his
travel. This rubbing behavior was similarly performed by the resident female and the emigrant
female, respectively. The resident female was seen
directing agonistic behaviors to the newcomer
female, who spent most of the time on group
Am. J. Primatol.
580 / Hirano et al.
periphery, only coming close to the adult male. The
subadult male always had been closely associated
with this resident female. Later the emigrant female
copulated with the resident male and achieved
resident status, staying at normal distances from
other group members.
Looking Direction
In most rubbing episodes the performer’s sight
was not clearly directed to any identified target. In
six intergroup encounters the adult male looked at
the other group or specifically at an adult male in the
other group (five rubbing records in Huebes Group
and one in Pedreira Group: three with hyoid, three
with sternum). Looks directed at birds of prey are
responsible for two successive observations in the
Huebes Group, with the subadult male rubbing first
his anogenital region, and then his dorsum while
facing the birds.
Responses
Responses to rubbing, such as licking and
sniffing, were not observed in this study. Besides
the above-mentioned overmarking in Group Huebes,
we observed responses to scent marks in captive
animals at CEPESBI; but as they are individually
housed, these were directed to their own marks.
Adult males, when rubbing with their region or chin,
sometimes salivated, scratched their wet muzzles or
sniffed the substrate they had rubbed.
DISCUSSION
In this study, adult male brown howler monkeys
at Morro Geisler were found to be the main
performers of rubbing behavior. If rubbing serves a
scent-marking function, then our observations are
consistent with sexual selection theory that predicts
that the sex characterized by a greater level of
intrasexual competition marks at a greater
frequency [Heymann, 2003a, 2006]. The greater
frequency of hyoid and sternum rubbing by males
is in agreement with this pattern as these forms of
rubbing are considered agonistic signals in howlers
[Sekulic & Eisenberg, 1983], and our data suggest
this function, with an apparent relationship between
this form of rubbing and intergroup encounters.
Given the low number of rubbing bouts, short study
period and small number of subjects in our study, the
function of rubbing in Alouatta still requires
additional study.
In addition, we found evidence of status-based
differences in rubbing behavior. Males are the main
performers of rubbing and also the dominant sex,
whereas among females, the dominant ones tended
to rub more than the subordinates. A clear relationship between social rank and frequency of rubbing
has been described in several primate studies [Epple,
Am. J. Primatol.
1986; Kleiman & Mack, 1980; Rylands, 1990;
Walraven & van Elsacker, 1992]. Heymann [2003a,
2006] concluded that sexual selection is probably the
main driving force in the evolution of scent-marking
behavior in Neotropical primates, leading to a
sexually biased-marking behavior. However, he
could not rule out intrasexual competition in both
sexes as an important factor, leading to individual
variation in marking related to intrasexual
hierarchy. We note that most studies of rubbing
in platyrrhines (regarded as scent-marking behavior)
have involved studies of callitrichids. Howlers,
with very distinct ecological and life-history patterns, may show different trends from those seen in
callitrichids.
Anogenital rubbing is strongly associated with
defecation, which points to a cleaning function for
this behavior. Braza et al. [1981] verified that
A. seniculus rubbed trunks and branches after
defecation, leaving a characteristic odor on the
substrate that could act as a scent mark. So, a
cleaning function does not necessarily preclude a
marking one for anogenital rubbing in howler
monkeys. Urine can have a marking function [Jones,
2003; Milton, 1975], and it is possible that feces also
have this function as they have a strong, characteristic scent in howlers [Emmons & Feer, 1990; Epple,
1986]. Both urine and feces are used as territorial
and/or resource defense markers in strepsirrhines
[Irwin et al., 2004] and in other mammals [Brashares
& Arcese, 1999; Gorman & Trowbridge, 1989; OwenSmith, 1975]. In this regard, anogenital rubbing
associated with urination and defecation can spread
(non-skin-gland) odoriferous signals onto a substrate.
Urine and vaginal secretions also can signal
reproductive status of females [Dixson, 1998], and
males can directly sniff females’ anogenital area as
well as anogenital marks to verify their reproductive
condition [Eisenberg, 1976; Neville, 1972]. In Lagothrix lagotricha, female anogenital marking is
significantly related to reproductive behavior
[Di Fiore et al., 2006]. Two episodes of anogenital
rubbing by an adult female in the Pedreira Group
were followed by copulations, which is consistent
with such a reproductive signaling function.
Hyoid and sternum rubbing seem to be associated with intergroup encounters, and could serve
both agonistic and territorial functions. Heymann
[2000, 2006] found little support for a territorial
function in platyrrhine scent-marking behavior, but
his analysis grouped distinct forms of marking that
could attend very different functions. Other authors
have long maintained that there is a territorial
function for primate-marking behaviors [Gosling
& Roberts, 2001; Mertl-Millhollen, 2006], as seen in
other mammals [Gorman, 1990]. Although howler
monkey groups do not have exclusive use of their
home ranges, they display behaviors that serve to
Rubbing Behavior in Howlers / 581
defend the use of an area or of resources (including
sexual partners) from neighboring groups, particularly their intense loud calls [Neville et al., 1988;
Sekulic, 1982; Whitehead, 1987, 1989]. Hyoid and
sternum rubbing also can be used this way, and
Sekulic and Eisenberg [1983] observed that hyoid
rubbing (‘‘throat rubbing’’) was usually associated
with a hostile reaction toward conspecifics in
A. seniculus, including intergroup encounters. The
presence of piloerection in some episodes of hyoid
rubbing also suggests an aggressive motivation by
the performer. Young [1982] observed hyoid and
chest rubbing by a solitary adult male of A. palliata,
peripheral to his study group, after this male
copulated with group females. Some time latter he
attained group membership, becoming dominant.
Our findings reveal that rubbing is probably an
important form of marking behavior that can serve
several functions depending on the context, form and
individual performing this behavior. Our data show
some support for the fact that rubbing plays an
important role in intersexual and intrasexual dominance interactions, including aggressive and territorial behavior. Functions probably vary according to
the body part used. However, the low number of
episodes observed makes us cautious about greater
generalizations, and all trends viewed here must
await confirmation by larger sampling of individuals
and increased numbers of observations.
The absence of easily to interpret responses by
group members or extragroup individuals to rubbing
makes it difficult to identify a clear function for this
behavior. Neville [1972] also failed to observe direct
investigation of rubbed substrates by other howler
group members. He concluded that rubbing behaviors were most likely mere scratching, without a
communicative function. In our view, some apparent
associations of rubbing with particular contexts
pointed to communicative functions. Even in callitrichids most marking events do not lead to
responses by other individuals [Heymann, 1998].
The single overmarking response, observed in
Huebes Group, can only be speculatively interpreted:
the dorsal rubbing observed could be a dominance/
agonism display in this context, directed to the
emigrant female, who in turn responded in the same
manner.
Further studies should differentiate among the
functions of several kinds of rubbing behaviors.
Particular attention must be given to variation
among individuals in distinct sex–age classes and
with different social statuses. This will serve to
clarify the social dynamics involved in rubbing
behavior and its relationship with howler monkeys’
social systems. Howlers of both sexes compete for
group status and membership [Jones, 1980; Pope,
2000], but the expression of competition is usually
not overt, being highly dependent on subtle signals
[Jones, 1983; Neville et al., 1988]. Thus, the study of
rubbing behavior can offer greater understanding of
howler monkey communication.
Finally, we need to ask whether howler monkeys’ rubbing behaviors could also be visual signals.
Marking behaviors can contain both olfactory and
visual signals [Mertl, 1976; Sauther et al., 1999]. A
scent-marking function for rubbing behavior does
not exclude a visual-marking one, as well as other
forms of visual displays. Heymann [2001] examined
whether scent marking in tamarins could act as a
means of visual signaling by analyzing the proximity
of other group members during scent marking. He
found that the number of occurrences with two or
more individuals being close to the signaler was
above the expected. As these behaviors in howlers
can be clearly observed by the human researchers
from several meters away, their execution can surely
act as visual displays on their own, or drive attention
to the odor signals left. The mentioned absence of
clear olfactory responses to surfaces rubbed by
howlers may indicate that the visual components of
this behavior are more relevant than the olfactory.
Pigment releasing glands are present on brown
howlers’ skin [Hirano et al., 2003]. These glands
were identified in regions of the throat, groin and
lower jaw of adult males, and had coiled tubular
secretory portions adjacent to the hair follicles in the
dermis. Secretory granules were noted, which produced a secretion similar to the pigment released by
the animals. These structures are probably differentiated sweat glands, being larger and having more
secretory units and apical cells in the secretory
epithelium. Similar, but less-developed structures
have been found in juvenile and female individuals
[Hirano, 2004]. The development of these glands into
their differentiated form in adult males is probably a
secondary sexual trait stimulated by the action of
sexual hormones during puberty. In at least
three field episodes (and in several observations in
captivity), we observed that rubbing behaviors left
definite colored pigment markings on tree trunks.
These color patches may guide an individual in
locating a spot where another howler has left a scent
mark. These findings suggest that lasting/non-instantaneous visual signals can enhance the olfactory
communication associated with rubbing behaviors.
Judicious field observations and well-designed field
and captive experiments with discrete stimuli [Dugmore et al., 1984; Mertl, 1977] can shed light on the
presumed functions and mechanisms associated with
rubbing behaviors. Substrates marked by distinct
body regions and stimuli (estrous non-estrous
female urine, dominant subordinate individuals,
male female,
familiar outgroup
individuals)
should be used. Visual function and color discrimination can be assessed through colored marks left on
substrates of distinct background (from lighter to
darker), and combined with and without associated
odors, to test for attractiveness of color marks.
Am. J. Primatol.
582 / Hirano et al.
ACKNOWLEDGMENTS
We thank Patricia Izar, Paul Garber and two
anonymous reviewers for their helpful comments.
Eugene Harris assisted with careful English revision.
Our thanks go to all the students and personnel at
CEPESBI (Indaial Biological Research Center) who
helped us with data gathering at Morro Geisler. We
also thank the support from the University of
Blumenau (FURB) and from the Municipality of
Indaial. This study was supported by grants from
CNPq (RD grant to D. A. G. O., process number
305372/2002-5) and FURB. This study is in compliance with animal care regulations and applicable
Brazilian laws.
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