The Behavioural Ecology of Saddleback Tamarins
(Saguinus fusicollis illigeri)
DI512: Practical Research Project, 2010
by Grace Turner
BSc Wildlife Conservation
Durrell Institute for Conservation and Ecology
University of Kent, Canterbury
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
By Grace Turner
ACKNOWLEDGEMENTS :
I would like to thank Tatyana Hulme, Christine Eagle and Cliff Turner for their regular
support and patience. Thanks are also due to Richard Bodmer for organising the field trip,
and David Birch for his past research at Pacaya-Samaria. A special mention goes to
Romer (my Peruvian field-guide), as without his expert tamarin tracking ability, this study
would have been impossible. Acknowledgement is given to Heather Jenkins and Declan
Crace, whose photography skills and moral support in the field provided me with
encouragement and shared a love for the tamarins.
ABSTRACT:
Saguinus fusicollis illigeri are cooperatively breeding, arboreal insectivorous New World
primates. There are few comprehensive field studies of S.f.illigeri behaviour in the wild
which limits understanding and conservation of the Saguinus genus. Study groups were
investigated at the Pacaya-Samaria National Reserve, Peru. A behavioural ethogram was
created from observation of their behaviour. S.f.illigeri were found to vary their activities
and use of canopy strata throughout the day Foraging was identified as the most dominant
of all activities: approximately 50% of all time budgets was devoted to the searching,
processing and consumption of food items. Average group size was found to be 5.5 (made
up of 4.2 adults and 1.3 infants). The canopy cover under which groups were found did not
correlate with group size. Scan sampling was found to be the most appropriate method in
the field for recording S.f.illigeri behaviour. Larger groups were found to spend more time
travelling between food patches, perhaps in relation to intraspecific feeding competition
and patch depletion. Larger groups also vocalised more than smaller groups in order to
maintain group cohesion. Individuals from all groups were more spread out during
foraging and travelling activities. Nearest neighbour distance correlated with vocalisation
frequency in relation to predation risk. Individuals were found to reduce vocalisations
when they were more than 20m from another individual. This study has highlighted that
lower-middle canopy levels are particularly important for S.f.illigeri. This could be useful
in relation to the conservation of forest fragments and identifying habitat for protection.
Some of the behavioural findings from this study could prove useful for future captive
breeding projects.
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
By Grace Turner
CONTENTS
Acknowledgements: .........................................................................................................................2
Abstract: ...........................................................................................................................................2
Section 1: Introduction....................................................................................................................5
1.2 Aims and objectives: ................................................................................................................................... 10
Section 2: Methodology .................................................................................................................11
2.1 Study Subject ................................................................................................................................................. 11
2.2 Study groups .................................................................................................................................................. 12
2.3: The study site .............................................................................................................................................. 13
2.4: Research method ........................................................................................................................................ 14
2.5 Data analysis .................................................................................................................................................. 17
Section 3: Results .........................................................................................................................19
Hypothesis 1.1: Sampling methods to evaluate time budgets differ significantly in their
appropriateness.................................................................................................................................................... 19
Hypothesis 1.2: The canopy cover where groups were identified may correlate with group
size ............................................................................................................................................................................. 22
Hypothesis 2.1 Activity time budgets vary across the day ................................................................. 23
Hypothesis 2.2 “Activity time budgets relate to vertical canopy usage”...................................... 25
Hypothesis 3: Activity budgets vary according to group size, larger groups will spend more
time foraging and vocalising........................................................................................................................... 27
Hypothesis 4.1 Group spread will be larger during feeding/foraging and travelling
activities than during other behaviours ..................................................................................................... 32
Hypothesis 4.2: As group spread became further apart, vocalization frequency would
increase .................................................................................................................................................................... 34
Section 4: Discussion ....................................................................................................................36
Section 5. Relevance for conservation ..........................................................................................49
Literature Cited: ............................................................................................................................50
Image.1: Front cover photograph taken in Pacaya-Samaria field site by Heather Jenkins,
2010
Image.2: Map and satellite of Pacaya-Samiria National reserve
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
By Grace Turner
List of figures
Fig.1.1: Bar chart displaying total % of focal behavioural categories
Fig.1.2: Bar chart displaying total % of scan behavioural categories
Fig.1.3: Group B focal pie chart
Fig.1.4: Group B scan pie chart
Fig.2.1: Time budget of foraging, travelling and resting activities throughout the day
Fig.2.2: Resting and foraging + feeding activities throughout the day
Fig.2.3: Average canopy height for different activities
Fig.2.4: Activity time budget against Canopy level
Fig.3.1: Group size against activity budget
Fig.3.2: Group size Vs time spent foraging+ feeding
Fig.3.3: Group size Vs time spent travelling
Fig.3.4: Proportion of time spent vocalising against group size
Fig.3.5: Vocalisation activity during the day of different tamarin groups
Fig.3.6: Time of day Vs number of vocalisations
Fig.3.7: Proportion of time spent vocalising during foraging + feeding against group size
Fig.4.1: NND Vs activities with foraging + feeding data combined
Fig.4.2: Canopy height against NND
Fig.4.3: Average group spread when vocalising against group size
Fig. 4.4: NND Vs vocalisation events
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
By Grace Turner
SECTION 1: INTRODUCTION
Comprehensive field studies of S.f.illigeri social behaviour and ecology are rare. This
paucity of data from the wild limits understanding of the Saguinus genus, and its
conservation. Various aspects of their behavioural ecology are investigated in this study.
It is the suborder of Platyrrhini; the New World primates, and in particular the family of
Callitrichidae to which the Saddleback tamarin (Saguinus fusicollis) belongs (O'Neil,
2010). The Callitrichidae family consists of three genus; (Saguinus, Leontopitheus and
Callithrix), (Terborgh and Goldizen, 1987). Saguinus is the most diverse of all the New
World genera, containing 11 species and 33 recognised sub-species (Mittermeier, 1988).
S.fusicollis are black with a trizonal tan coloured-saddle pattern across the back, with a
white stripe across the muzzle in adults. The infants are uniformly black until one month
old (Mittermeier, 1988). This has been suggested as an evolutionary adaptation making the
vulnerable infants less conspicuous to predation. S.f.illigeri has nonopposable thumbs and
claw like nails, except for the first digit on each toe (Ford, 1980). Unlike marmosets
(Callithrix), tamarin canines are larger than the incisors so their dental morphology does
not allow them to gnaw bark for gum. However they can still exploit secondary gum from
pre-made holes.
S.fusicollis average weight lies between 350-400g; typical of the Saguinus genus. Their
taxonomic traits were originally considered primitive (Hershkovitz, 1977) but more recent
theories suggest they are as a result of phyletic dwarfism; the shift from frugivorous to
insectivorous diets leading to the evolution of their smaller body size (Ferrari, 1993). They
are virtually monomorphic, so sexes cannot be identified in the field (without capturing to
examine genital differences). Studies show S.fusicollis group compositions range from 210 individuals, with an average group size of 5.1 (Heymann, 2001). The two main
selection pressures which influence group size are predation risk and resource availability
(Blumstein, 2008). An inverse relationship exists between group size and vigilance known
as the “Group-size effect” (Roberts, 1996). Individuals in larger groups spend less time
maintaining individual vigilance as there are more individuals, and therefore collectively
have more chance of detecting predators. Group size may also impact time spent
vocalising. Hypothetically, larger groups vocalise more to maintain group cohesion
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
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(Heymann and Stojan-Docar, 2010). Vocalisations are linked to maintaining vigilance, in
the form of alarm-calling. The positions of individuals in the canopy and nearest neighbour
distance (NND) influence predation risk (Heymann and Stojan-Docar, 2010).
S.fusicollis are widespread in Bolivia, Brazil, Columbia, Ecuador and Peru. There are nine
different subspecies (congeners) which have evolved, either sympatrically (within the same
place) or allopatrically (across regions) (Knogge and Heymann, 2002). The sub-species,
S.f.illigeri are the subject of this study; found between rivers Huallaga and Ucayali, south
of the Rio Maranon and the lower Rio Tapiche (Rylands et al, 2008). (See image 2 for
map).
S.f.illigeri travel across different habitat types, with a preference for secondary forests and
are commonly found in seasonally flooded forests (Mittermeier, 1988). They are highly
adaptive to survive in small forest patches (Rylands, 1993). Stable groups usually occupy
circumscribed home-ranges, otherwise known as territories (Tardif, 1993). Buchman Smith
and Smith (2004) report a mean home range size of 40ha. Territories are defined vocally
and physically against encroachment and remain relatively stable over time. The ability to
defend, monitor and exploit productive fruiting trees against neighbouring groups is
considered an important aspect of S.fusicollis survival (Garber, 1993).
S.f.illigeri are diurnal; they are active in daylight hours and sleep at night (Strier, 2003).
S.f.illigeri tend to rest around midday to avoid over-heating (Blumstein, 2008).
Consequently, subjects were often not visible beyond 1300 hours so the data collection
time was limited to the morning only. There is close synchrony of activity between all
group members (Mittermeier, 1988). S.fusicollis have been shown to spend 20-21% of the
day travelling (Terborgh and Godizen, 1987) and up to 44% of the day resting. The
remaining time is mainly used for social behaviours and foraging. Time allocation could
potentially constrain group size, due to the need to maintain vigilance for predators and to
avoid intraspecific competition for food resources (Strier, 2003). The costs and benefits of
sociality can be explained in terms of time budgets. Time is a finite resource that animals
must manage to maximise reproductive success (Blumstein, 2008).
Predation is an important selection pressure on primate social behaviour. Recent studies
of behavioural ecology have focused on vigilance, e.g. by measuring the frequency of
vocalisations. This study investigates how S.f.illigeri divide up their daily time budgets
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
By Grace Turner
between different activities, such as foraging and feeding, resting, travelling and
vocalising.
S.f.illigeri are cooperatively breeding primates, with multi-male, multi-female group
compositions. Cooperative breeding refers to “any breeding system in which individuals
other than parents help to care for and provision offspring” (Schaik, 2009). This is
uniquely important among Callitrichids due to the high dependence on others in the group
for individual survival and reproductive success. However, debates arise over their mating
strategies; many believe S.fusicollis to be cooperatively polyandrous (Goldizen, 1996). To
support cooperative polyandry, two or more males must mate with a single female and all
males must help care for the female’s young (Terborgh and Godizen, 1987). On the other
hand, Terborgh, (1987) suggests monogamy also prevails. Extensive helping behaviour is
associated with increased social tolerance (Schaik, 2009) and is demonstrated by infant
carrying, food sharing both by relatives and non-relatives as well as general group-defence
and vigilance. It has been suggested that a single pair would be unable to breed
successfully alone due to the high costs associated with infant carrying (Terborgh and
Godizen, 1987). It has historically been recognised that helpers; i.e. non parental groupmembers provide substantial infant care (Goldizen,1986). There is evidence to suggest that
dominant breeding females are able to reproductively suppress ovulation in subordinates
(Abbot, 1993) which has significant implications for group size.
S.f.illigeri are primarily arboreal insectivores using stealth to catch larger insect species up
to two inches long (see appendix 6) to gain maximum energy return from their high protein
diet (Ferrari, 1993). They also feed on fruits, exudates, bird eggs and other plant material;
leaf petioles, flowers and leaves (Mittermeier, 1988). Each Saguinus differs slightly in
foraging methods, S.f.illigeri operates primarily by investigating knot-holes and crevices of
tree trunks and terminal branches (Terborgh and Godizen, 1987). They are more generalist
than many species within Saguinus, capable of utilising both primary and secondary
forests. The ability of S.f.illigeri to exploit a variety of habitats is described as “the
hallmark of Callitrichid ecology” (Caine, 1993). When foraging, individuals within the
same family group maintain contact by vocalising. Scent-marking is a form of olfactory
communication also used to maintain intragroup cohesion, typically in dense vegetation
when visibility is lost. It has been shown already that tamarins adhere to the Optimal
Foraging Theory (Cesar, Bica-Marques and Garber. 2003), by habitually searching in the
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
By Grace Turner
forest understorey, where they favour small tree crown patches (Cesar, Bica-Marques and
Garber.2003). Tamarin feeding habits are closely shaped by predation pressures, from
above, by the raptor family (Buteoninae) and from below by various terrestrial carnivores
e.g. ocelot (Felis pardalis). These threats may determine S.f.illigeri‘s use of forest strata.
Studies have shown that S.f.illigeri generally forage at ground level and restrict all other
activities. This suggests they are especially vulnerable on the forest floor, so a balance may
exist between positioning in the canopy and maintaining vigilance whilst foraging
optimally.
Tamarin species differ in foraging patterns and use of forest strata. The subspecies,
S.f.illigeri are known to use all vertical canopy levels, but in particular tend to utilize the
lower levels (Heymann, 2001) due to the abundance of favoured insect prey. Evidence
shows that resting occurs primarily in the upper canopy, as they are less prone to predation
under the dense vegetation cover (Heymann and Stojan-Docar, 2010) and are inaccessible
to ground predators. The proposed hypothesis tests these assumptions by investigating
which activities occur at each canopy level. The percentage cover of the canopy is another
variable which may alter positioning in relation to vigilance (Heymann and Stojan-Docar,
2010) which is examined in the current study. Patch size also relates to time budgets, as
one would expect larger groups to deplete patches quicker and so spend more time
travelling between patches, exerting considerable costs upon individuals (Heymann and
Stojan-Docar, 2010).
NND is the recorded measurement of furthest distance individuals are from one another, in
relation to group density. This is frequently investigated in studies on cooperatively
breeding species. Many studies have shown that as NND increases, vigilance is increased
(Roberts, 1996). Close NND is also beneficial for thermoregulation and infant protection.
S.f.illigeri group spread differs widely, depending whether feeding on clumped or
dispersed food. Because of this, groups frequently overlap one another. NND is also
related to social cohesion as when individuals are closer to one another they are more
likely to carry out social interactions such as allogrooming. As a group becomes more
dispersed, one would expect vocalization frequency to increase in relation to contact calls,
separation calls and maintenance of group cohesion (Roberts, 1996). In addition to this,
Hamilton observed that predation risk was lower for individuals with closer neighbours
(Buchman Smith and Smith, 2004). It has already been noted that many behavioural
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
By Grace Turner
ecology studies support the “Group size effect” whereby one would expect vocalisations to
increase as group spread becomes larger. However, this is controversial as similar studies
in primates have found the opposite. Callitrichids are able to sit upright whilst feeding, so
are able to simultaneously scan and maintain vigilance. When closer together, they can
actually be at a disadvantage by visually obstructing one another’s view of potential
predators (Treves, 2000). Research has found that long distance vocalizations are used to
locate and communicate with other groups (Caine, 1993). Egalitarian species such as
tamarins are expected to show a higher amount of social vigilance for mutual protection
(Heymann and Stojan-Docar, 2010). Group size may influence social cohesion or
intragroup spacing of individuals but results from studies have differed widely across
different primate species and groups. NND is therefore an important measure within
behavioural ecology.
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
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1.2 AIMS AND OBJECTIVES:
This study explores various contributory factors in the behavioural ecology of different
tamarin groups.
It begins by investigating whether 1.1 The canopy cover where groups were identified
has no correlation with group size.
1.2 Sampling methods to evaluate time budgets differ significantly in their
appropriateness. Comparisons are made between group scan sampling and focal scan
sampling for the frequency of different behaviours to identify which is the most
appropriate technique in the field.
The specific objectives of the current study are to investigate the behaviour of S.f.illigeri,
in relation to the following hypotheses:
2.1 Activity time budgets vary across the day. Tamarins may be less active at mid-day as
they are diurnal primates and temperatures are at their highest at this time.
2.2 Activity time budgets relate to vertical canopy usage. Type of behaviour may
correlate with canopy height.
3.1 Activity budgets vary according to group size, larger groups will spend more time
foraging and vocalising. Vocalisations correlate with foraging and maintenance of group
cohesion.
4.1 Group spread will be larger during foraging and travelling activities than during
other behaviours. These activities require individuals to be more spread out across the
strata. It is for this reason that one would hypothesise:
4.2 As group spread became further apart, vocalization frequency would increase. In
relation to contact calls, one would expect more frequent contact calls as individuals
disperse and lose visual contact.
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
By Grace Turner
SECTION 2: METHODOLOGY
2.1 STUDY SUBJECT
S.f.illigeri was selected as they are one of the most widespread primate species in northeastern Peru, but are isolated from congener species (Birch, 2010). Over most of their
range, S.fusicollis share forested habitat with sympatric tamarin species, such as S. mystax.
In this study, they are the only species of Saguinus within the national reserve; the only
other Callitrichid being the pygmy marmoset (Cebuella pygmaea). Cebuella pygmaea
avoids competition and niche overlap due to its specialisation of gum exploitation.
S.f.illigeri exploits all canopy levels and a wide area due to its generalist adaptation.
However, studies show they can specialise to the lower canopy to avoid interspecific
competition with other primate species (Nadjafzadeh, 2008). S.f.illigeri is not under great
threat from hunting for bushmeat for two reasons; the first being its very small body size
(as it is an inefficient source of meat) and secondly, that local people are involved in the
management of the Protected Area. Consequently, primate hunting has reduced
significantly in the Pacaya-Samiria during recent decades (Bodmer and Puertas, 2007).
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
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2.2 STUDY GROUPS
To statistically analyse the behavioural data, ten separate groups were identified by their
compositions of adults: infants in order to test group size as a parameter affecting
behaviour (Bart et al, 1998).
Average saddleback tamarin group size in the Pacaya-Samiria reserve
Study
Group
Group
Total
compositions
A= Adult
I= Infant
A
5A,2I
7
B
4A,1I
5
C
3A,1I
4
D
31,2I
5
E
7A,21
9
F
4A
4
G
5A,1I
6
H
2A
2
I
5A,2I
7
J
4A,2I
6
Mean
4.2A , 1.3I
5.5
Group A, (shown in Table 1) was only found once on the opposite side of the river from
the study site so was used as a pilot study group to identify the behaviour categories. All
groups were included with reference to group size. Mean group size= 5.5 (SD+/- 1.96,
N=10) was found. Group composition means for S.f.illigeri consisted of 4.2 adults (SD+/1.4) and 1.3 infants/ juveniles making up the group (SD+/-0.8).
Two limitations arise: firstly the determination of group composition was subjective.
Secondly some group compositions possibly changed throughout the period of study, e.g.
additional births or sub-adults leaving. Such groups are not included in the main body, and
are indicated by italics in the table above.
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2.3: THE STUDY SITE
The Pacaya-Samiria reserve is located near the equator between the two rivers, the
Maranon and Ucayali, 100 miles west of Iquitos city, (see image.2, map) in the Department
of Loreto, Peru. The coordinates of the study site were: S503.127, W74 31.585 at an
elevation of 339 ft above sea level.
The river basins which form the reserve have been protected by the Peruvian government
since 1940 and cover an area of 2,000km2 (The Pacaya-Samiria National Reserve, 2010).
Image.2: Map and satellite of Pacaya-Samiria National reserve
(Google Earth, 2010)
Average daily temperature at the site during the study was around 29 degrees Celsius
(Passingham, pers.com). This is typical tropical rainforest climate; steady sunlight for
around 12 hours daily with little variation throughout the day, interspersed by heavy
equatorial showers in the afternoon. It is a seasonally flooded forest habitat. Between the
months of June and July 2010 when this field study was conducted the water levels fell by
approximately 3m (Liebthal, pers com). Even the arboreal primates, such as S.f.illigeri are
impacted by seasonal flooding as they have been found to feed primarily at ground to
lower canopy levels (Garber, 1993), which are clearly inaccessible when flooded. This is
primary evidence for the flexibility and adaptability of S.f.illigeri.
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2.4: RESEARCH METHOD
A trail was cut through the rainforest and walked everyday for five weeks between 07001300 hours, approximately seven miles, looped around both secondary (more open) and
primary forest habitat in a figure of eight on the west side of the river. S.f.illigeri appeared
to be equally distributed across both forest types. A pilot study was carried out over the
18th and 19th June whereby different behaviour categories were identified and determined.
Two main sampling methods were carried out between 20th June and 10th July to identify
which of the two was more appropriate in the field for the study. These included twominute focal scans and five-minute interval group scan samples (Altmann, 1973). If
observational conditions at the field site are less than perfect (e.g. like those of a dense
rainforest canopy) Altmann, (1973) advised focal sampling should only be done on one
individual at a time for as long as the subject is visible.
Group scan data were used in the main analysis section of this investigation. Every five
minutes an instantaneous group scan sample from left to right of the group (Martin, 2007)
was carried out and behavioural code noted (see appendix for datasheet). Records were
made of the behaviour of interest including the date and time of each sample session
(Altmann, 1973). Instantaneous recording does not give true frequencies but a proportion
can be considered representative (Martin, 2007). This was done by entering a behavioural
code into pre-designed datasheets. Two- minute focal scans (Goldizen, 1986) were
recorded opportunistically between scans, when the subjects had appeared to become
habituated to being surveyed and continued normal behaviour.
A behavioural ethogram (Table 2) adapted from Birch, (2010) below was made for the
following ten behaviour categories which were identified:
Foraging (FO), Feeding (Fe), Travelling (T), Vocalising (VO), Resting (R), Groom-self
(GS), Allogrooming (GA), Other- including Food-sharing (FS), Aggression (AG) and
Infant Carrying (IC).
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
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Table 2.
Key
Description
Behaviour
observed
Foraging
FOi
The act of manipulative searching in knotholes, crevices and curled
up leaves either vertical or horizontal positioning, frequent arm
for insects
movement then pursuing the prey (Lauro-Perea, 2004).
Foraging
FOp
picking plant material from branches (Terborgh, 1983).
for plants
Feeding
Time dedicated for the searching for ripe fruit and selectively
Fe
Rapid jaw movements of chewing food item, head often positioned
downwards, food item held in hands.
Travelling
T
Jumping vertically or horizontal through the branches across
multiple trees, practice cling and leap locomotion through the
canopies.
Vocalising
VO
Loud chattering/ whistling made, mouth open
Resting
R
Stationary on branch, trunk or ground. Not maintaining vigilance,
eyes may be open or closed, tail often hanging down or tucked
around body.
Groom-self
GS
Animal scratching or investigative movements in fur around body to
maintain appearance and fur condition
Allogroomi
GA
Exchanging physical contact with another individual, cleaning and
maintaining each others’ appearance, searching, picking and
ng
combing for parasites using hands or teeth.
Other:
FS
adult to juvenile)
Foodsharing
The passing of food items from one individual to another (often
AG
Aggression
Teeth showing, loud chattering often contact between individuals,
e.g. grabbing fur or cuffing.
Infant
carrying
IC
Infants carried on back clinging onto fur on scruff of neck or around
abdomen of adult.
Use of binoculars proved challenging in the pilot study, so were rejected for use in the
field: they were difficult to maintain focus when the subjects were fast moving through the
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dense canopy. The best technique identified was to locate a group, then get close enough to
observe their behaviour with the naked eye, causing minimum disruption to their natural
behaviours. Canopy cover was simply estimated by looking directly above the tamarins,
without disrupting them, and estimating the vegetation to sky ratio, and then recorded as a
percentage.
The climatic conditions throughout the day were noted, whether “sunny”, “sun and cloud”,
“cloud” or “cloud and rain” as these may explain particular behaviours, such as sheltering
from rain or sun.
The canopy level where the subjects were located, (whether lower, middle or upper
sections) were recorded; these changed regularly due to the high degree of movement
associated with this species. Canopy levels were determined by the following categories
(Heymann, 2000): Lower = <20, Middle = 20-30m and Upper = 31+m. Nearest Neighbour
Distance (NND) was recorded as an estimate of the furthest distance the visible individuals
were apart during the first minute of every scan.
A total of 19 hours, 25 minutes of data were recorded on S.f.illigeri over the six weeks at
the field site. A total of 433 individual scan sample events were collected, averaging
around 40 minutes solid data entry per day.
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
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2.5 DATA ANALYSIS
Average group size, composition and percentage of canopy cover of individuals’ locations
were recorded. Bar charts and pie charts were used to compare time budgets for all
recorded behaviours using both sampling methods for each group. Data from Group B are
presented and discussed (see fig.1.3 and 1.4) as it had the largest and most representative
sample size, fairly typical group composition and was the most frequently observed of all
study groups. Average canopy levels were compared against group size and time budgets
for each group. Group H (N=2) were frequently excluded from this analysis due to small
sample size.1
Standard deviations and standard error measures were applied frequently on graphs to
examine group size against time spent dedicated to all different activities, and various other
parameters. This was in order to calculate if there was any significant relationship between
the different parameters (Bart et al, 1998). Sample sizes were typically N=6 for the main
tamarin study groups, though occasionally N=8. (Two of these groups were often excluded
in analysis due to small sample sizes.)
A chi-squared test was used to investigate time of day and activity, separated by the three
most dominant activities; identified as Foraging + Feeding, Travelling and Resting. The
frequencies of behaviour were differentiated by time categories, 0700-0800, etc until 12001300 hours. The same was done for the three activities against canopy height, e.g. 0-5m, 610m, up to 31m+. Chi-squared tests were performed to compare these different frequencies
with the expected values. An assumption was made that the behavioural categories are
mutually exclusive and are based on actual numbers of observations (Eagle, 2011). A Onesample T-test was carried out to compare the two means of NND and proportion of time
spent doing each activity.
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Vocalisations throughout the day were recorded and compared against group size and
NND. Two Pearson product-moment correlation coefficients (PMCC) and five Spearman’s
Rank correlation coefficients2 were used to measure the way the variables change together
in order to test the hypothesises. The two were used interchangeably- depending on
whether using parametric or non parametric data samples. In all seven scatter graphs,
linear regression analyses were applied in order to calculate the line of best fit for the given
dataset, expressed as y = a + bx (Fowler et al, 1998). Both regression and correlation
coefficient analyses were then tested again to ensure the results were statistically
significant, using the Statistical Package for Social Scientists (SPSS), taking into account
the test statistic and sample size (N) to give the exact degree of confidence under 0.05%.
The Kolmogorov-Smirnov method was used to test whether distributions were normal
(Fowler et al, 1998). SPSS program was used to calculate linear regressions, PMCC, Onesample T-tests and Kolmogorov-Smirnov tests. All inferential statistical tests were carried
out at P= 0.05 level of significance. Microsoft Excel was used for all other forms of
statistical analysis and graph presentation.
1
Group E scan data was ignored in comparisons as it was thought that the group changed
in composition throughout the duration of the study. Group A was also excluded as it was a
pilot group. Group H and J were included in the majority of analysis but were frequently
ignored due to small data set, not representative of their whole time-budget.
2
Non-parametric tests are more suitable for testing biological data as they are not based on
stringent assumptions (Fowler, 1998), therefore Spearman’s rank (non-parametric) was
chosen over Pearson’s (parametric test) for most correlations, although it depended on the
specific parameters being tested.
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SECTION 3: RESULTS
HYPOTHESIS 1.1: SAMPLING METHODS TO EVALUATE TIME BUDGETS DIFFER
SIGNIFICANTLY IN THEIR APPROPRIATENESS
Fig.1.1 Total proportion of time from all behavioural focal samples.
Proportion of time (%)
35
30
25
20
15
10
5
defecated
aggression
infant carry
sheltering
food-share
unidentified
allogroom
self groom
resting
vocalising
travelling
feeding
foraging
0
Behaviour categories
Fig.1.1 Shows a greater number of behavioural categories recorded than in fig.1.2- due to
the detail associated with focal scans. Foraging and travelling were the most frequent
behaviours, followed by feeding and vocalising.
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Fig.1.2. Total proportion of behaviour from all scans samples.
Proportion of time ( %)
30
25
20
15
10
5
defecated
aggression
infant carry
sheltering
food-share
unidentified
allogroom
self groom
resting
vocalising
travelling
feeding
foraging
0
Behaviour observed
Fig.1.2 shows more travelling was recorded than during focal scans, as they ended if the
individual moved out of sight. Group scans were used as a main basis of evaluation, as
they show a better representative sample of behaviours, minimising any overrepresentation. Otherwise there is little difference in two methodologies.
Fig.1.3 Shows the proportion of time Group B spent doing different activities throughout
the day recorded via two-minute focal scanning technique
Group B Focal
foraging
feeding
travelling
vocalising
resting
self groom
allogroom
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
By Grace Turner
Below fig.1.4 Shows the proportion of time Group B spent doing different activities
throughout the day recorded via five-minute group scan sample technique.
Group B Scan
foraging
feeding
travelling
vocalising
resting
self groom
aggression
defecated
The two pie charts above (fig.1.3 and fig.1.4) show very similar results (shown here for
group B).
This pattern is consistent throughout all tamarin groups, with highest proportion of time
spent foraging, resting, and vocalising. The tamarins spent almost 50% of the sample time
collectively foraging and feeding. Focal sampling was more detailed than the scan
sampling technique.
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HYPOTHESIS 1.2: THE CANOPY COVER WHERE GROUPS WERE IDENTIFIED MAY
CORRELATE WITH GROUP SIZE
Group
Total (N)
Average % canopy cover
found at:
A
7
B
5
75
C
4
63
D
5
63
E
9
F
4
64
G
6
67
H
2
I
7
J
6
Group size
= 5.5
Pilot study
Not included
Not included
67
Not included
Average % canopy
cover:
65.66
Table.1 above shows 65.66% (SE+/- 1.86) was the average canopy cover tamarin groups
were found under. PMCC between canopy cover and group size (R= 0.282, which is not
statistically significant at P=0.05, N= 10) so the Null hypothesis is retained. There was no
correlation found between group size and average canopy cover.
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HYPOTHESIS 2.1 ACTIVITY TIME BUDGETS VARY ACROSS THE DAY
Number of observations (N)
Fig.2.1 Time budget of Foraging, travelling and resting activities throughout the day:
35
30
25
20
15
F+FO
10
T
5
R
0
Time of day
Fig.2.1 shows S.f.illigeri are particularly active between the hours of 0700- 1000 hours.
Foraging and feeding were identified as the dominant activity between 0700- 1100 hours.
Between 1100-1300 hours, foraging, feeding and travelling were reduced, and resting
became the more frequent behaviour.
A chi-squared test was applied, the calculated value of 35.5 was significantly larger than
the critical value of 18.41, N= 6, DF= 10, P= 0.05), therefore the Null hypothesis was
rejected. Behaviours did differ significantly with time of day.
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Fig.2.2 shows the proportion of time S.f.illigeri spent resting against foraging and
Proportion of time (%)
feeding behaviours within each hour of a typical day during the study.
100.00
90.00
80.00
70.00
60.00
50.00
40.00
30.00
20.00
10.00
0.00
R
Fo+F
Time of day
Fig.2.2 It is clear from the bar chart that time spent foraging and feeding activities declined
after 1100 hours, and that a higher proportion of time spent resting was observed between
the hours of 1100-1300.
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HYPOTHESIS 2.2 “ACTIVITY TIME BUDGETS RELATE TO VERTICAL CANOPY USAGE”
Fig.2.3 Average canopy height usage for different activities:
Average Canopy level (m)
30
25
FO+F
20
VO
15
R
10
T
O
5
0
N= 4
N=5
N=6
Group Size
Fig.2.3 shows the average canopy height that each activity was carried out for each Group
B-G. The canopy levels utilized maintained fairly consistent, around 20m with average
vocalising height slightly higher than other activities. All the averages were below 25m,
supporting that notion that S.f.illigeri exploit the majority of the lower-middle canopies.
These can also be compared with group size. Interestingly, Group G (N=6) appeared to
carry out activities at a slightly lower canopy level. Travelling (SE+/-2.22) showed the
greatest error margins, suggesting there was greater variation in canopy height for this
behaviour.
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Fig.2.4 Vertical canopy usage vs activity. Shows activities were spread across canopy
levels, with the 16-20m category being the most common canopy level utilized.
Number of observations (N)
40
35
30
25
20
FO + F
15
T
10
R
5
0
0-10
11-15m
16-20m
21-25m
26-30m
35m+
Canopy height
Fig.2.4 above, generally shows fewer behavioural observations were observed at 0-10m or
above 35m, showing the range of canopy utilization. These results correspond to the table
below showing average canopy height of 17.8m (SD+/-1.37), suggesting there was little
deviation from the norm.
A chi- squared test was applied to test whether there was a significant difference between
canopy height and activities, the calculated value of 18. 385 was just significantly larger
than the critical value, 18.31 (N=6, DF= 10 P=0.05), therefore the Null hypothesis was
rejected. There is a significant relationship between frequencies of behaviour carried out at
each canopy level.
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
By Grace Turner
HYPOTHESIS 3: ACTIVITY BUDGETS VARY ACCORDING TO GROUP SIZE, LARGER GROUPS
WILL SPEND MORE TIME FORAGING AND VOCALISING
Proportion of time (%)
Fig.3.1 Activity time budgets compared against group size
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
other
resting
vocalising
travelling
feeding
foraging
4
5
6
7
Group size (N)
Fig.3.1 Shows a comparison between group size against proportion of time spent doing
particular activities throughout the study period.
All groups showed a fairly consistent pattern, although the largest group (N=7) were
observed to spend considerably less time feeding and foraging, yet more time travelling
and resting than average. Both group sizes 6 and 7 spent a larger proportion of time
vocalising. N=4 spent a large proportion of time focused on feeding and foraging activities.
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
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Fig.3.2 Group size vs proportion of time spent foraging +feeding: compares group size
Time spent feeding + foraging (%)
of all main tamarin groups with time spent devoted to foraging activities.
60
50
40
30
20
10
0
0
2
4
6
8
Group size (N)
Fig.3.2 Yielded a negative correlation; as the smaller groups were observed to spend more
time foraging and feeding than the larger groups. The average time spent FO+F = 43.4%
(S.E+/-5). Spearman’s rank correlation coefficent was applied (R2= -0.765, N= 6, P=
0.076). So, although there appears to be a negative relationship between the two variables,
it is not statistically significant.
Fig.3.3 Group size vs proportion of time spent travelling
Proportion of time (%)
20
18
16
14
12
10
8
6
4
2
0
0
1
2
3
4
5
6
7
8
Group size (N)
Fig.3.3 Investigates whether there was a relationship between FO+F and time spent
travelling.
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Spearman’s rank non-parametric correlation coefficent was applied, (R2= -0.736, N= 6 P=
0.096). The correlation was not statistically significant, although larger groups appeared to
spend more time travelling than smaller groups. N=4 spent the least amount of time
travelling. The average proportion of time travelling for all groups was 14.61% (SD+/2.61).
Fig.3.4 Group size vs % of time vocalising
% time spent Vocalising
40
35
30
25
20
15
10
5
0
0
2
4
6
8
Group Size (N)
Fig.3.4 Shows a strong positive correlation as the average proportion of time spent
vocalising increased with group size. This finding supports Hypothesis 3, in that larger
groups (N=6 and N=7) spent more time vocalising than the smaller groups. PMCC (R =
+0.886, N= 6, P=0.019).
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Proprtion of vocalisations (%)
Fig.3.5 Vocalisation activity during the day for different tamarin groups
25
20
15
10
5
0
7-8am
8-9am
9-10am
10-11am
11-noon
12-13pm
Time of day
Group B
Group C
Group D
Group F
Group G
Fig.3.5 Shows that generally the total proportion of time spent vocalising decreases during
the sampling period.
However, the groups show a considerable pattern of fluctuation of vocalisation throughout
the day. Vocalisations generally are carried out whilst feeding.
Average number of vocalisations
(N)
Fig.3.6 shows the average number of vocalisations against time of day.
25
20
15
10
5
0
7
8
9
10
11
12
Time (hour)
Fig.3.6 Shows in general, vocalising decreases throughout the day with peaks during
feeding time, (SE+/- bars). Spearman’s rank correlation was fitted to means of all groups,
found a negative correlation, decrease in vocalisations across the morning (R2= -0.711, N=
6, P=0.072). However this is not a statistically significant result, as it cannot be said with
95% confidence. Mean time spent vocalising for all groups= 15.16% (SD+/6.1).
Fig.3.7 Proportion of time spent vocalising during FO+F against group size.
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
Proportion of time spent VO whilst FO
(%)
By Grace Turner
25
20
15
10
5
0
0
1
2
3
4
5
6
7
8
Group Size (N)
Fig.3.7 Shows the proportion of time all different tamarin groups spent vocalising against
the time spent feeding and foraging.
A positive PMCC, (R=+0.613, N= 6, P=0.195) which is also not statistically significant,
possibly due to small data set. But larger groups do appear to vocalise more frequently
during feeding than smaller groups.
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HYPOTHESIS 4.1 GROUP SPREAD WILL BE LARGER DURING FEEDING/FORAGING AND
TRAVELLING ACTIVITIES THAN DURING OTHER BEHAVIOURS
Fig.4.1 Nearest Neighbour Distance vs Activities with FO+F data combined:
60
NND Vs activity
FO + F
50
Proportion of time (%)
V
40
R
T
30
Other
20
10
0
0-5
6-10m
-10
11-15m
16-20
21-25
26-30
31+
NND (m)
Fig.4.1 These data collated from all groups are showing a clear trend that 20m was the
median inter-individual distance. There was fairly consistent group spacing throughout the
range of activities, with group spread being furthest during foraging and vocalising. During
travelling individuals were often around 21-25m apart. Resting too was most frequent
when individuals were medial-distance from one another.
Individuals were rarely >30m and rarely <10m from one another. “Other” activities were
observed across NND with no distinguishable pattern. The 11-15m category of NND had
the greatest variation of behaviour (SD +/-7.45).
A One-sample T-test was applied, all NND categories were found to be greater than the
critical value 2.132 at (DF=4, N=6, P=0.05) so all statistically significant with behaviours,
(with the exception of the 0-5m category which was not found to fit the general
relationship with activity).
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Fig.4.2 Canopy height of S.f.illigeri found against mean Nearest Neighbour Distance
(NND):
25
Mean NND (m)
20
15
10
5
0
0
5
10
15
20
25
30
35
40
Canopy level (m)
Fig.4.2 There appears to be a weak relationship between group spread (nearest neighbour
distance) and canopy level.
Spearman’s rank correlation coefficient (R2= +0.714, N=8, P=0.047) confirmed a
statistically significant positive correlation. Generally, individuals were between 15-20m
apart, no matter what level of the canopy they were utilizing. 23m was the furthest distance
individuals were apart at 30m high in the canopy.
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HYPOTHESIS 4.2: AS GROUP SPREAD BECAME FURTHER APART, VOCALIZATION
FREQUENCY WOULD INCREASE
Fig.4.3 Average group spread when vocalising against group size.
NND (m) during vocalising
25
20
15
10
5
0
0
2
4
6
8
Group size (N)
Fig.4.3 Shows there is a strong negative relationship exists between group size and NND
during vocalising. Spearman’s rank correlation coefficent (R2= -0.949 N= 6, P= 0.01)
statistically significant between the average group spread when vocalising compared
against group size. N=6 and N=7 appeared to be closer during vocalisations. Group sizes
N=4 and N=5 appeared to spread out more during vocalising.
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
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Fig.4.4 NND- Group spread plotted against % of Vocalisations events:
Proportion of time (%)
25.00
20.00
15.00
10.00
5.00
0.00
0-5
30
6-10
11-15
16-20
21-25
26-
NND (m)
30+
Fig.4.4 shows the average group spread whilst vocalising. Generally S.f.illigeri vocalised
frequently when their nearest neighbour was up to 20m away, beyond this vocalisations
dramatically reduced.
The one-sample Kolmogorov-Smirnov test was applied to determine whether the
distribution was normal. (Z-value = +0.884, N=7, P=0.05) supporting that the data set is
normally distributed.
Vocalisations show a normal distribution about the mean NND =14.29m. Individuals were
typically 11-20m distance from one another when vocalising. 26-30m away appears to be
the maximal distance for vocalisation events. S.f.illigeri vocalised less than 5% of the time
when their closest neighbour was beyond 26m away.
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SECTION 5: DISCUSSION
1.1. The canopy cover where groups were identified has no correlation with group
size
A number of other studies support the average group size result of 5.5 (table 4).
Heymann’s (2001) 5.1 average is similar, suggestions for why it is 0.4 higher in the
Pacaya-Samiria site could be that there are no competing tamarin species affecting the
subject groups analysed, therefore possibly allowing for a slightly higher density than
elsewhere with sympatric species. Others suggest a range; “commonly live in family groups
of 3-9 individuals” (Zehed, Kurian and Snowdon, 2010). There seems to be supporting
evidence from this study and other research that groups under three individuals have a
lower survival rate and group living becomes strained beyond nine individuals. An optimal
group size of seven was hypothesised by Caine, (1993). Any group of more than seven
individuals has no additional gain and instead incurs costs associated with increased
feeding competition. In agreement with this, only one group in this study was found with
more than this; (Group E, N=9). However Group E were only seen on one occasion, and
were likely to be two neighbouring groups temporarily joined together. Group size has
been identified as a crucial variable linked to reproductive success of breeders within
tamarin groups (Schaffner, 1996). This is primarily related to the need for infant carriers
within the group and to maintain vigilance against predation.
The average percentage cover that S.f.illigeri were located under was 65.66% (table. 4).
This is supportive of their small body size and high predisposition towards predation.
S.f.illigeri are under threat from both raptors above the canopy and from ground carnivores
below (Caine, 1993). Therefore one would expect them to be found under mediumcoverage of vegetation. This finding may also indicate that S.f.illigeri avoid very dense
canopy cover, and require some degree of openness in order to locate one another,
although this could be subject to sampling bias as groups under canopy cover of +80%
became very difficult to visually survey. Heymann and Stojan-Docar (2010) found
vegetation cover can act as both obstructive and protective against predators.
Though both parameters are understood, there was no statistically significant correlation
found to exist between group size (N) and percentage canopy cover.
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
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1.2: Sampling methods to evaluate time budgets differ significantly in their
appropriateness.
In comparison of focal vs scan data, (see figs.1.3 and 1.4), individuals were recorded in the
focal scans to spend more time travelling. Arguably, this is a consequence of sampling
bias, because individuals targeted for focal scans may have been disturbed and so travelled
away from the observer. Animals in the group scans were also recorded to vocalise more.
This too may have been due to sampling bias. A constraint of the focal method is that the
individuals being followed may have been under stress, so may have increased
vocalisations and self-grooming. In focal scans, some groups were found to self groom
(scratch) more regularly than other groups; possibly indicative of a higher parasite load. In
captive settings, self-grooming can be considered a sign of stress (Barros, 2001); however
it is unclear whether self-grooming serves the same function in the wild.
Difficulty in focal sampling techniques due to high levels of activity and often dense
canopy cover caused many focal scans to end abruptly. For these reasons, the group scan
data were used to compare with the other parameters in this investigation. It was
considered more representative of S.f.illigeri behaviour. However, focal sampling is useful
to look at more finite categories (fig.1.3), e.g. infant carrying. Scan sample data were also
more easily calculated into a time budget analysis. Drawbacks of the appropriateness of
scan sampling include overlooking the more specific behaviour categories (fig.1.4), by
only recording behaviours occurring on the first minute within the five-minute intervals.
There were a few other limitations with the methodology. Due to their small body size (in
comparison to all the other primates at the Pacaya-Samiria reserve), S.f.illigeri often
proved difficult to spot when high in the canopy, even by the local guides. Their adaptive
camouflage colouration (tan on black markings) makes the subjects difficult to distinguish
amongst the dark branches. Their frequent vocalisations were often used to locate the
groups. This visibility issue also questions the reliability of NND estimations.
Overlapping behavioural categories potentially cause over-representation in the time
budget analysis. For example, distinguishing foraging from a feeding event is prone to
some subjectivity. Similarly, vocalisation events were carried out simultaneously with
other activities, for example, S.f.illigeri frequently vocalised whilst foraging as a type of
communication known as food-calling (Buchman Smith and Smith, 2004) so were not
mutually exclusive and perhaps should have been recorded as events rather than behaviour.
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Hence, multiple behaviours at each interval were recorded due to high activity levels of the
subjects.
S.f.illigeri were not habituated to humans, so increased territorial and defensive postures
were paramount with both sampling methods. Barros, (2001) observed “tsik-tsik”
vocalisations as a direct aggressive reaction. They were frequently heard at the beginning
of surveying, possibly biasing the data. Higher levels of habituation can only be achieved
by spending longer in the field.
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
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2.1. Activity time budgets vary across the day
Time budgets offer a valuable insight into how species such as S.f.illigeri organise their
lives. (Terborgh, 1983). Fig.1.2 shows S.f.illigeri spent around 28% of their average time
foraging, and another 16% feeding. Field studies support this by “S.f.illigeri spend between
30-77% of their total foraging plus feeding time dedicated to arthropods” (Garber, 1993).
Further analysis of qualitative observations on feeding behaviour found slightly more time
was spent feeding on insects rather than plants; supporting indications that S.f.illigeri are
mainly insectivorous (See appendix 6). However this was excluded from the results as the
data were not representative due to the difference in time required to process food items
(Mittermeier, 1988). It was also difficult to distinguish between food types, due to their
small size and distance from the subjects. A significant distance had to be maintained to
avoid frightening subjects.
Food sharing was observed by focal sampling (fig.1.3), an interesting behaviour as it is a
unique aspect of Callitrichid social structure (Dunbar, 1995). Infant provisioning is
believed to play a substantial role in the formation of social group functionality (Tardif,
1993). The frequencies of the behaviour in the qualitative field notes suggest it is important
for the survival of young offspring.
Time of day certainly has shown to influence behaviour, including the consumption of
different food resources. The results from fig.1.2 would support that there is close
synchrony of activity between all group members (Mittermeier, 1988). Primary foraging
techniques observed in the field included hunting insects by stealth, turning over leaves
and exploring crevices and knotholes as well as pouncing through palm fronds (Garber,
1993), the majority of which occurred in the understorey.
Foraging and feeding peaked around 1000-1100 hours (fig. 2.1) after then, resting became
the more dominant activity, this is also supported via the stack bars in fig. 2.2, showing an
inverse relationship exists between resting and foraging activities across the day. Fig.1.2
shows that S.f.illigeri spent an average of 10% of the survey period resting. However this is
subject to sampling bias; during prolonged periods of resting, the tamarins often went to
high canopy levels, so were lost from view. The accurate proportion is likely to be over
10%. Time budgets (fig.2.2) and the field notes agree S.f.illigeri normally rested between
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By Grace Turner
1200-1300 hours. This finding can be explained by climatic factors. Midday is the hottest
time of day, so resting time is enforced to minimize heat load at low latitudes. Seeking
shelter in the dense upper canopy is an effective solution (Korstjens et al, 2010). Animals
may spend time resting due to physiological or ecological needs (Blumstein, 2008).
Travelling also declined across the morning- almost certainly corresponding with foraging
behaviour as groups travelled between different food-patches. Overall from the time
budget data (fig.2.1), there was found to be a statistically significant relationship between
the observed and expected frequencies of dominant activities; foraging and feeding,
travelling and resting against time of day.
Vocalisations throughout the day showed a fairly consistent pattern (fig.3.5); most
prevalent when foraging in morning, then fluctuated across the mid-morning and
attenuating towards 1200-1300 hours when they were believed to rest.
All these patterns indicate a strict time budget organisation, S.f.illigeri use energy via
actively foraging and travelling in the early morning, then gradually reduce activity levels
across the morning until they rest and conserve energy in the afternoon when temperatures
are at their highest.
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The Behavioural Ecology of Saddleback Tamarins (Saguinus fusicollis illigeri)
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2.2. Activity time budgets relate to vertical canopy usage:
Average canopy level where S.f.illigeri were found was 17.8m (Fig.2.3) supporting
multiple studies stating S.fusicollis favour the middle to lower understorey for the majority
of their activities (Garber, 1993). Individual exposure to predation varies depending on
group canopy positioning, e.g. those individuals foraging on terminal branches will be
more vulnerable than those within the main canopy (Treves, 2000). One would expect the
groups feeding on lower canopy levels to have a relatively high vigilance within the group.
However, it is important to note that predators also exist in middle and higher strata e.g.
snakes and raptors respectively. One limitation to this analysis was the subjective
estimation of canopy height determined in the field (often at distance).
Decisions about time allocation for Callitrichids are at the core of Optimal Foraging
Theory (OFT). Fig.2.3 shows that average canopy height usage for different activities
varied little around the average of 17.8m, ranging only between 15m-26m. Similar studies
found that Golden-mantled tamarins (S.f.tripartitus) used all levels of the forest from
ground to 25m, but the majority of activities were concentrated in the lowest strata.
Approximately 60% of all activities occurred below 6m (Heymann, 2000). Observations
this low were not found with S.f.illigeri, suggesting that S.f.triparitius were responding to
vertical canopy stratification because of competition with sympatric species; S.f.nigrifrons
(Heymann, 2000). As there were no sympatric species at the Samaria site, S.f.illigeri were
able to exploit a widespread utilisation of the canopy (fig. 2.4) as were not constrained by
interspecific competition.
Observed frequency of activities at different canopy levels were found to vary significantly
from the expected (see appendix for fig.2.4 chi-squared analysis). For example, foraging
was preferred in the lower-middle sections of the canopy whereas resting was observed
more regularly at higher strata (fig.2.4). Resting behaviour is often described as time not
allocated for other useful behaviours. However, Korstjens et al (2010) found resting is
important for recuperation, predator avoidance, digestion and thermoregulation.
At night, S.f.illigeri groups sleep curled up high in the canopy, huddling together. This
behaviour has been hypothesised as an excellent means of heat conservation.
Simultaneously, they reduce conspicuousness to predators by hiding all features and
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looking rounded, an S.f.illigeri group can be mistaken for a termite mound (Smith et.al,
2007). Such roosting behaviours appear highly adaptive for survival (Caine, 1993).
Evidence that regular sleeping sites were used by S.f.illigeri (Smith et al, 2007) allowed
some study groups to be easily located by returning to the tree where they rested
previously.
Group size may have correlated with average canopy level utilised. Fig.2.3 shows that
group size, N=6 were observed to utilise a lower average canopy level than the smaller
groups. Potentially as there was a higher degree of vigilance in the larger groups,
individual risk of predation is effectively diluted (Barnard, 2003) so consequently, groups
were able to exploit lower strata for a longer duration of time.
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3. Activity budgets vary according to group size, larger groups will spend more time
foraging and vocalising
Fig. 3.1 displayed by stack bars that larger groups were in fact observed to spend less time
foraging and feeding than smaller groups. Group size and time spent foraging was directly
correlated in fig. 3.2, although appears to correlate was not significant at the 95%
confidence level. This general trend is not what the above hypothesis predicted, however
an explanation can also be found by fig. 3.1. A corresponding increase in time spent
travelling is shown with larger groups, so findings can be explained by the patch depletion
hypothesis.
Travelling was observed to be a coordinated group movement through the canopy (Leigh,
2001). Fig. 3.3 compares group size against time spent travelling and has a correlation of
+0.73, as hypothesised, because larger groups deplete food patches sooner and so travel
further between sites (Cesar, Bica-Marques and Garber, 2003). However, due to a small
sample size, this result was not found to be statistically significant at the 95% confidence
level. Both groups with four individuals spent the least amount of time travelling; fewer
individuals could focus on a particular food patch for longer, without having to expend
more time travelling between patches, further supporting hypothesis 3. The distribution of
resources affects group size at each patch. This is illustrated by the Ideal Free Distribution
model, which predicts that group size is dependent on whether foraging for dispersed prey
or clumped fruit patches (Buchman Smith and Smith, 2004).
Time spent vocalising across the day (fig.3.6) was assessed not only as an indicator of
vigilance, but also for maintaining group cohesion whilst foraging and travelling. As
predicted larger groups e.g. Group G (N=6) were found to vocalise more than smaller
groups, e.g. Group B (N= 4). This pattern was found to have a statistically significant
correlation of +0.88 (fig. 3.4).
Another parameter investigated was whether time spent vocalising during foraging
correlated with group size. This was tested in relation to food calling, with the prediction
that larger groups will spend more time vocalising to one another during foraging in order
to maintain group cohesion with a larger number of group-members. Fig. 3.7 shows that
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By Grace Turner
N=6 and N=7 groups did spend a larger proportion of time vocalising whilst foraging than
smaller groups, (+0.6) However, the correlation was not strong enough to be statistically
significant.
One explanation of why activity budgets for certain groups differed from the expected
could be due to presence of dependent infants. The whole group alters their foraging
patterns to compensate for the costs of infant carrying (Tardif et al, 1993). Tardif et al
(1993) also found that carriers across a range of Saguinus spent significantly less time
foraging and travelling and more time resting, evidence that infant carrying poses
constraints on time budgets. Groups with infants would also need to maintain a higher
degree of vigilance as young individuals are more prone to predation (Mittermeier, 1988).
Fundamental elements of tamarin social behaviour include cooperation, tolerance and
adaptability (Caine, 1993). Relationships between group members are generally pro-social
with little aggression (Mittermeier, 1988). This generalisation holds true in the current
study.
Overall a relationship exists between group size and activity budgets, in relation to OFT
and patch depletion hypothesises. These could have been examined in more detail if the
data-sets were large enough to have higher confidence of their relationship.
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4.1. Group spread will be larger during feeding/foraging and travelling activities than
during other behaviours
Fig.4.1 shows group spread was furthest apart during foraging and vocalising activitieswhich is not surprising as individuals vocalize to communicate with one another across
distance and when feeding (Garber, 1993). Fig.4.1 T-test found there to be a significant
relationship between the two means (see appendix 5). S.f.illigeri individuals tend to have a
greater spatial convergence than other species of Saguinus due to their “cling and leap”
preference of vertical locomotion (Buchman Smith, and Smith, 2004). This is supported by
fig.4.1; as average inter-individual spacing was 16-20m during the majority of activities.
During foraging, NND was comparatively large as subjects focused on slightly different
food patches perhaps to avoid intraspecific competition.
Fig. 4.2 showed a significant positive correlation between group-spread and canopy level.
This is likely to relate to predation avoidance, there are different degrees of safety as
individuals travel through the canopy. This is likely to correspond with distance between
individuals. Inter-individual spacing also adheres to the dilution effect which predicts that
individual vigilance depends on group size. Theoretically an individual in a larger group is
less likely to be attacked than one in a smaller group (Roberts, 1996). However, there are
important confounding effects which must considered; these include canopy cover (Table
4), age and sex of individuals and observer proximity (Roberts, 1996). NND has been
suggested as a better predictor of individual vigilance than group size (Heymann and
Stojan-Docar 2010). Predation risk was observed to be lower for individuals with close
NND (Buchman Smith and Smith, 2004). In contrast, similar primate studies found the
opposite as Callitrichids are able to sit upright whilst feeding, so can scan to maintain
individual vigilance, thus relying less on others in the group (Treves, 2000).
Heymann and Stojan-Docar (2010) predicted groups to be more spread out during foraging
activities. In this study (fig.4.1), S.f.illigeri were typically 20m apart during foraging. NND
was smaller during resting or “other” activities, thus supporting hypothesis 4.1.
Allogrooming maintains social bonds and group integration (Lauro-Perea, 2004). Higher
frequency of social behaviours between two individuals, e.g. allogrooming and huddling
(represented via closer NND) indicate particularly close bonds such as a breeding pair
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(Mittermeier, 1988) although since S.f.illigeri appear sexually monomorphic this could not
be investigated in the field.
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By Grace Turner
4.2. As group spread became further apart, vocalisation frequency would increase
Spatial ecology is an important aspect of Callitrichid behaviour, with respect to position of
an individual in the canopy and an individuals’ proximity to others. Position of an
individual in a group can have profound implications on its general behaviour; notably
vigilance levels (Buchman Smith and Smith, 2004). Group spread is likely to vary with
respect to activity level and time of day (fig.2.1), season, the sex and visual status of
individuals and canopy level (fig.4.2).
Typically one would expect as individuals became further apart, vocalization frequency
would increase as they remain in vocal communication. However, it was found in studies
of S.Oedipus there was a higher frequency of calls when individuals were in closer
proximity (Roush and Snowdon, 2000). The same holds true with S.f.illigeri in the present
study; individuals most frequently vocalised when mid-distance from one another but less
so when beyond 20m apart, displaying a normalised distribution (fig.4.4). These results are
based on the assumption the majority of vocalisations recorded were food and contact
calls.
Density problems exist in Callitrichids when group members are so close they obstruct
each other’s visual field. Consequently, vigilance may increase with greater spatial
cohesion (Treves, 2000). This argument could explain why fig.4.3 had a strong negative
correlation with NND during vocalising against group size and potentially why close
individuals (6-10m) still vocalised.
Fig.4.5 is interesting in terms of vocalisation frequency and predation risk avoidance. 1620m appears to be the maximal distance individuals vocalise from their nearest neighbour
(fig. 4.5), and beyond this vocalisation declines dramatically. This may be because
S.f.illigeri reduce their individual conspicuousness to predators, as due to their cooperative
nature, they are far more vulnerable when alone. It is clear NND plays an important part in
group density and positional effects in relation to vigilance.
Research from nearby study sites predict raptor attacks occur once a week per group on
average (Goldizen,1986). Vocalisations are linked to vigilance in the form of alarm calls as
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By Grace Turner
a form of predator detection. An individual will alert the whole group of a predator’s
whereabouts.
In relation to predation pressure, it is likely that tamarins contact call one another to reduce
time expended visually searching for conspecifics, so more time can be devoted to
vigilance; i.e. by upright scanning. Animals must detect predators before they inflict
damage. Early detection can be achieved by monitoring surroundings beyond the
immediate vicinity or awaiting signals given by others (Caine, 1993). Many researchers
have hypothesised that aggregation size predicts vigilance; the “safety in groups”
hypothesis (Barnard, 2003). However, the current study has insufficient data to be able to
conclude that certain study groups were less vulnerable in terms of closer NND and larger
group size (Treves, 2000).
Moreover, predation impact on vocalisation is difficult to study as the majority of
vocalisations are likely to serve as food and contact calls, determining their plasticity
would have been almost impossible without the correct acoustic equipment in the field.
S.f.illigeri maintained constant vocalisations during foraging (fig.2.1 and fig. 3.7)
presumably to communicate the location of a food patch or have areas which have been
depleted. Groups are able to optimise foraging success (Barnard, 2003), thus saving time
within their daily routine, perhaps facilitating more social behaviour, e.g. allogrooming.
Overall, Hypothesis 4.2 is only partially supported; vocalisations were found to increase
with NND to a maximal distance, then decline. This has been hypothesised an antipredation behaviour.
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5. RELEVANCE FOR CONSERVATION
This study has highlighted general behavioural patterns of S.f.illigeri. It could potentially
be useful to assist in their welfare in captive breeding (ex-situ) conservation projects.
Tamarins spend a large proportion of time foraging, therefore this behaviour should be
encouraged in captive animals. Providing enrichment for such species, e.g. by hiding food
and presenting at different levels are techniques for prolonging the time it takes for animals
to process their food materials, thereby providing effective stimulus (Morberg, 2001).
S.f.illigeri live in extended groups with an average size of 5.5 (table 4). Therefore it is
important that similar sized groups are kept in captivity to replicate natural conditions as
much as possible. Applying behavioural aspects from the wild is useful for successful
reproduction in captivity, as lack of sufficient knowledge in zoos can have severe
implications for species conservation and can even lead to declines in genetic diversity.
Future studies could focus on the important role of tamarins as biological agents of seed
dispersal. Recent studies found Saguinus species to disperse far more seeds than previously
thought (Knogge, 2002). S.f.illigeri may be a keystone species, with the ability to swallow
certain plant seeds whole during feeding (Garber, 1993), (see appendix). Not enough is
known about these complex biological interactions (Knogge, 2002) so more research is
needed. Anthropogenic climate change may alter time allocation needs and have
detrimental effects on population viability and range (Blumstein, 2008). A longer term
study with habituated subjects would allow these factors to be investigated.
This study has highlighted that lower-middle canopy levels (around 17m) are particularly
important for S.f.illigeri in the Pacaya-Samiria reserve. Targeting these forest fragments for
protection should be prioritised. Fragmentation caused by deforestation elsewhere in the
Amazon is causing populations of S. fusicollis to become isolated. Once isolated these
groups can suffer inbreeding depression and undergo genetic drift by evolving separately
due to different selection pressures. Future conservation projects could favour S.f.illigeri
by maintaining areas of primary and secondary forest (Rylands, 1996) and joining habitat
fragments together via corridors. Identification and application of behavioural ecology
knowledge studies on sub-species such as S.f.illigeri contributes to further understanding
of the Saguinus genus which may prove useful for their conservation.
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