Primate super-groups? Polyspecific associations of captive monkeys
A thesis submitted to the Miami University Honors Program in partial fulfillment of the requirements for University Honors with Distinction
by
Samantha Russak
May 2006 Oxford, Ohio
ii ABSTRACT
PRIMATE SUPER-GROUPS? POLYSPECIFIC ASSOCIATIONS OF CAPTIVE MONKEYS By Samantha Russak
Polyspecific (or heterospecific or mixed-species) groups are quite common
among animals and vary greatly in their frequency, function, structure, and duration. The interactions between species may be very dynamic or passive with no apparent direct interactions. In the wild polyspecific groups are driven together by foraging and
predation pressures; in captivity, mixed-species groups can be more stimulating for the
animals. This paper examines three mixed-primate exhibits at the Lincoln Park Zoo over
a 12-week period. One of these exhibits was fortuitously in the process of gaining a third
species and so comparative data of before, during, and after stages were used for an in-
depth analysis. Results show that some species, in this case howling monkeys, are little
affected by the presence or absence of another species, while others, in this case sakis, are
greatly impacted.
iii iv
Primate super-groups? Polyspecific associations of captive monkeys
by Samantha Russak
Approved by:
______, Advisor Dr. William C. McGrew
______, Reader Dr. Homayun Sidky
______, Reader Dr. Scott Suarez
Accepted by:
______, Director, University Honors Program v vi
ACKNOWLEDGEMENTS
This project could not have been completed without the cooperation and assistance of the
staff at Lincoln Park Zoo, particularly Dr. Sue Margulis, Andy Henderson, Bonnie
Jacobs, Anita Yantz, Eric Meyers, and Leslie Lurz. I also thank Drs. William McGrew and Linda Marchant for their support and guidance throughout the project and Drs.
Homayun Sidky and Scott Suarez for their help with the write-up of this manuscript.
This research was funded by the Undergraduate Summer Scholars (USS) Program at
Miami University, Ohio.
vii TABLE OF CONTENTS
List of Tables and Figures 9 Introduction 10 Methods Study Subjects 14 Data Collection 16 Results Solitary and Social Behaviors Titis, Goeldi’s monkeys, Allen’s swamp monkeys, guerezas 17 Howling monkeys 17 Sakis 18 Location Howling monkeys 19 Sakis 19 Discussion Solitary Behaviors and Social Interactions 20 Location 23 Implications and Future Studies 24 References 26
viii LIST OF TABLES AND FIGURES
Tables
Table 1. Ethogram 28
Table 2. Proximity data for two mixed-primate groups 29
Table 3. Partial behavioral repertoire of howling monkeys 29
Table 4. Location of howling monkeys within exhibit 30
Figures
Figure 1. Partial behavioral repertoire of male saki 30
Figure 2. Partial behavioral repertoire of female saki 31
Figure 3. Partial behavioral repertoire of saki pair 32
Figure 4. Location of sakis within enclosure 33
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INTRODUCTION Large aggregations are not uncommon among animals, mostly being comprised of members of a single species. However, groups in which two or more species associate have also been well documented in both wild and captive settings. Polyspecific (or heterospecific or mixed-species) groups are best known in birds and mammals (Stensland et al., 2003), and among mammals, polyspecific associations in primates are perhaps the most studied (e.g. Chapman and Chapman, 2000). Such super-groups vary greatly in their frequency, function, structure, and duration, with species associating together for hours, days, weeks, or longer.
The two main hypotheses as to why polyspecific associations occur are anti- predator and foraging advantages. Larger groups provide increased detection of both predators and food resources, and can more easily deter predators (through confusion or mobbing), displace smaller groups, or defend territory (Terbough, 1990; Waser, 1982). It has also been suggested that some species exploit the resource knowledge of their associates, with one species using another species as a “guide” to lead it to food resources
(Norconk, 1990). Given these potentially important functions, it may be that polyspecific associations are co-evolved social structures, and if so, the consequent social relations may be important to participants. While the pressures of predation and foraging do not occur in zoos, there may be social benefits to housing together species that associate in nature. Captive mixed-species groups show greater overall activity levels and have richer
(more stimulating) lives (Hardie et al., 2003).
Most interspecific interactions in the wild are passive, with no apparent direct interactions. This includes tolerant spatial proximity resulting from a shared interest in
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resources, such as food and habitat, as well as changes in behavioral patterns. For
example, Chapman and Chapman (1996) found redtail monkeys to increase levels of
vigilance when in association with another species. In a later study, Chapman and
Chapman (2000) observed redtail monkeys to quickly follow red colobus groups when in association with this species; as black and white colobus rarely followed red colobus when in association, these findings suggest that redtail monkeys actively maintain their associations with red colobus, while black and white colobus simply tolerate the presence of red colobus. Dynamic interactions between species are much less common, and are usually limited to play among juveniles, such as in the case of white faced capuchins and mantled howling monkeys in Costa Rica (Rose et al., 2003) or contact aggression over food (e.g. Diana monkeys and putty-nosed monkeys during periods of low fruit availability; Eckardt & Zuberbühler, 2004).
Similar interactions are observed among mixed-species groupings in captivity.
However, as these groupings are predetermined by the facility’s staff, and as animals are spatially limited within enclosures, there is a greater risk for interspecific agonism or even violent encounters. This aggression can be overt, manifested in displacement, competition for space within an enclosure or food, or it can be subtle, evidenced as intimidation by social dominance or as stress (Thomas & Maruska, 1996). In contrast, species can be stimulated through non-hostile contact with one another. For example,
Hardie et al. (2003) documented instances of interspecific playing and grooming within a tamarin mixed-species troop.
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This paper presents an observational study of inter-species interactions between
mixed-primate groups housed in three different exhibits at the Lincoln Park Zoo. These
exhibits provided groupings reflecting different phylogenetic degrees of associations in
the wild (either on a generic versus a specific level), therefore providing comparative
data. Among New World primates, the most common participants of polyspecific
associations (in the wild and captivity) are members of the subfamily Callitrichinae. For
example, Goeldi’s monkeys (Callimico goeldii) are frequently found in association with
tamarin (Saguinus) troops (Porter, 2001; Azevedo Lopes & Rehg, 2003). These
associations are generally initiated by C. goeldii, and likely function to allow the parasitizing of Saguinus knowledge of fruit sources (Porter, 2001). Buchanan-Smith et
al. (2000) found stable bispecific associations among tamarins in northern Bolivia, and
occasionally observed trispecific associations with Callimico or Pithecia. This particular
study included a mixed group of Callimico and Callicebus. Although geographical
distributions of Goeldi’s monkey and members of the genus Callicebus (titi monkeys)
commonly overlap, there is not much documented on associations between the two taxa.
However, given that Goeldi’s monkeys and reed titi monkeys are within the same
taxonomic family, and that Goeldi’s monkeys are often found in polyspecific
associations, I hypothesized that this pairing would exhibit the most behaviors associated
with affiliation, including play, social groom, and proximity as compared to the other two
exhibits.
Howling monkeys (Alouatta caraya) and sakis (Pithecia pithecia), are more
closely related than the previous pair, and therefore might be expected to associate more
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frequently. However, these two genera occupy very different dietary niches, with
howlers being mainly folivorous and sakis being frugivorous, with a heavy reliance on
seeds. This may explain observed occurrences of saki groups within proximity to
howling monkeys with no apparent behavioral reactions (Vie et al., 2001). Further, it has
been found that within a mixed-species group, the species with the larger body size tends
to join the species with the smaller body size (Struhsaker, 1981). Therefore, with
howlers being almost twice the size of sakis and the lack of direct interactions in the wild,
I hypothesized that there would be fewer interactions than in the other two exhibits, and
that most, if not all, of the associations that did occur would be initiated by the howlers.
Among Old World primates, polyspecific associations are most commonly found
among cercopithecines. In addition to associating with other cercopithecines, they are
frequently found with colobines. Therefore, Colobus guereza and Allenopithecus
nigroviridis are not an unlikely pairing. However, many studies (e.g. Chapman &
Chapman, 1996; Struhsaker, 1981) have found Colobus to be the least frequent
participant in polyspecific associations due to their shy and secretive nature. Further,
Colobus spend most of their time in the upper canopy, while Allenopithecus are observed
most frequently on the ground (McGraw, 1994). Therefore, I hypothesized that these two
species would use their exhibit very differently, with Colobus using the upper half more,
and that this exhibit would have the least amount of social interaction among the three
exhibits.
The main aim of this project was to see whether two species would associate with
one another in the absence of pressures (e.g. predation and natural foraging) that seem to
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drive polyspecific associations in the wild; this may provide some indication of the significance of the mutualistic adaptation. This study allowed for a detailed look at the interactions and relationships of the animals involved that might not always be possible in the wild, and therefore has the potential to give insight into how polyspecific associations function in the wild. Most importantly, results showing that the pairing of these species was beneficial (i.e. increased levels of non-antagonistic activity) to the animals could provide encouragement to other zoos to establish mixed-species exhibits.
METHODS Study Subjects
The Helen Brach Primate House at the Lincoln Park Zoo, Chicago, Illinois housed
three mixed-species groups. The first group comprised a 19-year-old female and 12-
year-old male black-and-white colobus monkey (Colobus guereza), and a family of
Allen’s Swamp monkeys (Allenopithecus nigroviridis): 11-year-old female, 12-year-old
male, and their three sons, aged four years, two years, and three months. All ages
reported here were as of the start of the study. Guerezas live in primary and secondary
forest and wooded grasslands, while swamp monkeys live in swamp forests. These
species are not sympatric in nature, as swamp monkeys are found only in Zaire and
Angola, while guerezas occur from eastern Nigeria to Ethiopia, Kenya, Uganda, and
Tanzania, but swamp monkeys are sympatric with other black-and-white colobus species
(Colobus sp.).
The second exhibit housed a family of Bolivian gray titi monkeys (Callicebus
donacophilus; 14-year-old female, 8-year-old male, 2-year-old male, 1-year-old female)
that were on exhibit every other day with a mixed-species group. This group consisted of
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a breeding pair of Goeldi’s monkeys (Callimico goeldii), aged 5 years old (male) and 1 year old (female), and a pair of Bolivian gray titi monkeys, aged 26 years old (female) and 23 years old (male). The titis are highly endangered, being restricted to areas of
Bolivia, while the Goeldi’s monkeys are found in Brazil, Bolivia, Peru, and Columbia.
Both species live in tropical rain forests, with the titis occupying the upper canopy and the Goeldi’s monkeys frequenting the middle and lower levels.
The third exhibit was a group of black-and-gold howler monkeys (Alouatta caraya; two females aged 15 years old, a 6-year-old female, and a 9-year-old male) and a mother-son pair of white faced sakis (Pithecia pithecia; aged 13 years old and 7 years
old, respectively). In the middle of my study, a third species was introduced to this
group. These pied bare-faced tamarins (Saguinus bicolor) were a brother-sister pair, aged
6 years old and 2 years old, respectively. While the pied tamarins are critically
endangered and only found in a small area of Brazil, the other two species are at lower
risk and expand their ranges to include other areas of South America such as Paraguay,
Suriname, and Guyana. All three species are mostly found in secondary forest.
All three groups were put on exhibit in the morning before the zoo opened and returned to their sleeping quarters overnight, where all species stayed in separate cages, except for the Goeldi’s monkey/titi monkey pairing, which remained together. The primates were fed once in the morning and again in the afternoon, and had continuous
access to water. All primates were given daily enrichment of one of eight types, such as
browse, naturalistic toys, scents, and different food preparation.
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Data Collection Data were gathered over a 12-week period from May to August, 2005 on 56 days,
resulting in a total of 221 hours of data. Data collection entailed stratified random
sampling of focal-subjects, balanced for day of week, time of day, and before/after
feeding. I sampled all subjects daily from all three exhibits. This amounted to 15
minutes per subject per day, resulting in 4 hours of total observations per day. I
randomized the order of exhibits sampled each day to avoid any order or time-of-day
effects.
Behavioral observations of both species in each group were made using
continuous focal sampling, noting proximity, general activities, and social interactions
within and between species. I focused on locomotion, affiliation, play, grooming,
agonism, as well as non-social activities such as positional behavior, habitat-use, and
feeding (see Table 1). The daily feeding and care-taking schedule of the primates remained unaltered, but I worked with the zoo staff to plan observations around their
routines, in order to maximize data collection opportunities.
Given the lack of sufficient comparative data for the titi-Goeldi’s and swamp
monkey-guereza groups, and the unscheduled introduction of a third species into one of
the subject groups during the study, analysis was limited to data collected on the howler
monkey-saki-tamarin mixed-species exhibit. Data from the former two groups were used anecdotally to supplement the statistical results. Behavioral data were summed and
converted to percentages of total sample time for subjects and groups. Data were
analyzed using non-parametric statistics with two-tailed probability values using
MINITAB software.
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RESULTS Solitary and Social Behaviors Titis, Goeldi’s monkeys, Allen’s swamp monkeys, guerezas Amongst the titi-Goeldi’s monkey and Allen’s swamp monkey (ASM)-guereza
exhibits, there was almost no direct contact between heterospecifics. Therefore, sociality
of the two species in each exhibit could only be approximated through proximity data
(Table 2). The titis were often observed in close proximity with one another (40.3%), but
were only seen to be in proximity to the Goeldi’s monkeys 0.01% of the time. Similarly,
the Goeldi’s monkeys also preferred to be near a conspecific versus a titi monkey (50.1%
and 0.03%, respectively). While the ASM-guereza exhibit had more instances of inter-
species interactions, these occurrences were still relatively uncommon. The ASMs were
observed to be in proximity to another ASM 39.3% and to a guereza less than one percent
of the time. Likewise, guerezas were found to be in proximity to another guereza more
frequently than an ASM (6.37%, 0.08%). However, it should be noted that while often
not within proximity (as defined for this study), the guereza were just out of arm’s reach
of one another for the majority of the time.
Howling monkeys The most frequent behaviors, both solitary and social, of the howling monkeys are
listed in Table 3. The majority of their activity budget consisted of resting (group
average of 81.9%), followed by allogrooming and eating (group average of 10.0% and
3.8%, respectively). There were no statistically significant differences in any behavior between the two research conditions (i.e. on exhibit with sakis, H0, or on exhibit alone,
H1). In addition, well over half of the time was spent in proximity to another howler.
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Sakis The activity budget of the sakis greatly differed between the three research
conditions (i.e. on exhibit with howlers, S0; off-exhibit with and without tamarins, S1;
and on exhibit with tamarins, S2), but the three most common behaviors were rest,
locomote, and eat. The male saki spent significantly less time resting (H=5.99, df=2,
p=0.05; Figure 1) and more time eating (H=9.58, df=2, p=0.008) when on exhibit with
the howling monkeys than in either of the other two conditions. Percentage of time spent
locomoting was similar for both on exhibit conditions but was significantly less
(H=13.61, df=2, p=0.001) when off-exhibit. Occurrences of self groom were relatively
comparable for conditions S0 and S1, while no grooming (either self or social) was
observed for the male saki while on exhibit with the tamarins. Social groom occurred significantly more off-exhibit than when on exhibit (H=9.19, df=2, p=0.01). Social play by the male was only observed when off exhibit (H=6.37, df=2, p=0.041). The male saki was most often in proximity to the female saki when off exhibit (H=6.07, df=2, p=0.049) and slightly more so when on exhibit with the tamarins than with the howlers, but this difference was not significant.
The behaviors of the female saki were generally similar to that of the male, but
also showed different variations between conditions (Figure 2). Percentage of time spent
resting, eating, and foraging did not differ between conditions, while locomoting
significantly increased (H=5.99, df=2, p=0.05) when on exhibit with the tamarins. Self
groom was the same for conditions S0 and S2 and did not occur at all off exhibit
(H=11.97, df=2, p=0.003), while social groom was never observed for the female saki while on exhibit with the tamarins. Like the male, the female only socially played off
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exhibit, but not at a significantly different amount than when on exhibit. The female
spent relatively little amount of time in proximity to the male, but did so more when in
holding than when on exhibit (H=10.0, df=2, p=0.007).
Overall, the sakis as a pair did not exhibit significant changes of amount of resting or foraging between conditions (Figure 3). Both eating (H=8.12, df=2, p=0.017) and self groom (H=17.15, df=2, p=0.000) were observed more often when on exhibit with the howling monkeys than the other conditions. Similarly, social groom occurred more in conditions S0 and S1 and did not occur at all for S2 (H=10.07, df=2, p=0.007). When off exhibit, the sakis showed less locomotion (H=14.66, df=2, p=0.001), the only instances
of social play (H=9.55, df=2, p=0.008), and greater proximity to one another (H=15.06,
df=2, p=0.001).
Location Howling monkeys The howling monkeys spent the majority of the time in the top half of their
exhibit (group average 91.6%) (Table 4). They spent about 6.4% on average in the
bottom half and only 2.0% on the floor. Overall, the group spent a little more than half of
the time (group average 60.9%) in the back of their exhibit. These location preferences
were comparable both when the howlers were with the sakis and without. The only
exception is Female3’s preference for the back half of the exhibit when with the sakis
(79.0%) and the front half of the exhibit when without the sakis (61.3%; W=464,
p=0.096).
Sakis Figure 4 shows the percentages of total sample time that the sakis spent in each
area of their enclosures (floor is excluded as sakis were never observed on the floor).
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The male saki significantly spent the most amount of time in the top half of the enclosure when off exhibit and spent the majority of his time in the bottom half of the exhibit when with the tamarins (H=25.30, df=2, p=0.000). When on exhibit with the howlers, he spent most of the time in the back half of the exhibit, but showed a strong preference for the front half of the exhibit during the other two conditions, especially when off exhibit
(H=24.54, df=2, p=0.000). The female’s patterns of enclosure use differed slightly with the majority of time spent in the top half of the enclosure during all three situations, but less so when on exhibit with the tamarins (H=28.17, df=2, p=0.000). The female was observed more frequently in the back half of the enclosure when on exhibit (both with howlers and tamarins, but more so with the former) and in the front half of the enclosure when off-exhibit (H=40.02, df=2, p=0.000).
DISCUSSION Solitary Behaviors and Social Interactions In general, there were very few instances of direct inter-species interactions in any of the three exhibits. Instead, the social interaction could be described as mutual tolerance. In each exhibit, each species group had frequented spots that the other species would rarely approach, enter, or cross. Most often, this was a reflection of niche diversity found amongst these species in the wild. For example, both guerezas (Colobus guereza) and titi monkeys (Callicebus sp.) occupy the upper levels of the canopy, while their exhibit-mates (in this case Allen’s swamp monkeys and Goeldi’s monkeys) normally occupy lower levels, with swamp monkeys mostly on the ground (McGraw,
1994; Buchanan-Smith et al., 2000). The only occurrences of aggression observed, albeit rare and always non-contact, occurred over food; this happened a bit more frequently in
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the titi-Goeldi’s exhibit, as they have very similar diets. In addition, I only observed one
instance of intentional direct contact between species in these exhibits. The oldest juvenile Allen’s swamp monkey had a habit (as confirmed by the zoo keepers) of
“playing” with or grooming a guereza’s tail if the right opportunity came along. The event that I witnessed ended abruptly when the swamp monkey decided to stop grooming and start pulling; however, even this did not evoke a more aggressive response from the guereza than to simply run away.
The results of the more in-depth part of this study are consistent with other
research on Alouatta behavioral patterns (e.g. Bravo and Sallenave, 2003; Russak, 2005;
Estrada et al., 1999), with howling monkeys spending most of their day resting and
eating; this pattern is likely a reflection of their mostly folivorous diet which requires
large amounts of time and energy spent digesting low-quality food. The considerable
amount of time these howlers spent in proximity to one another and allogrooming also
compares favorably to behavior observed in field studies, and serves to strengthen social
bonds within the group (Bravo and Sallenave, 2003). As the activity budget of the
howlers in this study mirrored that of their wild counterparts and was not significantly
affected by the presence or absence of another species (i.e. the sakis), howlers (at least in
this study) seem like a good candidate for mixed-primate exhibits in captivity. This is supported by my observations of only one instance of non-contact aggression by the male
howler towards the male saki (who was the initiator) during the whole 12-week study
period. In addition, the zoo keepers have reported numerous attempts at housing other
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primate species with the howlers, and only had to discontinue these matches due to
aggressive behavior on the part of the other species and never the howlers.
In contrast, the behavior of the sakis was greatly negatively affected by
circumstances including change of enclosure and housing partners. During the first part
of this study the sakis were on exhibit with the howling monkeys, the normal grouping
that had been established for some time. As howling monkeys and sakis (although not
necessarily the two species in this study) are also sympatric in the wild (Lehman, 2000),
it is reasonable to assume that the behavioral patterns during this condition were
“normal” for the sakis. In fact, Vie et al. (2001) showed an activity budget for Pithecia
pithecia, with resting, moving, and eating as the main behaviors, which is comparable to
this study. When the sakis were moved off-exhibit to begin the introduction process with
the pied tamarins, they were housed in a smaller enclosure. This likely accounts for the
decrease in amount of locomotion and increase in proximity during this phase. What is
most interesting is the occurrence of social play between the mother-son pair while off-
exhibit, as no social play was observed while the sakis were on exhibit; usually this
consisted of chasing and play wrestling, initiated by the son. It is possible that the sakis
felt more at ease without having other primates to worry about competing for resources such as food and space.
It is clear from the results of this study, that the introduction of the tamarins into
the saki exhibit altered the behavioral patterns of the sakis. Most noticeable is the
complete lack of social grooming by the sakis; it is likely that the sakis occupied their
time instead with being vigilant of their new exhibit-mates. It is also interesting to note
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that while not significantly different, the sakis spent more time in proximity to one
another while on exhibit with the tamarins than with the howlers (4.9% and 3.0%,
respectively); this also is a reflection of their uneasiness. Unlike the howling monkeys,
the sakis were extremely affected by the change in their surroundings. While this
grouping is likely to stabilize over time, these results are important in showing that sakis
need more monitoring and perhaps a longer introduction period than the more laid-back
howlers when forming a mixed-species exhibit.
Location Once again the howling monkeys did not show any overall significant differences in the spatial use of their exhibit across conditions. Their general preference for the top half of the enclosure reflects preferences for upper canopies in the wild (Bravo and
Sallenave, 2003). Their preference for the back half of the exhibit was likely a by- product of their liking of a rope ladder that hung in this part of the exhibit, as this is where the howlers spent most of their time resting. During the study this ladder unfortunately broke and it is at this point where slight changes occurred in the use of the exhibit. One of the females found a new preferred spot more towards the front of the exhibit, thus seemingly changing her preferences. This female shifting closer to the front, in addition to frequent occasions of howlers right up against the window, leads me to believe that the tendency to be in the back was indeed correlated to resting spot preference and not out of a fear of the public, as might have been otherwise thought.
The location of the sakis within their enclosures differed immensely between the
varying conditions of the study. When on exhibit with the howlers, both the male and
female sakis showed extreme preferences for the top, back half of the exhibit. This
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reflects the middle to upper canopy niche they occupy in the wild (Vie et al., 2001).
While off-exhibit, the sakis still preferred the top half of their enclosure, but were more
frequently observed in the front half. This is once again most likely the by-product of external circumstances, as the front of the enclosure was closer to the keepers and gave the sakis better visual access to what the keepers were doing. This seems a plausible explanation, as when put back on exhibit with the tamarins, the sakis went back to spending more time in the back. However, during this part of the study, the sakis were more frequently observed in the bottom half of the exhibit. As this does not correlate to their natural behavior (both from field data and when with the howlers), it is clear that the presence of the tamarins altered their actions.
Implications and Future Studies The results of this study show that social interactions among captive mixed-
primate groups are generally passive, as the pressures (i.e. foraging and predation) that
drive such associations in the wild are absent. Within captive groups, some primate
species are more tolerant or less affected by the presence of another species (i.e. howlers), that some species are more aggressive (i.e. tamarins), and that others take a more submissive and stressed role (i.e. sakis). Furthermore, it is clear that one cannot assume that simply because species are sympatric in their natural habitats (e.g. sakis and tamarins) that they will instantly form a well-suited mixed-species group in captivity.
However, species that do associate with one another in the wild are still the best candidates for such exhibits. In order to determine what other groupings are successful, zoos need to continue to communicate past failures and successes with one another. In addition, while there have been some studies on the formation of mixed-species exhibits
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(e.g. Wojciechowski, 2004), more formal research needs to be done during the
introduction processes so that zoos know what to expect, what behaviors are acceptable,
and what signs to look for to indicate if the grouping will do well. Mixed-species groups are an important feature to have in zoos as they provide more stimulating exhibits for both the public and the animals involved.
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REFERENCES
Azevedo Lopes MAO, Rehg JA. 2003. Observations of Callimico goeldii with Saguinus imperator in the Serra do Divisor National Park, Acre, Brazil. Neotropical Primates 11: 181-183.
Bravo SP, Sallenave A. 2003. Foraging behavior and activity patterns of Alouatta caraya in the northeastern Argentinean flooded forest. International Journal of Primatology 24: 825-846.
Buchanan-Smith HM, Hardie SM, Caceres C, Prescott MJ. 2000. Distribution and forest utilization of Saguinus and other primates of the Pando Department, Northern Bolivia. International Journal of Primatology 21: 353-379.
Chapman CA, Chapman LJ. 1996. Mixed-species primate groups in the Kibale Forest: ecological constraints on association. International Journal of Primatology 17: 31-50.
Chapman CA, Chapman LJ. 2000. Interdemic variation in mixed-species association patterns: common diurnal primates of Kibale National Park, Uganda. Behavior, Ecology, Sociobiology 47: 129-139.
Eckardt W, Zuberbühler K. 2004. Cooperation and competition in two forest monkeys. Behavioral Ecology 15: 400-411.
Estrada A, Juan-Solano S, Martinez TO, Coates-Estrada R (1999). Feeding and general activity patterns of a howler monkey (Alouatta palliata) troop living in a forest fragment at Los Tuxtlas, Mexico. American Journal of Primatology 48: 167-183.
Hardie SM, Prescott MJ, Buchanan-Smith HM. 2003. Ten years of tamarin mixed- species troops at Belfast Zoological Gardens. Primate Report 65: 21-38.
Lehman SM. 2000. Primate community structure in Guyana: a biogeographic analysis. International Journal of Primatology 21: 333-351.
McGraw S. 1994. Census, habitat preference, and polyspecific associations of six monkeys in the Lomako Forest, Zaire. American Journal of Primatology 34: 295- 307.
Norconk M. 1990. Introductory remarks: ecological and behavioral correlates of polyspecific primate troops. American Journal of Primatology 21: 81-85.
Porter LM. 2001. Benefits of polyspecific associations for the Goeldi’s monkey (Callimico goeldii). American Journal of Primatology 54: 143-158.
- 27 -
Rose LM, Perry S, Panger MA, Jack K, Manson JH, Gros-Louis J, Mackinnon KC, Vogel E. 2003. Interspecific interactions between Cebus capucinus and other species: Data from three Costa Rican sites. International Journal of Primatology 24: 759-796.
Russak SM. 2005. Getting the hang of it: age differences in tail-use by mantled howling monkeys (Alouatta palliata). Neotropical Primates 13: 5-7.
Stensland E, Angerbjörn A, Berggren P. 2003. Mixed species groups in mammals. Mammal Review 33: 205–223.
Struhsaker TT. 1981. Polyspecific associations among tropical rain-forest primates. Zeitschrift fur Tierpsychologie 57: 268-304.
Terborgh J. 1990. Mixed flocks and polyspecific associations: costs and benefits of mixed groups to birds and monkeys. American Journal of Primatology 21:87- 100.
Thomas WD, Maruska EJ. 1996. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S (eds.). Wild mammals in captivity: principles and techniques. Chicago: University of Chicago Press, pg 204-211.
Vie JC, Richard-Hansen C, Fournier-Chambrillon C. 2001. Abundance, use of space, and activity patterns of white-faced sakis (Pithecia pithecia) in French Guiana. American Journal of Primatology 55: 203–221.
Waser P. 1982. Primate polyspecific associations: do they occur by chance? Animal Behaviour 30: 1-8.
Wojciechowski S. 2004. Introducing a fourth primate species to an established mixed- species exhibit of African monkeys. Zoo Biology 23: 95-108.
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Table 1. Ethogram
Behavioral Pattern Definition
Rest Little or no gross body movement; eyes opened or closed; posture variable
Eat Consume food
Forage Search for food
Locomote Move from one place to another
Solitary Play Actively explore or manipulate environment
Social Play Non-aggressive, rough-and-tumble interaction of subject and another
Displaced Move at least touching distance away from approaching subject
Contact aggression Grab, bite, slap, or grapple, etc. with another
Non-contact aggression Chase, lunge, threat, etc. at another
Present Orient rump toward another individual
Social Groom Pick through fur of another
Self Groom Pick through own fur
Proximity Within touching distance of focal subject
Copulation Mounts and copulates with another individual
Spacing Subject’s location in exhibit: Top-Bottom Ceiling, Top ½, Bottom ½, Floor Back-Front Back ½, Front ½ **All categories apply to individuals of all species present
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Table 2. Proximity data for two mixed-primate groups, expressed as percentage of total sample time Subject Neighbor Proximity
TITI Titi 40.3% Goeldi’s monkey 0.01%
GOELDI’S MONKEY Goeldi’s monkey 50.1% Titi 0.03%
ALLEN’S SWAMP MONKEY Allen’s Swamp monkey 39.3% Guereza 0.03%
GUEREZA Guereza 6.37% Allen’s Swamp monkey 0.08%
Table 3. Partial behavioral repertoire of howling monkeys, expressed as percentages of total sample time (bold* indicate significant difference at α = 0.05, Mann- Whitney U test) *RST EAT FOR LOC SGR SPL SCGR PROX **H0 H1 H0 H1 H0 H1 H0 H1 H0 H1 H0 H1 H0 H1 H0 H1 *F1 81.4 81.6 3.9 2.3 2.7 1.3 2.0 0.9 0.2 0.0 2.1 1.5 12.5 11.8 83.7 76.9 F2 79.5 84.7 6.5 5.1 1.1 0.7 1.6 1.0 3.7 4.4 0.0 0.0 7.6 4.1 80.8 77.5 F3 69.4 87.8 3.3 2.4 0.7 0.0 2.4 0.7 0.3 0.0 2.9 0.3 21.4 8.8 75.1 76.4 M1 85.4 85.2 2.5 4.2 0.6 0.8 2.5 1.9 0.1 0.0 0.4 1.9 8.3 5.3 84.9 77.5 GROUP 79.0 84.8 4.1 3.5 1.3 0.7 2.1 1.1 1.0 1.1 1.3 0.9 12.5 7.5 81.1 77.1 *RST=rest, FOR=forage, LOC=locomote, SGR=self groom, SPL=social play, SCGR=social groom, PROX=proximity to another howler, F=female, M=male **H0 represents condition of howlers with sakis on exhibit, H1 represents conditions of howlers alone on exhibit
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Table 4. Location of howling monkeys within exhibit, expressed as percentages of total sample time (bold* indicate significant difference at α = 0.05, Mann-Whitney U test) TOP BOTTOM FLOOR BACK FRONT H0 H1 H0 H1 H0 H1 H0 H1 H0 H1 F1 90.3 96.3 6.7 0.5 3.1 3.2 83.1 69.7 16.9 30.3 F2 93.5 92.3 6.1 6.6 0.4 1.0 53.6 57.0 46.4 43.0 F3 86.8 90.8 9.6 7.7 3.6 1.4 79.0* 38.7* 21.0* 61.3* M1 93.8 89.1 4.7 9.1 1.3 1.8 56.7 49.3 43.3 50.7 GROUP 91.1 92.1 6.8 6.0 2.1 1.9 68.1 53.6 31.9 46.4 *RST=rest, FOR=forage, LOC=locomote, SGR=self groom, SPL=social play, SCGR=social groom, PROX=proximity to another howler, F=female, M=male **H0 represents condition of howlers with sakis on exhibit, H1 represents condition of howlers alone on exhibit
80.0
S0 S1 S2 70.0
*
60.0
50.0
40.0
30.0
* 20.0 *
10.0
* * * * 0.0 * * REST EAT FORAGE LOCOMOTE SELF GROOM SOCIAL PLAY SOCIAL PROXIMITY TO GROOM SAKI
Figure 1. Partial behavioral repertoire of male saki in percentages of total sample time; asterisks within each behavioral category indicate significant difference at α = 0.05, Kruskal Wallis test (S0 represents condition of sakis on exhibit with howlers, S1 represents condition of sakis off-exhibit in holding both with and without tamarins, S2 represents condition of sakis on exhibit with tamarins)
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80.0
S0 S1 S2 70.0
60.0
50.0
40.0
30.0 *
20.0 * * 10.0
* * 0.0 REST EAT FORAGE LOCOMOTE SELF GROOM SOCIAL PLAY SOCIAL PROXIMITY TO GROOM SAKI
Figure 2. Partial behavioral repertoire of female saki in percentages of total sample time; asterisks within each behavioral category indicate significant difference at α = 0.05, Kruskal Wallis test (S0 represents condition of sakis on exhibit with howlers, S1 represents condition of sakis off-exhibit in holding both with and without tamarins, S2 represents condition of sakis on exhibit with tamarins)
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80.0 S0 S1 S2 70.0
60.0
50.0
40.0
30.0
* 20.0 *
* 10.0 * * * * * * 0.0 REST EAT FORAGE LOCOMOTE SELF GROOM SOCIAL PLAY SOCIAL PROXIMITY TO GROOM SAKI
Figure 3. Partial behavioral repertoire of saki pair in percentages of total sample time; asterisks within each behavioral category indicate significant difference at α = 0.05, Kruskal Wallis test (S0 represents condition of sakis on exhibit with howlers, S1 represents condition of sakis off-exhibit in holding both with and without tamarins, S2 represents condition of sakis on exhibit with tamarins)
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100 * * * S0 S1 S2 90 * *
80 * *
70
60 * * 50 * * * 40
30 *
* 20 *
* 10
0 M1 F1 PAIR M1 F1 PAIR TOP BACK
Figure 4. Location of sakis within enclosure in percentages of total sample time; asterisks for each subject indicate significant difference at α = 0.05, Kruskal Wallis test (S0 represents condition of sakis on exhibit with howlers, S1 represents condition of sakis off-exhibit in holding both with and without tamarins, S2 represents condition of sakis on exhibit with tamarins; “floor” is excluded as sakis were never observed on the floor; “bottom” and “front” are excluded as percentages are complimentary to “top” and “back”)
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