David Birch
1. Introduction
Organisms within ecological communities are linked together by biotic relationships
like competition, predation, and mutualism. Sociality and the formation of groups
includes both elements of mutualism and competition, and the evolution of sociality
and the mechanisms of group living have received much consideration (Heymann and
Buchanan-Smith, 2000).
Two of the most important selective advantages for animals living in groups are
increased protection from predators, and increased likelihood of finding or capturing
food. To be weighed against these benefits are costs of group living such as increased
competition for food or mates, and increased conspicuousness to predators (Krebs and
Davies 1987).
Groups are usually formed by conspecifics, but as a special kind of interspecific
relationship within communities, groups may also be composed of members from
different species (Heymann and Buchanan-Smith, 2000). Some of the benefits of
group-living can be enhanced, and some of the costs reduced, by living in mixedspecies groups or MSGs as opposed to single-species groups or SSGs. This is because
niche differentiation and differing resource use patterns between species means that
food competition is reduced, and sexual competition is often eliminated, (unless
hybridisation occurs between closely related species (Buchanan-Smith 1990)). This
allows an increase in group size without the constraints of intra-specific competition.
Among primates, mixed-species associations are most commonly observed in African
monkeys of the genus Cercopithecus, and New World monkeys of the genus Saguinus
(Bicca-Marques and Garber 2003).
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It is the MSGs within the genus Saguinus, more specifically, the costs and benefits of
these associations to Saguinus fuscicollis, which this study investigates.
Tamarins of the genus Saguinus are small bodied (250-650g) neotropical primates.
They are diurnal, arboreal, and may be described as frugivore-insectivores (Prescott
and Buchanan-Smith 2002). However they are known to have a varied diet and
consume small vertebrates, nectar, and exudates as well as fruit and invertebrates
(Prescott, Buchanan-Smith, and Smith 2005). Within the tamarin breeding system
there is generally only one reproductive female. Although their mating systems are
described as flexible, monogamy still appears to be the most common, and polyandry
more common than polygyny (Buchanan-Smith 1999).
Tamarins are vulnerable to a wide range of predatory birds, reptiles and mammals,
and it has been suggested that, due to their small size, they have higher rates of
predation relative to larger bodied primates (Prescott and Buchanan-Smith 2002).
Given such high predation risk, it is expected that anti-predatory considerations may
impose strong constraints on tamarin foraging behaviour (Peres 1992).
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1.1 The study species
Figure 1
Saguinus fuscicollis. Photograph by A. Zeller (2008).
The focus of this study is the Saddle-back tamarin Saguinus fuscicollis (Fig. 1),
which has the largest distribution of the tamarins (Prescott, Buchanan-Smith, and
Smith 2005), and forms consistent, stable mixed-species groups with heterospecifics
wherever congeners are found in sympatry (Fig. 2). More specifically, the subspecies
under investigation is S. f. illegeri, which occurs in an area of north-eastern Peru in
isolation from congeners (Fig. 3), and therefore obviously cannot form MSGs.
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a
b
c
d
Figure 2
The known range of occurrence of S. fuscicollis (a), S. mystax (b), S. labiatus (c), and
S. imperator (d). Taken from IUCN (2008).
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Figure 3
A more detailed range map for S. fuscicollis displaying the different ranges of the
different S. fuscicollis subspecies. Taken from IUCN (2008).
MSGs have been reported between saddle-back tamarins and either moustached
(S.mystax), red-bellied (S. labiatus), emperor, (S. imperator) or black-mantle
tamarins, S. nigricollis (Windfelder 2001). Also they have been found to associate
with Snethlage’s marmosets (Callithrix emiliae) (Smith 2004), Goeldi’s monkey
(Callimico goeldii) and sometimes Squirrel monkeys (Saimiri boliviensis) (Soini
1987). The four tamarin species that are sympatric to S. fuscicollis are mostly or
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wholly allopatric to one another (Norconk 1990).
These associations between tamarin species are some of the most stable within
Primates (Garber 1987). Previous studies have revealed a continuum of stability in
mixed-species tamarin troops: S. fuscicollis form the most permanent associations
with S. mystax, S. fuscicollis and S. labiatus show intermediate levels of association,
and S. fuscicollis and S. imperator show the lowest levels of association (BuchananSmith 1999; Peres 1992).
Each mixed-species troop is made up of a reproductive group of each species (Smith
et al 2005) which feed, forage, rest, and travel together during much of the year
(Bicca-Marques and Garber 2003).
Tamarins usually form MSGs with only one other congeneric troop, i.e. it is always
the same pair of groups which are found in association (Norconk 1990).
These troops share a common home range. Home ranges are usually around 0.2-0.4
km², although it has been reported that mixed troops of S. mystax and S. fuscicollis
utilized home ranges of more than 1 km² (Peres 1992). MSGs defend these home
ranges together, against neighbouring troops (Heymann and Buchanan-Smith, 2000).
Time spent in association varies during the daily activity period. The degree of
association also varies from day to day (Buchanan-Smith 1991).
1.3 The benefits of being in a mixed-species group
Costs and benefits of MSGs may vary considerably depending on seasonal changes in
food availability and distribution, facultative changes in troop cohesion, site-specific
differences in predation risk, and species differences in foraging strategies (BiccaMarques and Garber 2003).
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Functional explanations for MSGs usually fall within two categories: foraging
advantages and predator avoidance. The advantages do not have to be equally
distributed between the participating species (Stensland, Angerbjorn and Berggren
2003).
The primary benefits of tamarin MSGs may include enhanced vigilance against
predators, as well as an increased ability to defend productive feeding sites. Mixed
associations are considered as adaptations for achieving an optimal balance between
predator protection and feeding efficiency. The geographical occurrence of habitual
primate polyspecific associations corresponds to regions harbouring large monkeyeating raptors (Terborgh 1990).
1.3.2 Increased vigilance
MSGs of tamarins are in general larger than SSGs (Heymann and Buchanan-Smith
2000), and can frequently involve a doubling of numbers (Buchanan-Smith 1999).
The effect group size has on the effectiveness of anti-predator strategies has been
well-established. An increase in group size can have multiple benefits against the
threat of predation. The first is safety in numbers, a purely statistical effect, whereby
as the group size increases, the probability of any individual being attacked decreases
(Terborgh 1990). This however does not take possible individual differences between
group members into account. Groups may display a distinctly non-random internal
spatial organisation. This is true of mixed tamarin groups as S. fuscicollis always
spends the majority of time on the lower levels of the forest, and thus could be more
vulnerable to certain predators (Buchanan-Smith 1999; Norconk 1990.
In a larger group there are more eyes and ears for the detection of predators- making
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predator detection more likely. The efficacy of this mechanism rests on the
transmission of warning signals (Terborgh 1990). The alarm calls of tamarins fall into
this category, and the alarm calls of associating cogenerics are mutually undersood
(Heymann 1990). A further benefit of the increased group vigilance rates is that there
is a reduction in the need for vigilance at the individual level, thus freeing up more
time for other important behaviours such as forgaing (Terborgh 1990).
Alpha males of all the tamarin species display sentinel behaviour (Bicca-Marques
and Garber 2005). It is thus likely that mixed-species groups which then inherently
have two alpha-males, will presumably consequently have two sentinels that are
dedicated to vigilance, which may infer anti-predatory benefits for the whole group.
Also MSGs have been found to have complementary vigilance.
Peres (1993) found that in MSGs, the S. fuscicollis accounted for most of the
vigilance and detection of terrestrial and scansorial threats, whereas S. mystax scanned
for and detected most aerial and arboreal threats. Similarly, Buchanan-Smith and
Hardie (1997) reported S. labiatus looked up more often than saddleback tamarins.
This increases the likelihood of the detection of a raptor, tamarin’s biggest predatory
threat (Peres 1993).
1.3.3 Increased foraging efficiency
S. fuscicollis within MSGs can benefit from the shared or parasitized knowledge of
food resources from the other species, and the different species can transmit
information to one another (Windfelder 2001).
It has been shown that S. mystax more often encounter large productive food patches
located higher in the forest that could accommodate the entire mixed-species troop,
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while S. fuscicollis more often encounter smaller food patches lower in the forest
(Heymann and Buchanan-Smith 2000).
It has also been shown that the two species can learn from one another. Prescott et al
(2005) in experimental studies of S. labiatus and S. fuscicollis, found that an
individual’s food aversion is modified equally well by social interaction with nonaverse individuals from either species. This means that individuals from both species
can learn from congeneric group members, of ripe fruit for example, quicker than
SSGs which are generally smaller. This would increase the foraging efficiency of
individuals within MSGs.
Another potential benefit for S. fuscicollis within MSGs is ‘insect flushing’. Each of
the different congeneric species to S. fuscicollis travels and forages significantly more
in higher levels of the forest, and in so doing disturbs a number of different
invertebrates which fly or fall to the lower levels (Heymann and Buchanan-Smith). It
has been shown that S. fuscicollis are adept at locating the landing point of insects
flushed by S. mystax to the forest floor or lower strata and retrieving them (Heymann
and Buchanan-Smith 2000). Animal prey represents the highest quality dietary
component for wild tamarins, and in one study over 70% of the prey biomass
harvested by S. fuscicollis was flushed prey (Peres 1992b), making this a potentially
substantial benefit.
There is also a possibility that S. fuscicollis in MSGs benefit from a reduced need to
expend energy in territorial defence because it has been shown that the congener
invests more energy into this activity.
Peres (1992) found that S. fuscicollis spent significantly more time resting during
inter-group encounters, and would often see the S. fuscicollis resting as far as 40
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metres away from the fight, adopting a role of ‘standby spectator’ whilst the S. mystax
invested significantly more time and effort in territorial defence. This activity is
energy intensive as the agonistic encounters between groups involve a lot of
vocalising and movement (Peres 1992).
Additionally, and key, the benefits of this defence may also be greater for S.
fuscicollis. This is because on average, S.fuscicollis feed on smaller fruit patches than
S. mystax, and spend a lot of time searching for non-mobile and embedded prey in
small microhabitats (Smith 2000). These feeding resources would be much more
easily and swiftly depleted by rival groups.
Further, S. fuscicollis prey capture success was found to be higher in the core of the
group’s home range as compared to the periphery, where other groups may deplete
resources (Peres 1992).
S. fuscicollis thus emerge as the net beneficiary of the tamarins' joint territorial
system, enjoying a protective shadow against resource depletion by other groups,
which is provided primarily by the S. mystax which devote greater effort in range
defence.
1.4 The costs of being in a mixed-species group
However there are also foraging costs accrued by S. fuscicollis within MSGs, and
costs associated with maintaining association with another species.
1.4.1 Foraging efficiency
The main foraging costs proposed for these associations are the presumed effects of
increased troop size on feeding competition, through either interference and/or
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exploitation, and an increase in the day range required to locate a greater number of
feeding sites or more productive feeding sites (Heymann and Buchanan-Smith 2000).
In this regard, foraging costs are expected to be higher for S. fuscicollis, especially
with small, highly monopolizable feeding patches, because they are subordinate to
other tamarin species because they are smaller (Heymann 1990). Although
interspecific agonistic interactions between tamarins are relatively rare (Heymann
1990), they have been reported to occur mainly over monopolizable fruit, exudate, or
nectar sources where the smaller S. fuscicollis is almost always the loser and is
displaced (Bicca-Marques and Garber 2003; Heymann 1990 ).
In Garber’s (1987) study of MSGs of S. fuscicollis and S. mystax, 74 % of the 166
fruit and exudate trees fed in by S. mystax were also visited by S. fuscicollis.
Similarly, 9 of the top 10 tree species in the diet of S. mystax also were among the top
10 species in the diet of S. fuscicollis. These species accounted for between 69 % and
75 % of feeding time respectively.
This extensive dietary overlap in the fruit portion of the diet, coupled with the
knowledge that the larger congeners routinely monopolise and exclude S. fuscicollis
from feeding resources, even if it was the S. fuscicollis that had found the resource,
would lead to the presumption that extensive foraging costs are incurred by S.
fuscicollis whilst in MSGs.
However this does not seem to be the case, as divergence between the species can be
found within other aspects of the diet.
Studies on MSGs of S. fuscicollis and S. mystax have found that the two species
forage for, and capture invertebrate prey from, significantly different substrates within
the forest (Smith 2000).
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Feeding competition in general is reduced by niche differentiation between the
different species. Patterns of habitat use within MSGs of tamarins maintain spatial
segregation, by differences in support use, vertical stratification, and inter-individual
spacing (Norconk 1990).
A clear pattern can be seen with regard to vertical stratification. S. fuscicollis is
usually found at lower heights than their congeners, and vertical stratification is most
pronounced during resting, travelling, and foraging (Buchanan-Smith 1999).
It has thus been suggested that within-troop feeding competition is generally not a
critical factor in the feeding ecology of mixed-species groups (Garber 1988).
1.4.2. Maintaining association and increased conspicuousness to
predators
All individuals within a MSG are actively involved in maintaining the association and
group cohesion (Heymann and Buchanan-Smith 2000). The mechanisms by which
this is done include: antiphonal calling (Pook & Pook, 1982; Heymann, 1990; Peres,
1991), backtracking and calling when separated (Pook & Pook, 1982; Terborgh, 1983;
Buchanan-Smith, 1990) and choosing sleeping sites relatively close to one another
(Peres, 1991). These actions are likely to incur energetic costs, and they may also alert
potential predators to the group (Heymann and Buchanan-Smith 2000).
However, interspecific calling has been found to be much rarer than intraspecific
calling, and so the rareness of these interactions are thought to keep the costs they
incur very low (Heymann 1990). Further, that MSGs are more conspicuousness to
predators has not been quantified with predation rates, and is likely to be in part offset
by increased vigilance within MSGs.
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1.5 Aims of this investigation
Given the overall benefits that theoretically come from being within a MSG for S.
fuscicollis, this study aims to investigate the consequences of being without an
associating congener for individual S. fuscicollis, in terms of habitat use and
behaviour, and to discuss these in terms of the relevance to the conservation of the
species. This will be done by comparing data from this study with other studies of
Saguinus MSGs.
Experimental hybridizations of S.f. illegeri and S.f. lagonotus, found evidence of
hybrid vigour as hybrid infants were found to have significantly higher survival rates,
which suggests genetic divergence between the subspecies, and possible reproductive
isolation in the wild (Jaquish 1994).
Further evidence of genetic divergence between subspecies comes from a study by
Cheverud et al (1993) which also looked at S.f. illegeri. The study found that there are
large differences in allele frequencies among subspecies for genes affecting
craniofacial morphology. This suggests that the subspecies are likely to be
independent, largely isolated, evolutionary units. This could mean that the S.f. illegeri
observed within this study, due to genetic isolation, may have evolved different
patterns of behaviour as an adaptation to living within SSGs.
Five hypotheses to be tested within this investigation are proposed as theoretical
predictions of what such differences in behaviour and habitat use could be.
These are:
Hypothesis 1
The average group size found in the study area will be larger than the average size of
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S. fuscicollis groups within MSGs, due to selective pressure from predation for
increased vigilance.
Hypothesis 2
The S. fuscicollis in MSGs are displaced from utilising higher levels in the forest by
dominant congeners. The S. fuscicollis in the study area will therefore use the upper
levels of the forest more than S. fuscicollis within MSGs. They will feed, forage,
travel, and rest at a wider variety of heights in the forest, as they are not constrained
by a dominant congener.
Hypothesis 3
The S. fuscicollis in the study area will spend more time travelling and foraging and
so less time resting, because of a reduced foraging efficiency without the aid of a
congener. In the absence of the potential knowledge a congener could share about the
location of feeding sites, as well as the absence of ‘insect flushing’ from the congener,
the S. fuscicollis in this study will have to travel more to find feeding sites, and forage
more to compensate for the lack of insect flushing. This will leave less time for
resting.
Hypothesis 4
The diets of the S. fuscicollis within the study area will have proportionately less
insects than the diets of S. fuscicollis within MSGs, because of the lack of insect
flushing.
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Hypothesis 5
The S. fuscicollis within the study area will spend more time being vigilant, to
compensate for the reduction in overall group size and lack of complimentary
vigilance which comes with being in MSGs.
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