Consequences of Joint-Territoriality in a Mixed-Species Group of Tamarin Monkeys

Author(s): Carlos A. Peres

Source: Behaviour, Vol. 123, No. 3/4 (Dec., 1992), pp. 220-246
Published by: BRILL
Stable URL: http://www.jstor.org/stable/4535071
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 Behaviour123 (3-4) 1992, E. J. Brill, Leiden

CONSEQUENCES OF JOINT-TERRITORIALITY IN A
MIXED-SPECIES GROUP OF TAMARIN MONKEYS

by

CARLOS A. PERES1,2)
(Museu Goeldi, Departamento de Zoologia, Cx. Postal 399, Belem, Para 66.040, Brazil)

(With 5 Figures)
(Acc. 16-XII- 1992)

Summary

Groups of saddle-back (Saguinusfuscicollis) as moustached tamarins (Saguinus mystax) in a

western Amazonian forest jointly defended home ranges larger than 100 ha, which were
held in common throughout the year. Resources were defended by direct exploitation in
extensive areas shared with other groups, or through intensive and frequent intergroup
interactions along territorial boundaries. These interactions were expressed primarily
during intergroup encounters, and affected the use of space, movements, time budget, and
foraging success of tamarins. During encounters, animals of both species spent more time in
energetically costly activities, such as rapid travel and intergroup chases, and less time in
energetically positive activities, such as feeding and foraging. In addition, foraging success
per unit of foraging effort within overlapping areas of the range periphery was lower than in
exclusive areas of the range centre, particularly for saddle-back tamarins. The time and
energy allocated by moustached tamarins to boundary contests was considerably greater
than that of saddle-backs, despite the fact that only the latter species increased its foraging
efficiency by shifting from exclusive areas in the group's range to those shared by other
groups. This is probably because of saddle-back's greater use of depletable food supplies,
such as small fruit patches and small microhabitats containing embedded prey items. These
benefits are likely to justify the substantial amount of time and energy invested in territorial
defence for both saddle-backs and moustached tamarins, but appeared to be highly asym-
metric between species.

Introduction
Interspecific territoriality can occur between individuals of different spe-
cies (heterospecifics) defending space against one another (e.g. ORIANS &

l) Present address: Center for Tropical Conservation, Duke University, Simons Building,
3705-C Erwin Road, Durham, NC 27705-5015, U.S.A.
2) This study was supported by World Wildlife Fund-US grant 6199. I wish to thank the
Brazilian oil company (Petrobras) for logistical support in the upper Urucu. I am grateful to
Andrew JOHNS,Yarrow ROBERTSON, Robin DUNBAR,David CHIVERS, and one anonymous
reviewer for providing helpful comments on earlier drafts of the manuscript. Mr. K. HAGAN
kindly wrote two Fortran programs used in the analysis. My studies at Cambridge University
were funded by the Brazilian Science and Technology Council (CNPq).
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 221

WILLSON,1964; REED, 1982), or between mixed-species groups sharing a

territory, and jointly defending it against other similar mixed-species
groups (MUNN& TERBORGH,1979). Under resource-limited conditions,
associated heterospecifics should segregate to a certain extent (e.g.MAY,
1974). Yet joint-territorialityshould be expected to occur more frequently
in stable mixed-species groups, because low interspecific overlaps in
spatial and resource requirementsshould increase the costs, and decrease
the benefits of forming and defending a common territory. It should also
be more likely to occur in species sharing a renewing food supply (WASER,
1981), because in this case asynchronoususe of resourceswould decrease
foraging efficiency, even if the number of consumersremained unchanged
(CODY, 1971; DAVIES & HOUSTON, 1981).
That spatial priority of access to resources, or exclusion of neighbour-
ing competitors, entails a trade-off, is a well-establishedand tested propo-
sition (e.g. GILL& WOLF, 1975). Resources should not be defended unless
the benefits of doing so are greater than the costs (BROWN,1964; BROWN
& ORIANS,1970). Costs of territorial defence often equate to high ener-
getic expenditure and decreased foraging success associated with agonis-
tic interactionswith non-residents, or overexploitationof peripheralfood-
supplies shared by neighbours (PATON & CARPENTER, 1984; PERES, 1989).
On the other hand, this frequently results in the exclusion of non-resi-
dents from an area, which denies them access to resources. This increases
the local availability of food to territorial residents, which constitutes a
common benefit of territoriality (GILL, 1978).
It has been argued that the enhanced cooperative defence of a common
territory is an important benefit of mixed-species associations, whether
they may be between primates (TERBORGH,1983, 1984), birds (MUNN &
TERBORGH, 1979), or coral-reef fish (ROBERTSON et al., 1976). For
instance, a permanent mixed-species group of guenons in Gabon pro-
gressivelyincreased its range size over a 5-year period to the detriment of
a neighbouring monospecific group (GAUTIER-HION
et al., 1983). How-
ever, studies of mixed-species societies have implied, or failed to tests the
underlying assumption, that different species holding a common territory
equally share the costs and the benefits of territorialdefence (e.g.MUNN&
TERBORGH, 1979; TERBORGH, 1983, 1984). Costs are likely to differ if, for
instance, different species invest different amounts of time and energy in
territorialcontests, or if in doing so, one species becomes more vulnerable
to predators than others. The benefits derived by different species from
resource defence also need not be symmetric, particularlyif spatial over-
lap between neighbouring mixed-species groups affects the distribution
222 CARLOS A. PERES

and availability of each species' food supply in different ways. For

instance, the consequences of range exclusion for two species using differ-
ent-sized food patches should differ, because small patches are more
limiting, and more depletable, than large patches.
In this paper I investigate the joint-territorial behaviour of two small-
bodied primate species the Avila-Pires saddle-back tamarin (Saguinus
fuscicollis avilapiresi) and the red-capped moustached tamarin (Saguinus
-
mystaxpileatus) resulting from their highly stable mixed-species associa-
tions (PERES,1991, 1992). Possible costs and benefits of resource defence
are examined in terms of (1) energetic investments allocated to territorial
interactions, and (2) increased foraging success derived from range exclu-
sion of neighbouring groups. Two mechanisms of resource competition
(PARK,1954) are identified. Interference competition occurs when contes-
tants decrease one another's access to resources via direct aggressive
interactions, which are often highly conspicuous. Exploitative competi-
tion occurs when competitors, which need not take part in direct contests,
deny one another's access to a common resource supply by directly
depleting it (e.g. DAVIES & HOUSTON, 1981; PATON & CARPENTER, 1984;
PERES, 1989). Mixed-species groups of tamarins compete with other
groups by interference primarily during intergroup encounters, and by
exploitation when foraging within extensive home range areas shared by
other groups. Comparisons between different contexts of intergroup
interactions are used to examine the effects of interference on tamarins'
time budgets, use of space, and foraging success. Comparison between
exclusive and overlapping areas in the home range are used to examine
the consequences of exploitative competition of these same parameters.

Methods

Study area and animals.

This study was conducted at an entirely undisturbed, low land (53-71 m a.s.l.) tropical
moist forest, located 4 km inland from the upper Urucu river, Amazonas, Brazil (4°50'S,
65°16'W). This site appears to be representative of vast expanses of yet inaccessible and
poorly known unflooded (terra firme) forests in remote regions, which account for 95% of
the Amazon basin. Most of the 900-ha study plot of high forest was located within a refined
11 5-km2 trail grid which had been created and then abandoned by a seismic company, but
habitat disturbance and selective hunting had never taken place (PERES, 1991). Mean
annual rainfall in this plot was 3256 ± 589 mm (N = 2 full years).
Thirteen primate species occur at this site, including the saddle-back tamarin (adult
weight - 394 + 42 g, N = 17), and its larger-bodied congener, the moustached tamarin
(adult weight = 523 ± 70 g, N = 6). These two tamarin species consistently formed and
maintained highly stable heterospecific groups during 97% of their activity period through-
out the year (PERES,1991, 1992). Monospecific groups occurred at a density of 1.78 groups/
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 223

km2, maintained a very stable membership throughout the year, and consistently associated
with the same group of the other species, with which they shared a perfectly congruent
home range of approximately 150 ha (PERES,1991).

Behaviouralsampling.

Systematic observations were conducted on habituated groups of both tamarin species

during 5-7 days in each of 14 consecutive months (August 1988-September 1989), when
groups were followed continuously, and located every 10 and 15 min throughout their daily
activity period. Data reported here are based largely on one study group (hereafter, main
group) of 5-8 saddle-backs (2-3 adult males, 1 adult female, 0-1 subadult male, 0-2 subadult
females, and 0-2 infants or juveniles) and 8-10 moustached tamarins (3-5 adult males, 1-2
adult females, 1-2 subadult males, 0-2 subadult females, and 0-2 infants or juveniles)
observed during 106 days. On 76 of these days I was certain whether none, one, or more
intergroup encounters had occurred. Locations and activities of 5 other groups, whose
home ranges partially overlapped that of the main group, were also noted whenever
possible. These groups became individually recognizable primarily because of the distinc-
tive patterns of ear-scars of adult moustached tamarins.
Behavioural data consisted of scan samples (ALTMANN,1974) obtained every 10 min
throughout the day from all visible animals of both species in the group, but I strived to
sample individuals of all age-sex classes during each group of scans regardless of their
behavioural differences. Behavioural patterns were divided into the following broad, mutu-
ally exclusive categories: (1) move, (2) rest, (3) feed (on plant-items), (4) forage (for animal
prey), (5) within-group and (6) between-group social interactions. These data were recorded
in the same fashion during and outside intergroup encounters to allow behavioural compar-
isons. The time encounters began and terminated, and thus their duration, was also noted.
The foraging success of each tamarin species was examined by considering the animal
component of their diet. Captures of animal prey, such as a wide range of orthopterans,
involved clearly identifiable foraging patterns which were distinctive between species
(PERES, 1992). Scans of individuals performing a foraging maneuver (e.g. pounces, snatches,
lunges, swipes, manipulations) were prolonged for up to 10 sec to allow me to quantify
whether or not such capture attempts yielded a successful outcome. Capture success is then
defined per foraging effort (i.e. the number of prey items obtained per unit of foraging scan),
and per foraging maneuver (i.e. the proportion of prey capture attempts which actually
resulted in successful captures). For these purposes, therefore, capture attempts which
resulted in undetermined outcomes were disregarded. The prey capture success of each
species were then compared between different contexts of intergroup interactions, and
between different parts of their home range.
A combination of contiguous 0.92-ha quadrats used exclusively by the main group is
defined as an exclusive area, whereas overlapping areas refer to quadrats shared with other
groups. Encounter quadrats were those occupied during direct intergroup encounters.
These were located in the periphery of each group's home range, were not necessarily
centred around key food sources such as food trees, but were used consistently throughout
the year by any two neighbouring groups. Approach quadrats are defined as those near the
range periphery, and were used primarily when groups moved towards, or withdrew from,
one another shortly before, and shortly after a given encounter.
Centrality is defined as the straight-line distance between any given quarter-hour loca-
tion and the geometric centre of the group's home range. Centrality distances were
computed by a Fortran program for each 0.058-ha quadrat occupation record based on
their x, y intersection, and that of the home range centre. Because home range geometry
can affect the congruence between centrality distances and proximity to boundaries, the
average distance from the home range centre to territorial boundaries (c) was evaluated as a
224 CARLOS A. PERES

function of range eccentricity (E), which ranges from zero (in a perfect circle), to one (in an
infinite straight line). Home range shape has essentially no effect on 'c' unless it is highly
eccentric (E > 0.9: MITANI& RODMAN,1979). The study group's range eccentricity was,
however, very low (E = 0.33), suggesting that results obtained from centrality analysis were
robust with respect to range shape.

Statistical analysis.

Non-parametric statistics follow SIEGEL(1956). Two-sample Kolmogorov-Smirnov and

Mann-Whitney U-tests were used to examine differences between two observed distribu-
tions, and other continuous variables. Categorical data were analysed using log-likelihood
ratio tests (G-tests: SOKAL& ROHLF,1981), and X2 tests. I follow BROWN(1974) in examining
cell contributions to overall X2 values. Activities which contributed the most to x2 values
were examined by replacing observed numbers of records with those expected from null
spatial or temporal contexts. Cells were not considered significant if the exchange of their
observed values resulted in a decrease of the overall X2 to less than the critical X2 value at p
= .05 (e.g. BROWN,1974).
There appeared to be little temporal dependency in the data sets used here, partly
because not all individuals of each species in the group were observed during single 10-min
intervals, and activities were not necessarily synchronous between conspecifics. For
instance, when comparing greatly asymmetric sample sizes, medium frequency scores of
activities from 10 randomly subsampled data sets, which approximately matched that of the
smaller data set, were not more than 1% different from their respective proportions in the
entire original samples. It was thus possible to control for unrealistically inflated signifi-
cance levels due to unequal sample sizes.
Three-way contingency tables were based on log-linear models (SOKAL& ROHLF,1981),
and used to test for interactions between categorical variables, and their effects on a
frequency variable, such as the number of scans in different activities or successful prey
captures. For instance, the spatial heterogeneity of capture success was tested by examining
the effects of location of capture attempts, and tamarin species attempting a capture, on
whether captures were successful or not. Because prey capture attempt could have only two
outcomes, frequencies of foraging scans and capture maneuvers were incorporated into the
model as dichotomous variables defined by whether they resulted in successful captures.
Distance from capture location to the range centre was assigned to one of seven centrality
zones, and fitted as a categorical variable. Logistical regression models were then used to
test for differences in estimated probabilities of prey captures by tamarins in different
centrality zones. Tamarin species and centrality zone were fitted as covariates of captures
success. Whether or not coefficients were equal to zero were then tested by the Wald
statistic (SOKAL & ROHLF, 1981), which follows a X2 distribution.
When comparing encounter days with days in which encounters did not occur, I used an
analysis of covariance (ANCOVA) on each dependent variable using one or more indepen-
dent variables. In every case, the slope heterogeneity was tested before testing for differ-
ences in the intercept. All data were analysed using SPSSx (NIE et al., 1975).

Results
Patterns of intergroup interactions.
Two contexts of interactions between neighbouring mixed-species groups
are distinguished: long-range and face-to-face encounters. Long-range
encounters were defined by intergroup distances of 40 m or more, and
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 225

were characterized by frequent exchange of long-calls between groups.

The frequency of counter-calling increased as neighbouring groups
approached one another, which invariably escalated to a direct inter-
group contest, or face-to-face encounter. These disputes were defined by
short intergroup distances (< 40 m), when conspecifics of different groups
usually remained within sighting distance of one another, maintained
very high levels of aggression, and exchanged frequent long-calls, which
often fused into staccatos of short whistles, or 'chatter' calls (sensuPERES,
1986). Aggressive interactions and postures included piloerection,
arching displays (sensuRATHBUN, 1979), vigorous chases, and occasionally
actual fights. Chases often involved reciprocal displacements between
conspecifics of each group along boundaries, often resulting in rapid back
and forth travel by the entire group. Fights occurred when a chaser
caught up with its opponent, were characterized by explosive and vig-
orous wrestling, and could result in biting wounds. Aggressive inter-
specific interactions between members of neighbouring groups were never
observed. Encounters eventually terminated as neighbouring mixed-spe-
cies groups 'lost interest' and drifted apart towards the respective centres
of their home ranges.
Face-to-face encounters accounted for 9% of the main group's overall
time budget (N = 731 h). These tended to begin early in the day (0835 h 9
min, N = 39), last over one hour (74 ± 64 min, N = 39), and terminate by
mid-morning (0949 h ± 2 h 5 min, N = 39). On certain days, however,
tamarins allocated as much as 60% of their waking time (e.g. 356 min of a
589-min day) to long-range and face-to-face encounters. Although such
unusually prolonged encounters lasted until midday or early afternoon,
68.5% of time spent in encounters took place before 0930 h (Fig. 1), and
those beginning after 0930 h were more likely to last for shorter periods (rs
= -0.41, p = .01, N = 39).
All group members of both tamarin species were present in all face-to-
face encounters. Such encounters occurred almost every other day, and
were observed in 39 (51%) of 76 days spread equally over the 14 months
in which the occurrence of encounters was determined. The total number
of encounters in this period was actually 42 because double-encounters
with distinct neighbouring mixed-species groups occurred in 3 of the 39
encounter-days. In an additional 8 days, long-range encounters led to
intergroup approaches within 150 m, which atypically failed to escalate
into actual face-to-face encounters. There were no between-month differ-
ences in the observed number of intergroup encounters. In fact, monthly
frequencies of encounters were very similar to that expected on the basis
226 CARLOS A. PERES

f I 21
Jg 7 -n=/o aays

6 7 8 9 10 11 12 13 14 15 16

mixed-species
tamar-s. group of

.80). mixed-species group of tamarins.

Patterns
of of intergroup
observation number of complete days, X2 = 5.8, 12 df, p >
effort (e.g. spacing.
.80).

Patterns of intergroup spacing.

A total of 5 mixed-species groups of tamarins had home ranges contig-
uous or partially overlapping with that of the main group. There was a
large spatial overlap between the home range of all neighbouring groups
and that of the main group (Fig. 2); 163 (76.2%) of 214 quadrats of 0.92-
ha in the group's range were known to be used by at least one other
group. Despite this large overlap, the main group still retained an exclu-
sive area of 50.7 ha.
Areas of overlap appeared to be stable throughout the study, and
encounters between any two groups appeared to occur consistently within
the same encounter quadrats. As expected, areas occupied during face-to-
face encounters were biased towards the range periphery (Fig. 2). Central-
ity distances during encounters averaged 602.8 + 133.8 m (N = 221), and
where thus significantly longer than those at other times (437.1 ± 179.3, N
= 2046; Kolmogorov-Smirnov, Z = 7.6, p < .001).
Mixed-species groups of tamarins were never observed to change the
direction of their movements to avoid intergroup encounters. Rather,
they appeared to move towards the location of neighbouring groups as
soon as their long calls were heard. If movements of neighbours were
independent of one another, the probability of simultaneous visits to the
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 227

Type of quadrat
* Encounter
H Approach
| Overlap
D[ Exclusive

Fig. 2. Home range of the main mixed-species group of tamarins divided into 0.92-ha
quadrats. Encounter and approach quadrats were those where face-to-face encounters, and
intergroup approaches took place, respectively. Overlapping quadrats were those shared by
other groups, but where encounters did not take place. Exclusive quadrats were those used
only by the main group.

same encounter quadrats should be low. The observed tendency of

mixed-species groups to approach and collide with one another was thus
tested against that expected from WASER'S(1977) random movement
model (see also WASER& WILEY, 1979). This model generates an expected
frequency of encounters on the assumption that groups move indepen-
dently of each other as in a 'two-dimensional gas'. Expected daily encoun-
ter frequency (/ is thus defined as:
f= 8 p a (d+s)/7,
228 CARLOS A. PERES

where 'p' is the density of mixed-species groups (per km2); a is the average
group velocity (km/day); 'd' is the criterion distance at which an encoun-
ter is said to occur; and 's' is the average spread of the group. Given a
density of 1.78 groups/km2, a mean group velocity of 1991 m/day, a
mean group spread of 20 m (PERES, 1991), and that face-to-face encoun-
ters were defined by intergroup distances ranging from 0 to 40 m,
expected rates of encounters ranged between 0.180 and 0.541 encounters
per day. The total observed frequency of 0.553 encounters per day (42
encounters in 76 days) was thus higher than predicted to occur in the
same period (13.7 < f < 41.1 encounters).

Effects of defence on ranging patterns.

Mixed-species groups of tamarins in the Urucu jointly held very large

areas. The main group used a 141-ha home range, an estimate based on
0.23-ha quadrats and locations every 10 min, and two other groups
followed less systematically were known to use areas of at least 85 and 110
ha, respectively. The main group used most intensely those home range
areas shared by other groups, and spent nearly twice as much time in
encounter quadrats than expected from their availability in the home
range (Table 1). Encounter and approach quadrats were used more often,
and those elsewhere less often, than expected by chance (X2 = 406.2, 2 df,
p < .001).
Use of peripheral quadrats occurred primarily early in the morning,
following rapid boundary approaches. Tamarins then remained close to
boundaries, which resulted in centrality distances before 1200 h being
longer than those in the afternoon (Kolmogorov-Smirnov, Z = 5.21, p <
.001, N = 2267; Fig. 3a). Centrality distances were on average 453 ± 182
m (N = 2263), and skewed towards sub-terminal areas in the home range
(Fig. 3b); tamarins spent more time away from the range centre than
expected on the basis of range areas occupying 19 concentric zones with a
radial width of 50 m (G-test, G = 111.0, 18 df, p < .001). The group
usually approached, entered and remained within the range periphery
regardless of whether a neighbouring group had been detected. The
amount of time tamarins remained within these areas was thus not simply
determined by the presence of other groups. Indeed, only a small fraction
of the time allocated by the group to encounter quadrats was actually
spent in encounters. Because tamarins always vocally advertised their
presence through long-calls when approaching encounter zones, they
were unlikely to go undetected unless their calls were outside a neigh-
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 229

TABLE 1. Number of group locations within encounter and approach

quadrats, and elsewhere in the group's range
Quadrats Number of group locations
Quadrat zone Freq. % Observed % Expected X2

Encounter 25 11.3 692 21.8 359.0 308.7*

Approach quadrats 21 9.5 391 12.3 301.6 26.5*
Other areas 175 79.2 2091 65.9 2513.3 71.0*

Total 221 100 3174 100 3174.0 406.2*

* 2 df, p<0.001. Expected number of locations were calculated on the basis of the area
available to the group within each type of quadrat.

bour's hearing range. This is supported by the fact that tamarins invaria-
bly discontinued their activities, initiated counter-calling, and moved
towards the other group, in response to long-calls of neighbours. They
then tended to remain in encounter quadrats, even if encounters failed to
escalate, at least until those calls were no longer heard.
The study group entered 16.6 ± 3.5 (N = 38) quadrats during complete
days in which encounters occurred, and 14.4 ± 4.9 (N = 30) quadrats
during days without encounters (Mann-Whitney U-test, Z = 1.64, p =
.10). This failed to result in a significant difference in the diurnal diversity
of quadrat use, as determined by the Shannon-Wiener index (encounter-
days: H' = 2.50 ± 0.25; non-encounter days: H' = 2.36 ± 0.42, Mann-
Whitney U-test, Z = 0.77, p = .44), even when differences in observation
time were controlled for. Both daily number of quadrats entered
(ANCOVA, F1,60 = 2.5, p = .12) and daily quadrat diversity (ANCOVA,
= 1.2, p = .28) remained unchanged between encounter- and non-
F1,60
encounter days. This can be explained by the fact that the slightly greater
area used during encounter days was compensated for by the more even
allocation of time to different quadrats during days without encounters,
when tamarins were not forced to spend a discrepantly large amount of
time within encounter quadrats.
Whether or not encounters occurred on any given day affected the
distance travelled by the main group during complete days. The distance
covered on encounter days (2104 + 313 m, N = 38) was greater than that
on days without encounters (1835 ± 484 m, N = 30; Mann-Whitney
U-test, Z = 2.0, p = .04). This reflects differences in group velocity, which
was greater during encounter-days (234 ± 48 m/h, N = 38) than during
days without encounters (196 ± 56, N = 30, Mann-Whitney U-test, Z =
2.54, p = .01). Distances moved during intergroup approaches (when they
230 CARLOS A. PERES

. -_ n=2263 locations
C 600-
.' -- lal
o 550- -
80

o 450 --- -

400-
u 350-

300- -
'5
4
. . . . . . .
250 .
6 7 8 9 10 11 12 13 14 15 16
Time of day

350
n=2263
300-
I Ibi
~~~~~~~*
·v250-
200-

,150-

50
100-

0 100 200 300 400 500 600 700 800 900

Distance (m) from home range center

Fig. 3. (a) Diurnal variation in group centrality during quarter-hour locations throughout the
study, showing (b) the overall distribution of time spent in different centrality zones. Numbers
of locations obtained (n) are shown for each figure.

reached their greatest velocities) were highly inconsistent, ranging from

less than 100 m to 920 m, a distance almost as long as their home range
diameter.
MITANI & RODMAN'S(1979) ratio between day ranges and range size, or
'index of defendability' D (defined by D - d/d', where d' = /4A/a)
suggests that the main group was able to defend space by using a large
part of its range per unit time and frequently approach different points in
the range periphery. Given that the diameter of a circle (d') with an area
(A) equal to the main group's home range size was 1389 m, and that the
group moved a mean distance (d) of 1991 m per day, D was 1.43 the
average number of home ranges which could be crossed by the group on a
daily basis. This allowed tamarins regular visits to territorial boundaries,
regardless of how their movements were affected by the location of other
groups.
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 231

TABLE2. Proportion of time spent by each tamarin species, and both

species combined ("both sp."), in different activities during long-range
and face-to-face encounters, and outside encounters
Long-range Face-to-face Outside
encounters encouters encounters
Activity pattern S.f S.m. both sp. S.f S.m both sp. Sf S.m both sp.

Move 42.6 * 43.4 43.0 45.4 * 47.0 46.4 31.4 28.4 29.8
Rest 25.0 * 16.2 20.0 24.9 * 5.0 13.1 22.8 17.4 19.8
Feed 12.0 * 12.3 12.2 11.7 * 10.2 10.8 26.6 27.6 27.2
Forage 9.9 * 16.3 13.6 5.7 * 11.7 9.3 14.6 21.2 18.2
Intra-group social 1.7 2.5 2.2 1.1 * 1.2 1.2 3.0 3.3 3.1
Inter-group social 8.4 * 8.6 8.5 10.6 * 24.7 18.9 0.9 1.3 1.1
Other 0.3 0.7 0.5 0.6 0.1 0.3 0.7 0.8 0.7

Number of scans 573 754 1327 615 895 1510 11230 13814 25044
X2 values 434 445 870 775 4121 4778
*
Log-linear models on interspecific comparisons: log-likelihood ratio tests, 3 df, p<0.0001.
Italic numbers indicate significant cell contributions to overall X2 values (BROWN,1974)
based on species-specific comparisons of scan frequencies during each encounter context,
and those outside encounters. Log-linear models are based on 3-way interactions testing for
interspecific differences in scan frequencies of each activity between each encounter con-
text and that outside encounters.

Effects of defence on time budgets.

Time budgetsduringintergroupencounters.
The time budget outside encounters of either tamarin species was signifi-
cantly different from those observed during long-range and face-to-face
encounters (Table 2). During face-to-face encounters, tamarins of both
species spent significantly more time moving and interacting with non-
group conspecifics, and significantly less time feeding and foraging, then
when they were outside encounters. Moustached tamarins spent signifi-
cantly less time resting during encounters, whereas saddle-backs did not.
The same was true for long-range encounters, except that the difference
in the amount of time spent foraging was not significant. Considering
both species combined, standardized residuals were greatest for feeding
and moving during long-range encounters, and feeding, intergroup social
interaction, and resting during face-to-face encounters, whereas other
activities failed to reach significance. At close quarters to other groups,
moving and intergroup interactions by both tamarin species accounted
for twice the amount of time of that outside encounters. Feeding, which
accounted for over one quarter of tamarins' null time-budget, declined to
232 CARLOS A. PERES

11-12% of their time during face-to-face and long-range encounters,

respectively.
Time budgets also differed between the two types of encounters (X2 =
93.5, 6 df, p &lt; - rest and
.001), although only two activities intergroup
social - were significant contributors to this difference. Animals
appeared to allocate a similar amount of time foraging for arthropods
between contexts outside encounters and those of long-range encounters.
This may be explained if animals anticipated long-range interactions to
escalate into direct confrontations, and increased their foraging effort to
compensate for the small amount of time which could be spent on
foraging during actual boundary contests.
These differences although derived from lumping all age-sex classes,
did not appear to have resulted from oversampling behaviourally conspic-
uous individuals during contexts of intergroup interactions. For instance,
observed frequencies of scans obtained from adult males - the most
active members of the group during territorial encounters - were not
significantly different from that expected based on their representation in
each monospecific group during either long-range (fuscicollis: X2 = 0.07, 1
df, p = 0.79; mystax:X2 = 0.22, 1 df, p = 0.88) or face-to-face encounters
(fuscicollis:x2 = 0.43, 1 df, p = 0.51; mystax:x2 = 2.17, 1 df, p = 0.14).

Interspecificdifferencesin time budgets.

Although both tamarin species were involved in all encounters, their time
budgets differed significantly from one another during either face-to-face
(G- test, G = 170.6, 6 df, p &lt;.001) or long-range encounters (G = 24.1, 6
&lt;
df, p .001), suggesting an asymmetric division of labour in their terri-
torial defence effort (see Table 2). Interspecific differences in time budgets
were greater during either types of encounters than at other times, as
examined by 3-way matrices based on loglinear models, using scan fre-
quencies of all activities as a dependent variable of species identity and
intergroup interaction context (long-range encounters: G = 749.4, 18 df,
p &lt;
.001; face-to-face encounters: 1770.0, 18 df, p &lt; .001). Comparing the
time tamarins allocated to each activity against that to all others, inter-
specific differences remained highly significant for all activities during
both types of encounters (log-linear models, 3 df, p &lt; .001 in all cases),
except for 'within-group social interactions' (G 7.2, df, p = .07) and
= 3
'other' (G = 2.5, 3 df, p = .48) during long-range contests (Table 2).
Moustached tamarins usually dictated the velocity of intergroup
approaches and withdrawals, were the first animals to come into contact
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 233

with, and the last to retreat from, conspecifics of a neighbouring group,

and led the course of face-to-face encounters. This species spent 25% of
their time in what appeared to be highly conspicuous and energetically-
demanding intergroup agonistic interactions. Frequent chases and dis-
placements between moustached tamarins accounted for the bulk of the
intergroup aggression displayed by the entire mixed-species group. In
contrast, saddle-backs spent only 11% of their time during encounters
interacting with non-group conspecifics.
The proportion of time spent resting during encounters by moustached
tamarins (5%) was less than a third of that outside encounters, whereas
saddle-backs spent slightly more time resting during encounters (25%)
than at other times. During joint-territorial disputes, saddle-backs of all
age-sex classes were often found quietly resting at inconspicuous and
retreated positions as far as 40 m from their quarrelling heterospecifics.
Usually, however, they adopted a passive role of 'stand-by' spectators,
watching moustached tamarins chase one another, and only occasionally
engaging in their own squabbles with conspecifics of the other groups.
Face-to-face encounters also comprised the only context in which saddle-
backs spent a greater (albeit not significantly different: G-test, G = 0.9, 1
df, p = .34) amount of time feeding than moustached tamarins. This is
supported by the fact that saddle-backs spent more time feeding during
the time of day when most encounters occurred (0700-1100 h) than at
other times (G = 16.2, 1 df, p &lt; .001), whereas this difference was not
significant for moustached tamarins (G = 0.9, 1 df, p = .34).
In addition, saddle-backs consistently 'lost interest' in encounters
sooner than moustached tamarins, and collectively moved away from the
encounter site. Their persistent long-calls during such premature with-
drawals appeared to be targeted to moustached tamarins, and often
preceded the termination of encounters. Indeed, the only time the two
species were observed to drift apart took place towards the end of a
prolonged encounter, when saddle-backs clearly drifted off while mous-
tached tamarins still vigorously confronted their neighbours.

Time budgetswithin encounterquadrats.

In order to disentangle the potential effects of exploitative and inter-
ference competition on tamarins' activities, time budgets were examined
within and outside encounter quadrats, but outside contexts of actual
encounters. Time budgets outside encounter quadrats, in this case, were
considered as the null state. Only 14.3% of 10830 minutes allocated by
234 CARLOS A. PERES

TABLE3. Proportion of time spent by each tamarin species, and both

species combined (both sp.), in different activities within and outside
encounter quadrats, excluding time spent in actual intergroup encounters
Inside encounter quadrats Outside encounter quadrats
Activity pattern S.f S. m both sp. S. f S. m both sp.

Move 28.6* 26.6* 27.5* 33.4 29.8 31.4

Rest 23.6 18.4 20.8 23.5 17.7 20.3
Feed 29.0* 27.9 28.4* 23.7 25.8 24.8
Forage 14.5 21.7 18.4 14.6 21.3 18.3
Intra-group social 2.6 3.3 3.0 3.2 3.3 3.2
Inter-group social 0.9 1.4 1.1 1.0 1.3 1.2
Other 0.7 0.7 0.7 0.6 0.8 0.7

Number of scans 3108 3796 6904 7806 9671 17477

*
Significant cell contributions (p<.05) to overall X2values (BROWN,1974). X2 tests are based
on species-specific comparisons between scan frequencies inside and outside encounter
quadrats (see methods): S.fuscicollis: X2 = 62.6; S. mystax:X2 = 21.8; both species combined:
X2 = 71.0, 6 df, p<.001.

the group to approach and encounter quadrats was actually spent in

encounters. Thus groups appeared to be outside their neighbours' hearing
range during most of the time they spent in peripheral quadrats.
There were significant differences between the time budgets of the two
species, both within (G-test, G = 80.7, 6 df, p < .001) and outside
encounter quadrats (G = 206.5, 6 df, p < .001); Table 3). Each species also
differed in its time budget between quadrat types, particularly in the
amount of time spent moving and feeding. The lower proportion of time
spent moving by both species, and higher proportion of time spent feeding
by saddle-backs, within encounter quadrats (but away from the other
groups) may be related to the high probability of intergroup encounters in
these areas. Tamarins frequently evoked responses from neighbouring
groups via long-calls, did not move away, and concentrated their spare
time around local food sources, which were clearly shared by other
groups. Again, interspecific differences in time budgets were a function of
the fact that moustached tamarins allocated a greater effort in assessing
their neighbours' location. For instance, one or two adult males of this
species consistently drifted away from their core group-members, into the
adjacent territory, where they persistently called for, and apparently
listened to other groups, clearly to the detriment of their own feeding
success.
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 235

Effects of centralityon time budgets.

Distance from the home range centre affected the time budget of both
tamarin species, as there was a significant association between the
amount of time animals spent in different activities and group location in
one of seven centrality zones (G-tests, saddle-back: G = 298.8, 30 df, p &lt;
.001; moustached: G = 408.0, 30 df, p &lt; .001; Fig. 4). There appeared to
be no significant differences between the amount of time each tamarin
species allocated to a given activity as they moved away from the range
centre (Table 4). As centrality decreased, however, tamarins of either
species spent more time interacting with members of neighbouring
groups, and moustached tamarins spent less time in intragroup social

45 30
I-J- u S. fusdcollis
* S. mystax
40 25

> 35 20

~o~~ V~o
30 - 1 15

U) 25 'I 10
0 0 35 , 20
E (

30 - 16
co
25 I12

0 0
*- 0- ~~~~~~~
20~u5 0 8

C 0

0 6-) 8

0.0

0 0

0-200 200 300 400 500 600 >700 0-200 200 300 400 500' 600 >700

a as function of centrality zone.

Distance (in) from the home range center

Fig. 4. Variation
Fig. Variation in
in the proportion of
the proportion of time
time spent by each
spent by each tamarin species in different
tamarin species different activities
activities
as a function of centrality zone.
236 CARLOS A. PERES

TABLE 4. Comparisons between each tamarin species' time budget in each

of 7 centrality zones, and correlations between centrality and amount of
time each species spent on different activities
Interspecific differencesa Spearman rank correlationsb
Activity pattern G p S. fuscicollis S. mystax

Moving 6.5 0.37 0.43 0.61

Resting 9.1 0.17 -0.61 -0.50
Plant-feeding 3.0 0.81 -0.43 -0.50
Foraging 11.3 0.08 0.54 0.64
Intra-group social 6.9 0.33 -0.50 -0.86**
Inter-group social 5.2 0.51 0.93** 0.75*
a
Log-likelihood ratio tests, 6 df;
b n=
7; * p<0.1; ** p<0.05.

activities (Table 4). Other activities were not significantly correlated with
centrality. That centrality most obviously affected the amount of time
animals spent in intergroup social interactions is expected, since these,
with the exception of long-calls, could not occur away from range
boundaries.

Effects of defence on foraging success.

Capturesuccessduringintergroupencounters.
Capture success of each tamarin species, considering both foraging time
and maneuvers, was calculated in different contexts of intergroup interac-
tions (Table 5). These parameters within tamarin species were not signifi-
cantly different between either types of encounters and non-encounter
null states (G-tests, p > .10 in all cases). There were also no three-way
differences in the effect of encounter context on rates of successful cap-
tures by each tamarin species (log-linear models; prey items per capture
attempt: G = 0.91, 2 df, p = .64; prey items per foraging scans: G = 0.96,
2 df, p = .62). In real terms, however, few prey-captures took place during
encounters compared to those outside encounters because the amount of
time spent away from neighbours was substantially greater. Thus, inter-
group distance per se may not be an important variable in determining
direct arthropod foraging costs and benefits of territorial defence. The
effects of spatial overlap with neighbouring groups on capture success,
independently of intergroup distance, is examined below.
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 237

TABLE5. Percentage of time spent foraging by each tamarin species, and

both species combined (both sp.), in different encounter contexts, showing
the proportion of foraging scans and prey capture attempts which resulted
in successful captures
Long-range Face-to-face Outside
encounters encounters encounters
Percent of time Sf S.m both sp. Sf S.m both sp. Sf S.m both sp.

Stationary foraging 5.8 9.4 7.8 1.8 5.5 4.0 5.7 10.5 8.3
Foraging maneuvers 1.9 2.0 2.0 1.8 1.6 1.7 4.2 3.5 3.8

Capture success (%)

Per foraging scan 10.2 23.2 19.0 18.5 33.0 28.2 14.1 21.7 19.0
Per capture maneuver 31.3 63.4 53.6 31.3 68.9 56.9 27.9 52.4 42.7

Number of scans 573 754 1327 615 895 1510 11230 13814 25044
Number of prey captures 5 26 31 5 31 36 182 536 718

Prey items were considered irrespectively of their size class.

TABLE6. Percentage of time spent foraging by each tamarin species, and

both species combined, within and outside encounter quadrats, showing
the proportion of foraging scans and prey capture attempts which resulted
in successful captures
Inside encounter quadrats Outside encounter
quadrats
Percent of time S.f S.m both sp. Sf S.m both sp.

Stationary foraging 5.3 10.3 8.1 6.1 10.9 8.8

Foraging maneuvers 4.4 4.1 4.0 4.3 3.5 3.9

Capture success (%)

Per foraging scan 13.3 21.8 18.9 12.5 20.5 17.7
Per capture maneuver 25.3 50.2 40.8 25.6 51.5 41.3

Number of scans 3108 3796 6904 7806 9671 1747

Number of prey captures 46 151 197 116 361 477

Prey items were considered irrespectively of their size class.

Capturesuccesswithin encounterquadrats.
Use of encounter quadrats outside actual encounters determined no sig-
nificant effect on the amount of time tamarins of either species spent in
stationary foraging, foraging maneuvers, foraging in general, and on
frequencies of prey captures (G-tests, p > .20 in all cases; Table 6).
238 CARLOS A. PERES

Capture success also remained unchanged for both species between these
two types of quadrats: there were no significant three-way interactions
when a log-linear model was applied to capture frequencies per capture
attempt (G = 0.03, 1 df, p = .87), or per foraging scan (G = 0.01, 1 df, p =
.99). Within encounter quadrats, both tamarin species combined
obtained 197 prey items during 18.9% of the time they spent foraging (N
= 1041), and completed on average 40.8% of their capture attempts (N =
483). Outside encounter quadrats, the 477 observed captures resulted in a
slightly lower capture rate per unit of foraging time (17.8%, N = 2687),
but slightly greater rate per unit of capture attempt (41.3%, N = 1155).
Because encounter quadrats represents an arbitrary measure of tam-
arins' fields of isolation, and accounted for only a small part of a group's
total range area overlapping with those of other groups, foraging success
was further examined as a function of distance to range boundaries.

Effects of centralityon capturesuccess.

The effects of group centrality on its foraging efficiency were examined
using 7 contiguous rings of activity, concentric on the home range centre.
For these purposes, foraging data were pooled within the two most
central, and two most peripheral zones, because of inadequate sample
sizes. Resources near the range centre are least likely to be depleted by
other groups, and are subject to reduced intergroup exploitative competi-
tion. This should allow resource availability and predictability to be
greater in these areas to the resident group. Residents' foraging success
should then increase with distance from range boundaries if other groups
are able to affect the distribution of a particular resource type.
Capture success of tamarins was affected by the forager's species iden-
tity and its centrality zone (Fig. 5). These two variables, when incorpo-
rated into a log-linear model, determined significant effects on the
number of foraging maneuvers yielding successful captures, whether they
were considered separately, or in a two-way interaction (Table 7). The
same effects applied to the number of captures when overall scan frequen-
cies of all foraging activities were considered.
The number of prey captures per foraging scan for saddle-backs
decreased significantly as the group moved away from the range centre,
into the range periphery (r = -0.78, 6 df, p = 0.04), but not for mous-
tached tamarins (r = -0.71, 6 df, p = .07; Fig. 5a). This effect was far more
pronounced within intermediate zones of 300-600 m from the home
range centre, the portion of the group's range subjected to the most
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 239

0.30
* mystax
fusdcollis
0.25.2--

0.20

(o
0 0.15
(a)
0.10

E ,________ ___
0.05
0-200 200 300 400 500 600 >700

E 0.6'

(d 0.4 -

0.3

00.2

0.1
0-200 200 300 400 500 600 >700
Distance (m)from the rangecenter

Fig. 5. Effects of group centrality on each species' prey capture success, defined as the number
of captures obtained (a) per foraging effort (time spent foraging), and (b) per foraging
maneuver (individual capture attempts).

intensive use by the main group and its neighbours. In this area alone,
centrality explained 98% (r = -0.99, 3 df, p = .01) of the variation in
capture rate per attempted capture by saddle-backs (which were largely
manipulative foragers), but only 9% (r = -0.30, 3 df, p = .70) of that by the
visually foraging moustached tamarins.
The frequency of successful prey captures per foraging maneuver by
both tamarin species also suffered a significant decrease with increasing
distance from the range centre (saddle-back: r = -0.74, 6df, p = .06;
moustached: r = -0.84, 6 df, p = .02; Fig. 5b). Capture success per
foraging scan was again strongly correlated with distance to boundaries
within the four intermediate centrality zones, explaining 99% of this
parameter for saddle-backs (r = -0.10, 3 df, p = .004), but only 16% of
that for moustached tamarins (r = -0.40, 3 df, p = .60).
240 CARLOS A. PERES

TABLE 7. Log-linear models showing the effect of tamarin species and

centrality on the capture success of animal prey items
Per foraging maneuver Per foraging scan
Source G df p G df p
Tamarin species 26.3 12 0.01 31.1 12 0.002
Centrality zone 138.1 7 0.001 76.1 7 0.001
Species and centrality zone 12.1 6 0.06 23.4 6 0.001

TABLE8. Parameter estimates for a logistic regression model considering

centrality distance and tamarin species as independent covariates of
whether prey captures were successful or not
Per foraging maneuver Per foraging scan
Independent variable Coeff.±SE Wald test Coeff.±SE Wald test

Tamarin species 0.582±0.054 116.1** 0.331±0.047 48.9**

Centrality zone 0.095±0.029 10.6** 0.044±0.024 3.4*
Constant 0.110±0.128 0.7 1.416±0.105 181.9**
** 1 df, p<.001; * p = .067.

These linear correlations are confirmed by a logistic regression model

where centrality zone was a significant predictor of frequency of prey
captures per foraging maneuver for both tamarin species (Table 8). Fre-
quency of prey captures per foraging scan also differed significantly
between tamarin species, but failed to reach significance between central-
ity zones.

Discussion
Resource defence by interference displayed by mixed-species groups of
Saguinusis similar to that documented for many other territorial species.
All wilds callitrichids, for instance, are typically neighbour-intolerant,
and use regular long-distance vocal signals to seek out, vigorously
approach, and confront other groups. Intense territorial interactions
occur along relatively narrow boundaries between groups of lion tamarins
(RYLANDS, 1983; PERES, 1989), marmosets (RYLANDS, 1983; HUBRECHT,
1985), and other tamarins (TERBORGH, 1983, 1984; GARBER, 1988).
Intergroup vocal interactions, such as long-calls, occurred mostly early
in the morning, when conditions for sound transmission in tropical forests
are nearly optimal (WASER & WASER, 1977). Tamarins moved to bound-
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 241

aries at this time of day, a pattern similar to that of many other territorial
primates (e.g. gibbons: CHIVERS, 1974; titi monkeys: ROBINSON, 1979).
Intense long-calling whilst neighbouring groups approached one another
then usually escalated into ritualized intergroup encounters, often within
relatively restricted, and apparently traditional sites. These encounters
occurred more frequently than expected if movements of groups were
independent, which markedly contrasts with many other forest primates
that adopt mutual-avoidance spacing systems, and encounter neighbours
at a rate lower than predicted by chance (e.g. WASER, 1976; WHITEHEAD,
1987).
Centripetal movements, particularly after territorial interactions, occur
in many forest primates (WASER, 1976; ROBINSON, 1979), suggesting
avoidance of resource-depressed, peripheral areas. This may be possible
when defence by interference alone prevents intruder trespassing, effec-
tively excluding other groups from a resident's home range (e.g. ROBIN-
SON, 1979). In contrast, use of space by tamarins and lion tamarins is
biased towards the range periphery, particularly encounter zones, despite
the extensive range overlap between neighbouring groups (PERES,1989,
this study). If range boundaries are defined by the location of intergroup
encounters, then they did not coincide with the most peripheral range
areas. This is supported by the fact that tamarins' aggression fields were
apparently highest in subterminal areas of their range: when approached
by other groups near the fringes of its home range, the main group often
rapidly retreated a short distance into more central encounter quadrats.
This is also the case in golden lion tamarins, whose highly defended
territories overlap as much as 60% with those of neighbouring groups
(PERES, 1986). The proportion of time spent in peripheral, rather than
exclusive, areas was substantially greater than that expected by chance.
This facilitated detection of intruders, allowed resource defence by
exploitation, and depleted resources which otherwise would have been
lost to neighbours.
Use of the range periphery when neighbouring groups are far apart
appears to complement defence by interference, particularly when the
latter alone cannot exclude competitors from large feeding territories.
This is likely to be the case in mixed-species groups of tamarins in the
Urucu because their home ranges are extremely large compared to those
in other Amazonian sites, as well as other frugivore/insectivore primates
of equivalent group biomass (PERES,1991). Range defence thus appeared
to be very costly, even though is failed to exclude other groups entirely.
Defence by exploitation also occurs when residents are unable to directly
242 CARLOS A. PERES

challenge intruders, whether because these are larger-bodied (GILL &

WOLF, 1975; KODRIC-BROWN & BROWN, 1978), or in large flocks or
schools (MYERSet al., 1981). Exploitative competition between tamarin
groups through peripheral bias in range use can thus be seen as an
energetically inexpensive form of resource defence. This seems to play a
major role in the territorial system of these and other callitrichid species
(PERES,1989), analogous to that shown for other territorial vertebrates
foraging primarily in the range periphery, such as reef fishes (ROBERTSON
et al., 1976), hummingbirds (KODRIC-BROWN & BROWN, 1978; PATON &
CARPENTER, 1984), sunbirds (GILL & WOLF, 1975), and shorebirds (MYERS
et al., 1981).
It is clear that day-to-day territorial interactions occurred frequently,
and were often long-lasting, even though they provided no short-term
benefits to either species of tamarins. Intergroup interactions, particularly
face-to-face encounters, imposed strong energetic costs on tamarins, gen-
erally resulting in greater proportions of time spent in energetically
expensive or negative activities, such as moving to boundaries, displaying
to, and chasing non-groups members. They allowed little time for ener-
getically conservative or positive activities, such as resting, feeding and
foraging. Time budgets during encounters suggest that the energetic
burden, at least through interference mechanisms, fell mostly on mous-
tached tamarins. During encounters, tamarins of this species engaged in a
comparatively greater range and frequency of agonistic interactions with
conspecifics of other groups, to which they allocated significantly more
time than did saddle-back tamarins. Fights between non-group members
probably explain the ear-cuts and scars, which occurred in nearly half of
all adult moustached tamarins in 5 groups, but not in any saddle-back
tamarin. Moustached tamarins also determined the timing and direction
of intergroup approaches and withdrawals, generally leading territorial
contests. Saddle-backs, on the other hand, usually remained stationary in
the vicinities of encounters between their heterospecifics, often grooming
one another, and spending far less time in energetically demanding, or
hazardous activities.
Because home ranges of groups of each species were congruent, the
potential benefits of defence could be equally shared by the two species.
These benefits are, however, likely to be greater to saddle-backs - the
species which contributed with the least defence effort -because of
differences in the nature and distribution of foods used by the two species.
What lack of overlap there is in use of plant-food patches was largely
attributed to patch size (PERES, 1991): moustached tamarins, on average,
 JOINT-TERRITORIALITY IN TAMARIN MONKEYS 243

fed on larger patches than did saddle-backs. Small fruit patches are most
susceptible to higher rates of depletion than are large patches, which
increases the relative foraging benefits associated with exclusive use of
space (CHARNOV et al., 1976; WASER,1981). In addition, some 48% of the
prey items captured by saddle-back tamarins were non-mobile and
embedded in very small, and highly depletable microhabitats (PERES,
1991). The abundance of these items need not be evenly distributed in
space. Rather, they should track the distribution of the specific micro-
habitats in which they hide. Once probed, a microhabitat is rendered
useless to a subsequent forager before it is recolonized by new prey. Local
scramble competition between different groups is thus potentially higher
for manipulative foragers, such as saddle-back tamarins. In contrast, prey
items exploited by moustached tamarins - a leaf-gleaning predator
relying on embedded prey in only 4% of its captures - were highly
mobile and widely scattered in the midstorey foliage. This probably
explains the observed differences in the effects of centrality on the prey-
foraging efficiency of the two species. Capture success was sustained at
comparable levels for moustached tamarins, whereas for saddle-backs it
increased substantially as they moved from peripheral areas shared by
other groups to exclusive areas near the range centre. The depression of
capture rates in the range periphery observed in saddle-backs is analogous
to that of golden lion tamarins, which are also manipulative predators
relying heavily on embedded prey (PERES, 1989). This indicates that,
although contributing less to territorial defence, saddle-backs appeared to
derive relatively greater benefits from exclusive use of space than did
moustached tamarins. Saddle-back tamarins thus emerge as the net bene-
ficiary of tamarins' joint territorial system, enjoying a protective shadow
against resource depletion by other groups, which was provided primarily
by moustached tamarins' greater effort in range defence.
Given that joint-territorial benefits were strongly biased towards only
one tamarin species, what then accounts for the investments and toler-
ance of the other in maintaining such remarkably stable associations?
Range defence should be considered in the wider context of other adap-
tive advantages of heterospecific group living, such as division of labour in
locating different-sized plant-food patches (PERES,1991), foraging bene-
fits associated with piracy and facilitated harvest of flushed prey items
(PERES, 1992), and detection of different forms of predation threats held in
common by both species (PERES,in press a). In addition, what infrequent,
but nevertheless decisive, competitive interactions which occurred
between the two species, such as physical displacements over small and
244 CARLOS A. PERES

spatially restricted food patches, invariably favoured the larger-bodied

and dominant moustached tamarin to the detriment of their smaller
heterospecifics (PERES,1991). In any case, there is no evidence to suggest
that the energetic costs of interference competition between neighbouring
moustached tamarin groups would have been reduced by the absence of
saddle-backs. Indeed, the costs of attending a mixed-species group
appears to be higher for the smaller-bodied saddle-back tamarin, mainly
because of its invariably subordinate status, but negligible for moustached
tamarins. Benefits of mixed-species associations to the subordinate spe-
cies were, however, in many respects greater than those of moustached
tamarins. Yet, should these two ecologically very similar species co-exist
at all, their joint-territorial system should be weighed against the no more
attractive alternative of their exploiting an almost identical set of
resources (PERES,in press b) asynchronously by holding overlapping
monospecific spacing systems independently of one another.
Finally, there are cases where a solitary territory holder will accept an
intruder because the feeding costs it imposes are outweighed by the
benefits of increased defence (DAVIES & HOUSTON, 1981). This switch
from solitary to social territoriality may approach the conditions under
which group territoriality has evolved (BROWN,1964). Joint territoriality,
in turn, may result in cases where large monospecific groups will enhance
resource defence by both interference or exploitative mechanisms, but
increases in group size are prevented by ecological or reproductive
thresholds (PERES,1991). In such circumstances, joint-territoriality, par-
ticularly between ecologically similar species, may represent the best
solution to maintain a favourable feeding territory.

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