envr451 - final project report d. kim, e. riondato · 1 introduction!!...
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The influence of canopy cover and connectivity on the habitat
selection of Saguinus geoffroyi in the Parque Natural Metropolitano
Da Jeong Kim and Emily Riondato
Host Information: Parque Natural Metropolitano de Panama Address: Avenida Juan Pablo II, Panamá Host Organization Contact: Yarabi Vega
Phone: 232-‐5552/16 Fax: 232/5613
Email: [email protected]
April 2016 Total hours spent working on the project: 175 hours
Hours in the field: 77 hours
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Executive Summary
The influence of canopy cover and connectivity on the habitat selection of Saguinus geoffroyi in the Parque Natural Metropolitano
Da-‐Jeong Kim & Emily Riondato Host organization: Parque Natural Metropolitano, Avenida Juan Pablo II, Panamá
An important element in the study of behavioural ecology is the understanding of how an organism uses the space in its surroundings. The spatial configuration of a forest is determined by the arrangement of its vegetation, with tree canopy cover and connectivity being important aspects of forest structure. Our study was interested in exploring the possible ways in which forest structure influences the selection of habitat by primates. Specifically, we wanted to see if the selection of habitat by Geoffrey’s tamarin (Sanguinus geoffroyi) is affected by the level of primary canopy cover and connectivity. One of the primary threats faced by the tamarins currently is the loss of their habitat, so we hope that this research will provide a greater understanding of a habitat preferences of S. geoffroyi and that could possible contribute towards conservation efforts aimed at preserving their population.
Our study was conducted in the Parque Natural Metropolitano during March and April of 2016. We began each observation by walking along each park trail for 5 minutes and then turning off of the trail and walking into the forest for 30m. We then recorded our position with a GPS, recorded the percentage of canopy cover (the proportion of sky covered by leaves and branches overhead), the level of connectivity (the level of overlapping tree canopies), and any tamarin sightings. If we spotted any tamarins, we followed them for as long as possible at took GPS points and data recordings periodically. Afterwards, we would return to the trail and begin our observations again. We then analyzed the data to determine if the level of canopy cover or connectivity correlated with the presence of tamarins in an area. For the purposes of the research, we considered the presence and sighting of S. geoffroyi in an area to be the indicator of a preferred habitat. We collected 98 points of observation during the study. 45 of these points were zero points, where no tamarins were observed, and the rest were observational points from 12 individual tamarin sightings. When we analyzed the relationship between canopy cover and the frequency of tamarin sightings, we found that the level of canopy cover in an area was a reliable predictor of whether there would be a tamarin sighting. A higher degree of canopy cover may provide several benefits. To begin with, tamarins are frequently preyed on by birds of prey, so a higher degree of canopy cover would allow them to hide from aerial predators. Secondly, fruits and vegetation make up a significant portion of the tamarins’ diet and these would most likely be found in areas with fruit-‐bearing trees that have a high level of canopy cover. Finally, canopy cover provides shade and can prevent heat stress. We also analyzed the relationship between the level of canopy connectivity and the frequency of tamarin sightings and found that the level of canopy connectivity was not a significant predictor of whether there would be a tamarin sighting in that area. This may be because in areas with wide gaps between trees, we observed that the tamarins would descend to a lower forest canopy and travel across it until they reached a primary canopy tree and could return to the primary canopy. Also, we observed that the tamarins could jump across narrower canopy gaps, so they could be found in areas
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that did not have complete connectivity. However, we found that all of our tamarin sightings were in areas that had either medium, medium-‐high, or high levels of connectivity, so there may be a possibility that they require at least a medium level of connectivity in their habitat. In summary, this study explored the element of animal space use through observations and analysis of S. geoffroyi. By focusing on canopy cover and connectivity in the primary canopy, we were able to understand that the forest canopy structure indeed plays a role in the tamarin’s habitat selection within their home range. Our findings showed with a moderate significance that S. geoffroyi takes canopy cover as one of the factors in determining their habitat. This conclusion is crucial in understanding and managing tamarin populations and ensuring the maintenance of their appropriate habitat. Resumen Ejecutivo
La influencia de la cobertura y conectividad del dosel arbóreo sobre la selección de hábitat de Saguinus geoffroyi en el Parque Natural Metropolitano
Da Jeong Kim & Emily Riondato Organización: Parque Natural Metropolitano, Avenida Juan Pablo II, Panamá
Un elemento importante en el estudio ecológico del comportamiento es la comprensión de la manera en que un organismo utiliza el espacio en su entorno. La configuración espacial de un bosque se determina por la forma de su vegetación: la cubierta de las copas de los árboles y la conectividad que son aspectos importantes de la estructura del bosque. Nuestro estudio estaba interesado en explorar las posibles formas en que la estructura del bosque influye en la selección del hábitat de los primates. Específicamente, queríamos ver si la selección de hábitat del mono tití (Sanguinus geoffroyi) se vio afectada por el nivel de cobertura forestal y conectividad del primer dosel arbóreo del bosque. Una de las principales amenazas que enfrentan los monos tití es la pérdida de su hábitat, y el objetivo de esta investigación era lograr una mayor comprensión de las preferencias del hábitat de S. geoffroyi y posiblemente contribuir a los esfuerzos de conservación de la población de los monos.
Nuestro estudio se llevó a cabo en el Parque Natural Metropolitano durante marzo y abril de 2016. Comenzábamos cada observación caminando a lo largo de cada sendero del parque durante 5 minutos y luego nos salimos del sendero y caminábamos por en el bosque en línea recta por 30m. Luego anotábamos nuestra posición con un GPS, registrábamos el porcentaje de cobertura de copa (la proporción de cielo cubierto por las hojas y las ramas que estaban por encima de nosotras), el nivel de conectividad (el nivel de la superposición de copas de los árboles) , y cualquier avistamiento de los monos titi. Si podríamos ver los monos, los seguíamos durante el mayor tiempo posible mientras tomábamos puntos de GPS y grabaciones de datos. Después, volvíamos al sendero y empezábamos de nuevo una observación. A continuación analizamos los datos para determinar si el grado de cobertura forestal o conectividad se correlaciona con la presencia de los monos en cada área. En nuestra investigación, se consideró que la presencia y el avistamiento de S. geoffroyi en una zona indicaba que era un hábitat preferido.
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Recogimos 98 puntos de observación durante el estudio. 45 de estos puntos eran cero puntos donde no se observaron los monos, y el resto eran puntos de observación de 12 avistamientos individuales de los monos titi. Cuando se analizó la relación entre la cubierta forestal y la frecuencia de avistamientos de los monos, se encontró que el grado de cobertura forestal en un área era un predictor fiable de si habría un avistamiento de los monos. Un mayor grado de cobertura de copa puede dar varios beneficios. Primero, los depredadores mayores de los monos son las aves rapaz, por eso un mayor grado de cobertura del dosel les permitirían esconderse de los depredadores aéreos. Segundo, las frutas y vegetación forman una parte importante de la dieta de los monos tití y éstos muy probablemente que se encontrarían en áreas con árboles frutales que tienen un alto grado de cobertura forestal . Por último, la cobertura del dosel da sombra y puede prevenir el sobrecalentamiento.
También analizamos la relación entre el nivel de conectividad del dosel y la frecuencia de avistamientos del mono tití y encontramos que el nivel de conectividad dosel no fue un predictor significativo de si habría un avistamiento tití en cada área. Esto puede ser porque en las zonas con amplias brechas entre los árboles se observó que los monos bajaban a un nivel de bosque más bajo y cruzaban a través de este nivel hasta que llegaban a un árbol que tenía un dosel primario y podían regresar a el dosel primario. También, se observó que los monos tití podían saltar a través de espacios pequeños en el dosel, entonces ellos también se podrían encontrar en las zonas que no tenían conectividad completa . Sin embargo, encontramos que todos nuestros avistamientos de los monos se encontraban en áreas que tenían un nivel de conectividad medio, medio-‐alto o alto, y por eso puede haber una posibilidad de que los monos tití requieren por lo menos un nivel medio de conectividad arbóreo en su hábitat.
En resumen, este estudio exploró el uso del espacio por parte de los animales a través de observaciones y análisis de S. geoffroyi. Al enfocarnos en la cobertura del dosel y la conectividad en el dosel primaria, pudimos concluir que la estructura de la cubierta forestal de hecho juega un papel en la selección del hábitat del tití dentro de su territorio. Nuestros resultados mostraron que S. geoffroyi toma cubierta de copas como uno de los factores en la determinación de su hábitat . Esta conclusión es crucial en la comprensión y manejo de poblaciones de los monos tití y podría ayudar a asegurar el mantenimiento de su hábitat apropiado.
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Table of Contents EXECUTIVE SUMMARY II
RESUMEN EJECUTIVO III
INTRODUCTION 1
LITERATURE REVIEW 4
METHODS 9
EXPERIMENTAL DESIGN 9 DATA COLLECTION 10 DATA ANALYSIS 12
RESULTS 13
DISCUSSION 17
CANOPY COVER 17 CANOPY CONNECTIVITY 19 COVER AND CONNECTIVITY 20 LIMITATIONS & CONSIDERATIONS 22
CONCLUSION 24
REFERENCES 25
1
Introduction
An important element in the study of behavioural ecology is the understanding of
an organism’s manner of space use. The behaviour of habitat selection enables species
to coexist while individually seeking an optimal environment (Rozensweig, 1981).
Territorial behaviour or site fidelity, distribution of resources and location of other
animals are general contributing factors to the variations of habitat (Horne et al., 2008).
These factors, along with other spatial and temporal factors, non-‐exclusively play into
animals’ tendency to confine themselves to a home range (Horne et al., 2008). The
densities of primate populations fluctuate across different landscapes, but even within
the boundaries of their home ranges, space has also been observed to be used unevenly
by various species (Dietz et al., 1997; Warner, 2002). The spatial distribution of tropical
forest primates has been shown to be affected by the spatial configuration of vegetation,
as forest structure differs significantly between known habitat areas and non-‐habitat
areas (Palminteri et al., 2012). The three-‐dimensional structure of forests likely affects
the ability of arboreal vertebrates to travel through their habitat (Emmons & Gentry,
1983) and avoid aerial predators (Raboy et al., 2004; Youlatos, 2004), as well as their
ability to locate food (Hill et al., 2004).
Tropical forests support an immense diversity of primates, with each species
giving preference to different levels of vegetation (Cannon & Leighton, 1994). The niche
separations among arboreal primates have often been categorized according to the
vertical stratification during travel and feeding (MacKinnon & MacKinnon, 1980). This
stratification has often been attributed to differences in the locomotor behaviour of
species (Cannon & Leighton, 1994). For instance, the efficient travel of forest primates
through the rainforest canopy is constrained by their capacity to use available structure
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as well as to cross any tree canopy gaps (Temerin, 1983; Cant, 1992). The ability to
traverse gaps depends on the size of the gap itself along with the presence of the
appropriate structures at either end of the gap needed by the animal to facilitate
crossing (Cannon & Leighton, 1994). The presence of a higher degree of canopy
connectivity, with more canopies interconnected by lateral branches and lianas, would
therefore be expected to facilitate travel through a forest canopy (Madden et al., 2010).
The relative number and diversity of available travel paths through a forest would also
depend on the morphological and behavioural qualities of each species (Cannon &
Leighton, 1994). Different species of primates are therefore adapted to specific forest
habitats through their ability to travel efficiently through that particular forest structure
(Cannon & Leighton, 1994).
In this study, we study the habitat selection Geoffroy’s tamarin (Saguinus
geoffroyi), known as the mono titi in Panama. A member of the Callitrichidae family, the
tamarins are diurnal and live in extended family groups that number between 3-‐9
individuals (Dawson, 1977). S. geoffroyi are arboreal primates that inhabit areas of
secondary moist seasonal dry forest (Garber, 1993; Moynihan, 1970). Their home
ranges vary from 9.4 ha (Garber, 1980) to 32 ha, depending on the abundance and
distribution of resources (Dawson, 1979). Group densities in Panama have been found
to range between 0.34 groups/km^2 to 5.35 groups/km^2 (Skinner, 1985). They can
communicate through vocalizations which include ‘bird-‐like’ whistles, trills, and rasps,
though they vocalize less when unaware of being observed by humans or other
potential predators (Moynihan, 1970).
S. geoffroyi’s habitat extends from central Panama to the Pacific coast of
Colombia (Moynihan, 1970). Their relatively restricted range combined with the
extensive deforestation that has taken place in the region over the past few decades
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(Rasmussen et al., 2002) may pose a threat to the tamarins’ native habitat. Though they
remain relatively common within their range, there may be declines in several areas
due to ongoing habitat loss (Rasmussen et al., 2002). In Panama, S. geoffroyi is
frequently captured to be sold into the pet trade (Rasmussen et al., 2002), and there
have also been reports of trapping and trade of the tamarins in Colombia (Vargas,
1994).
S. geoffroyi can be found within the city limits of Panama City, in the Parque
Natural Metropolitano (PNM). The park is a 232 hectare stretch of protected tropical
forest that comprises part of the biological corridor of protected areas along the east
shore of the Panama Canal (‘Park Profile’). The PNM is a rich source of biodiversity in
Panama and is home to approximately 300 animal species (‘Park Profile’). The park has
a colourful history, having been used as pastureland and as a military base by the
American and Panamanian armies before being inaugurated as an official park in 1988
(‘Park History’). Deliberate reforestation began in 1913 and has resulted in a landscape
that has been partially designed by the park management (Sr. Sixto, personal
communication, February 4, 2016). The park contains moist forest, which is classified as
having a mixture of deciduous and evergreen broadleaf trees (Condit et al., 2010).
Due to the presence of both deciduous and evergreen trees within the park, there
are a variety of forest types that S. geoffroyi could choose to inhabit. The aim of our
research is to examine this dynamic, focusing on the relationship between the various
forest structures such as within the park and the preferred habitat of S. geoffroyi.
Canopy cover and canopy connectivity of the primary forest canopy are the covariates
for forest structure characteristics that this study will focus on. We aim to analyze the
locations in which the tamarins are found and search for similarities between the forest
structure in these points as well as any underlying commonalities between points in
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which the tamarins are not found. We therefore hope to gain a greater understanding on
the link between the structure of the primary canopy and the preferred habitat of S.
geoffroyi by analyzing the forest structures within the areas of frequent tamarin
sightings.
This research has the potential to provide additional insights into the specific
forest structures that characterize the ideal habitat of S. geoffroyi. Given that one of the
primary threats faced by the tamarins is the diminishment of their range, any
contributions towards the habitat preferences of S. geoffroyi may be valuable towards
conservation efforts aimed at preserving their population.
Literature Review
Wallace et. al (1998) studied the population density and preferred habitat of
several primate species within a national park in Bolivia. They measured the population
densities of each species within a variety of landscapes to determine their habitat
preferences and found that the brown capuchin monkey (Cebus apella) and the black-‐
tailed marmoset (Callithrix argentata melanura) showed considerably higher
population densities in low vine forests (Wallace et al., 1998). The black spider monkey
(Ateles paniscus) showed a significant preference for tall forest and other structurally
similar habitats (Wallace et al., 1998), confirming the results found during previous
studies in Colombia and Peru (Klein & Klein, 1976; Terborgh, 1983). Wallace et al
(1998) also found that there existed clear differences in the use of forest strata between
the various primate species at the study sites. The majority of owl monkey (Aotus
azarae) and C. melanura and sightings were in the middle levels of the forest stratum,
and C. apella was observed to be more of a generalist, splitting its time evenly between
the upper strata and the middle levels of the forest (Wallace et al., 1998). Through this
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research, Wallace et al. (1998) demonstrated that primates consistently hold preference
for specific types of habitat, this being significantly influenced by forest type and
structure.
Carol Skinner (1985) conducted a three-‐month field study of S. geoffroyi in
Panama to determine its presence and relative abundance across several study sites.
Although the tamarins could be found in a range of locations throughout the country,
she discovered that the presence of large trees, specifically species which become
“emergent” in large forests, was a common element of each habitat in which the
tamarins were sighted (Skinner, 1985). The tamarins are thought to rely on large trees
for food, cover from predators and sleeping sites, and they also provide travel routes
across open areas (Skinner, 1985). Skinner (1985) concluded the study by proposing
that the numbers and spacing of select canopy tree species significantly affect S.
geoffroyi density in an area.
The role that forest structure plays in protecting callitrichids from aerial
predators has been explored in several studies. Previous research has indicated that
members of the Callitrichidae are preyed on by a number of animals but are particularly
vulnerable to birds of prey (Ferrari & Ferrari, 1990; Izawa, 1978). Ferrari and Ferrari
(1990) examined the alarm calls of a callitrichid, Callithrix flaviceps, and found that the
variations in the frequencies of alarm calls indicated a higher level of vigilance by C.
flaviceps while they were in the higher levels of the forest and when canopy leaf cover
was low. The relationship between predator avoidance and the use of forest structure
was further explored by Vidal and Cintra (2006). In this study, they measured the
population densities of groups of bare-‐faced tamarins (Saguinus bicolor) in order to
examine the influence that forest structure exerted on the patterns of primate
movement and habitat use. Canopy cover was included as a factor that could affect S.
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bicolor density and they hypothesized that areas with more canopy openings would
allow increased chances of detection and predation on the tamarins by birds. The same
study found that the occurrence of S. bicolor groups had a significant inverse correlation
with forest canopy opening. Vidal and Cintra (2006) concluded their study by stating
that although there is some recognized behavioural flexibility in the Callitrichinae
family, the distribution and abundance of S. bicolor responds significantly to variances
in the forest structure and to some degree as a result of predator avoidance strategies.
Previous research has also suggested that callitrichids prefer to use secondary
forests, open areas in mature forests, borders of primary forest, and areas with dense
shrubbery (Goldizen, 1987; Terborgh, 1983). These preferences can generally be
explained by the tamarins’ diets, primarily insectivorous-‐frugivorous, and the high
abundance of insects in areas of secondary vegetation along with the increased
presence of fruiting pioneer trees (Mittermeier & van Roosmalen, 1981; Terborgh,
1983; Yoneda, 1984). An extensive study on the relationship between forest structure
and the feeding behaviour of S. geoffroyi discovered a preference for foraging for insect
prey on thin, flexible supports in the forest understory, and clinging to large, vertical
trunks while feeding on plant exudate (Garber, 1980).
A number of studies have explored the relationship between the morphology of
S. geoffroyi and the ways in which moves throughout its habitat. Many primatologists
have identified the similarity of locomotor behaviours between callitrichids and tree
squirrels of the genus Sciurus (Napier & Napier, 1967; Hladik, 1970; Jolly, 1972;
Cartmill, 1974). Callitrichids posses “claw-‐like” nails on their manual and pedal digits,
unlike the flattened nails that many other primate species possess (Hladik, 1970). The
evolution of these claws has resulted in callitrichids developing a classical quadrupedal
gait and allowed them to run on branches and climb along tree trunks by digging their
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claws into the bark (Hladik, 1970). The development of these claws is thought to be
related to the habitual use of large, vertical supports during travel (Hladik, 1970).
Garber (1980) also found that the claws of callitrichids possess elements that increase
the leverage and support capabilities of each digit, allowing them to cling onto large
vertical supports, especially while feeding. He also noted the tendency of S. geoffroyi to
travel through the canopy not by ascending and descending trunks, but by travelling
across tree canopies via a series of leaps. The morphology of each primate therefore
influences the ways in which they travel through the forest, and they may select habitats
based on whether the forest structure is conducive to their particular locomotor
behaviours (Garber, 1980).
Madden et al. (2010) examined the influence of tree canopy connectivity and the
availability of food resources on habitat selection by S. geoffroyi in Panama. Tamarins
often forage in fragmented forests that have canopies that are interconnected by
branches, lianas, and other forms of vegetation that hang over trees and spread out into
forest gaps (Garber 1993). Garber (1988) described tamarin movement through the
forest as ‘trap-‐lining’, where several trees of the same species are used during the same
day as they forage for food. Habitat selection that determines the path of a trap-‐line
might be a response to a high availability of food or alternatively, the physical
characteristics of the route and the frequent contact between tree canopies (canopy-‐
connectivity) (Madden et al., 2010). Madden et al. (2010) determined that S. geoffroyi’s
habitat preference is influenced primarily by the amount of canopy connectivity within
an area rather than by the abundance of fruits. S. geoffroyi is able to employ a mixed
feeding strategy and exploit fruits, insects, and plant exudates throughout the year, and
this may explain why they base habitat selection primarily on canopy structure rather
than food resource distribution (Madden et al., 2010). By inhabiting and foraging within
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forests that have a high degree of canopy-‐connectivity, S. geoffroyi would have access to
a greater number of routes for travel, foraging, and predator avoidance (Madden et al.,
2010).
The Parque Natural Metropolitano encompasses a moist tropical forest that
contains deciduous and evergreen broadleaf species of trees in the forest canopy
(Condit et al., 2010). Panama experiences an annual dry season that spans 4 to 7 months
and typically begins in mid-‐April (Weider & Wright, 1995). During this time, many
species of deciduous trees, vines, and herbs shed their leaves in order to conserve
(Janzen, 1988; Weider & Wright, 1995). In the moist forests near the Panama Canal
zone, approximately 12% of tree species drop their leaves during the dry season in
order to conserve water (Croat, 1978 ). During the wet season the the forest appears to
be uniformly green, but when the dry season arrives and certain species of trees shed
their leaves, the forest becomes a mosaic of diverse habitat types characterized by
different proportions of leafy canopy cover (Janzen, 1988). Within moist forests,
seasonality therefore has a direct influence on canopy cover. Bianchini et al., (2011)
confirmed that deciduous forests experience a higher degree of canopy openness
throughout the dry season that only decreases once the wet season begins.
For the purposes of this research, we are assuming that areas that have high
tamarin density are representative of their preferred habitat type. The research cited
above that discusses population density and forest structure therefore provides us with
a sense of the ideal habitat of each primate. Having considered the available information
on the links between habitat-‐type and the population density of S. geoffroyi and other
primates, we hypothesize that there is direct relationship between forest structure and
the preferred habitat of S. geoffroyi within the Parque Natural Metropolitano.
Specifically, we expect to find more sightings of the tamarins in locations of the park
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that have a greater degree of canopy cover and connectivity that would facilitate travel
and avoidance of predators. S. geoffroyi is able to travel across canopies by leaps, but we
believe that the small size of the tamarin would prevent it from leaping for very long
distances and they would therefore require some degree of canopy connectivity in their
habitat. Our research takes place during Panama’s dry season, so we anticipate having
fewer sightings of S. geoffroyi in areas of mostly deciduous trees as the bare branches
would offer the tamarins minimal food resources or protection from predators. The
tamarins have been also found to favour the highest forest stories, so we also expect to
to see them in the primary and emergent forest canopies. We expect to have the highest
numbers of S. geoffroyi sightings in areas that have a forest structures that are
representative of their preferred habitat. Specifically, we hypothesize that the preferred
habitat of S. geoffroyi is forested areas with a significant presence of a primary canopy
and a high degree of canopy cover and connectivity within the primary canopy.
Methods
Experimental Design
The study site was the main and south region of Parque Natural Metropolitano,
studied through March and April of 2016. It is important to note that the studied region
was highly impacted by the dry season. The research conducted was observational and
we made an effort to minimize the influence of our presence on the tamarins’ behaviour.
No treatments were implemented onto the tamarins. Observations were collected
during the full opening hours of the park. We hypothesized that the preferred habitat of
S. geoffroyi would be in the primary canopy of the forest, so the investigation centered
on the relationship between forest structure of strictly the primary forest canopy and
the habitat preference of S. geoffroyi. The primary canopy structure was the central
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explanatory variable of our study. We focused on two specific variables that described
the primary canopy structure: (1) the level of canopy cover and (2) the level of canopy
connectivity. The habitat preference of S. geoffroyi was the response variable. For the
purposes of the research, we considered the presence and sighting of S. geoffroyi in an
area to be the indicator of a preferred habitat. Data collection and sampling was
repeated on all trails and we ended replication once all trails had been observed in the
morning and afternoon.
Data Collection
We began each of our observations by walking along the main trails of the park
for intervals of five minutes, keeping our speed as constant as possible. After five
minutes of walking along the path, we turned either left or right and walked into the
forest for a distance of 30 m perpendicular to the trail. The direction in which we
walked was chosen randomly by flipping a coin. If it was not possible to walk off of the
trail for any reason we continued along the path until we were able to turn off of it. It
was important to cover as much of the parks’ area as possible in order to obtain data
from a variety of habitat types and keep an even distribution of observations across the
park. Some of the park’s most isolated areas are significantly far from the main trails, so
walking for 30 m from the trails allowed us to cover a wider area of the forest and
increased our chances of observing tamarins, especially if they avoided areas with high
human foot traffic.
Once at 30 m from the trail, we stopped and recorded the spatial coordinates of
our location with a Global Positioning System (GPS). We then observed our
surroundings for five minutes while noting the forest structure in the area with a radius
of approximately 10 m surrounding us. We also noted the presence or absence of any
tamarin groups. We then estimated and recorded the percent canopy cover and the
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level of canopy connectivity in our surroundings. Canopy cover was approximated and
expressed as a percentage by estimating the proportion of sky that was covered by the
primary tree canopy when looking upwards from the understory. The canopy
connectivity was also estimated by using a numbered ranking system (Table 2).
Rank Canopy connectivity Characteristics
1 Low Minimal overlapping branches between the primary canopy trees. Canopy gaps are wide.
2 Low-‐Medium Some overlapping branches between the primary canopy trees. Some wide canopy gaps.
3 Medium Half of the primary tree canopies overlap. There is an even split between small and large gaps.
4 Medium-‐High Most primary tree canopies overlap. Some small gaps.
5 High Almost all primary tree canopies overlap. Minimal canopy gaps.
Table 2. Ranking system used to quantify the level of canopy connectivity.
The data was recorded using voice notes, which was later transcribed to allow
for further analysis. If any tamarins were spotted, we began a focal follow of the group.
The focal follow allowed us to collect as much data as possible on the distribution of S.
geoffroyi given the limited time available to collect field observations. We followed the
group as they moved through the forest, noting the time of each sighting taking GPS
readings at each tree they passed through and taking voice notes describing the
surrounding forest structure. Any feeding behaviours were also recorded as well as
details of how the tamarins moved from tree to tree and the species of trees used by the
tamarins. The focal follows continued until we either lost sight of the tamarins or were
unable to continue any further due to the terrain. After each period of observation we
returned to the trail and continued walking for another five minutes before repeating
the observational process. If at any point we saw or heard the tamarins while walking,
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we tried to get as close as possible and began another focal follow while recording all
necessary observations. We only recorded visual observations of the tamarins because
their calls are very similar to that of birds. If we thought we heard the tamarins but
were unable to see them, we did not record this as an observation because we also
wanted to collect information on group sizes. We also ensured that the entirety of each
trail was walked along at least twice, once in the morning (8:00 AM to 12:00 PM) and
once in the afternoon (12:00 PM to 5:00 PM) in order to prevent any bias in the data
from any possible behavioural changes of the tamarins throughout the day. We ensured
that the length of the morning period of observation was the same as the length of the
afternoon period of observation to reduce the risk of any influence on our data
collection.
Data recorded on the voice notes were later transcribed into a spreadsheet that
included all of the necessary details from our field observations. When we sighted a
tamarin group, we took points (these included a GPS point and a corresponding voice
note) during the entirety of the focal follow. The values for canopy connectivity and
canopy cover of each separate focal follow were averaged and they represented each
follow, or ‘series’. For instance, the value for the canopy cover of Series 6 was the
average of the canopy cover measured at each point during the focal follow of the sixth
tamarin group sighted. The combination of data into series made it more feasible to
compare individual sightings as the focal follows were very uneven lengths and had
different numbers of points associated with them.
Data Analysis
The collected data was analyzed through statistical procedures as well as
qualitative analysis, depending on the nature of the variables. We analyzed the
relationship between the level of canopy cover and the number of S. geoffroyi sightings
13
through a boxplot representation of the range of canopy cover of areas where tamarins
were sighted (observation points) and areas where no tamarins were sighted (zero
points). We used the Binomial Logistic Regression to test whether if the level of canopy
cover or connectivity were statistically significant predictors of a S. geoffroyi sighting in
the area. Canopy cover levels had been recorded as a percentage, so we transformed the
percentage values using an arcsine transformation before performing the test. The
Binomial Logistic Regression was chosen for this analysis because it is used when the
dependent variable is dichotomous (i.e. presence/absence of S. geoffroyi) and the
independent variables (canopy cover/canopy connectivity) are continuous or ordinal
but non-‐parametric (Harrell, 2001).
Finally, we examined the relationship between the level of canopy connectivity
and the level of canopy cover to determine if one was a reliable predictor of the other.
We graphed the level of canopy cover (recorded as a number from 1 to 5) versus the
level of canopy connectivity with a scatterplot graph and then ran a linear regression
analysis to determine any significant correlation between the two variables.
Results
We collected 98 points of observation during the study. 45 of these points were
zero points, where no tamarins were observed, and the rest were observational points.
We collected 12 series of observational points from 12 individual sightings of S.
geoffroyi. The shortest series were Series 1 and Series 9, each associated to a single data
point taken during the focal follow. The longest series was Series 6 with 15
observational points. We did not experience a significant difference in the number of
sightings according to the time of day. Five of the series were recorded during the
14
afternoon, and seven of the series were recorded during the morning. 25 of the zero
points were recorded during the morning, and 20 were recorded in the afternoon.
In the points where no tamarins were spotted (Fig. 1), the values for the percent canopy
cover ranged from 0% to 90% with a median of 50% and a mean of 48%. In the series
where tamarins were spotted, the percent canopy cover ranged between 25% and 85%
with a median of 80% and a mean of 69%. The inter-‐quartile range of canopy cover for
zero points is between 26% and 68%, whereas the inter-‐quartile range of canopy cover
for observational points is between 60% and 80%. The box plot for S. geoffroyi spotted
is skewed left, with only the spread between first-‐quartile and the median visible, as the
median of 80% is equal to the third-‐quartile.
Figure 1 The range of percentages of canopy cover in points where S. geoffroyi was spotted and points where they were not spotted. Each individual series of sightings is represented by one averaged value of canopy cover.
15
Figure 2. The percentage of canopy cover was transformed using arcsine transformation in order to run through a Binomial Logistic Regression. The value for S. geoffroyi spotted is binary, with 0 meaning no tamarins spotted and 1 meaning at least one tamarin spotted.
The Binomial Logistic Regression test demonstrated that the level of canopy
cover was a statistically significant predictor of whether or not there would be a
tamarin sighting (Fig. 2). Canopy cover showed significance to the 95% confidence level
(P<0.05; P=0.015425). There was a positive correlation between canopy cover and
tamarin sightings. The estimated slope of the relationship was 3.275 with a standard
error of 1.517.
The tamarins were spotted only in areas with medium, medium-‐high, or high
connectivity. However, the majority (63%) of the zero points were recorded in areas
that had either medium-‐high or high connectivity and 23% of the zero points were
taken in areas that had low or medium-‐low connectivity. Due to some inconsistencies in
data collection, there were 35 zero points that had an associated level of canopy
connectivity recorded out of a total of 45 zero points that were taken. Therefore, the 10
16
observation points missing connectivity data were omitted for the graphing of Fig. 3.
The Binomial Logistic Regression test demonstrated that there was no
significant relationship between the level of canopy connectivity and the number of
tamarin sightings (p>0.05). The level of canopy connectivity in an area therefore was
not an accurate predictor of whether there would be a tamarin sighting.
Fig. 4 demonstrates the relationship between the level of canopy cover and the
level of canopy connectivity at the zero points and observational series that were
sampled. The linear regression test had an r-‐value of 0.5886, which demonstrated a
moderate correlation between canopy cover and connectivity.
Figure 3. The levels of canopy connectivity recorded in areas where tamarins were spotted and in areas where they were not spotted. The ‘number of points’ along the Y-‐axis represents the number of zero points and the number of series.
17
Figure 4. The correlation between the level of canopy cover and the level of canopy
connectivity.
Discussion
Canopy Cover
The data demonstrated that the level of canopy cover in an area was a reliable
indicator of whether or not S. geoffroyi could be found in that location. The tamarins
likely prefer habitats with a higher degree of leafy cover due to the protection that a
thick canopy of leaves can offer from aerial predators. During our field observations, we
noted that we rarely saw birds of prey flying within the forest under the top tree
canopy layer. The majority of our sightings of birds of prey were of the birds flying
overhead above the tallest trees. If a tamarin were to remain underneath trees that
offered a higher level of canopy cover, they would presumably have a lower risk of
being spotted by a potential predator.
18
Both Fig. 1 and Fig 2. show that higher presence of tamarins is related to higher
canopy cover. A second explanation to add on to the first previously mentioned is the
change in abundance of food from low to high canopy cover. The diet of S. geoffroyi has
been estimated to consist of approximately 30-‐38% fruits and 10% other vegetation
(Garber, 1980; Hladik, 1975). Any trees that are leafless due to the dry season or
otherwise have lower levels of vegetation are less likely to be producing fruits or other
vegetation that fit to the diet of the tamarins. As habitat selection is ultimately
associated to food and escape cover (Horne et al., 2008), the preferred habitat of S.
geoffroyi is likely to be one that contains enough food resources to support their
population. Due to the association between fruit and vegetation growth and leaf cover
on trees, tamarins may prefer habitats with high canopy cover because there is a
greater abundance of food resources in the area.
During the dry season, there is very little shade provided by clouds. In Panama
City, temperatures can reach a high of 38 degrees Celsius during the months of April to
August (‘ Datos Climáticos Históricos’). Primates have been shown to experience heat
stress at 40 degrees Celsius (Gathiram et al., 1988; Hiley, 1976), and temperatures
above approximately 44 degrees Celsius have been recorded as being fatal to a number
of species (Bouchama et al., 2007; Gathiriam et al., 1988). There have also been several
cases of Saguinus oedipus, a close relative of S. geoffroyi dying in captivity due to heat
stress (Leong et al., 2004). During periods of elevated temperatures, S. geoffroyi may
seek out habitats with more canopy cover in order to stay cool in the shade.
Due to the correlation between canopy cover and the frequency of S. geoffroyi
sightings, we expected to see more tamarins in areas that had the highest level of
primary canopy cover as represented by the leftward skew of the plot for S. geoffroyi
spotted in Figure 1. However, we did not observe any tamarins in areas that had greater
19
than 85% canopy cover. Furthermore, the highest level of canopy cover in areas of no
sightings was recorded as 90%. This discrepancy can be explained by observer error
while in the field. It was more difficult to spot the tamarins in areas that had an
extremely dense primary canopy with a thick level of canopy cover. Therefore, though
the tamarins may have preferred high canopies with thick leaf cover, our results may
have missed a number of sightings in these habitats due to the difficulty in spotting
them.
Canopy Connectivity
The results from the Binomial Logistic Regression test did not show that there
was a statistically significant relationship between the level of primary canopy
connectivity and the frequency of sightings of tamarin groups. We had hypothesized
that the preferred habitat of S. geoffroyi (and the majority of sightings) would be in
areas with a high degree of connectivity in the primary canopy that would assist their
travel through the forest. However, during our observations we noted several instances
where the tamarins were in areas of lower primary canopy connectivity and when faced
with a wide gap between trees of the primary canopy they would travel down to a
lower story that had more connectivity. Once they travelled through the secondary and
reached a tree that was well connected to the primary canopy, the tamarins would
climb back into the tall, primary canopy trees. The secondary story thus played a more
significant role than we had anticipated in facilitating their travel throughout the forest.
The presence of wide gaps in the primary story was therefore not a significant
deterrent to the tamarins as long as there was a sufficiently well connected secondary
story in the area as well.
Throughout our field observations, we also noted the tendency of the tamarins
to leap across small canopy gaps. Therefore, tamarins would be able to inhabit areas
20
that are not perfectly connected as long as the distances between the trees are small
enough for them to jump across. The data collected as well as our anecdotal field
observations suggest that the tamarins do not necessarily need a very high degree of
primary canopy connectivity in their habitat. However, we did not have any sightings of
the tamarins in areas that had low or medium-‐low levels of canopy connectivity as
shown in Fig 3., suggesting that they do require at least a medium level of connectivity
in their habitat. It is important to note, however, that the number of data points taken
with and without tamarin sightings both follow a similar positive trend. A possible
conclusion could be that the sightings of tamarins in higher connectivity areas may
simply be due to the larger proportion of areas of high connectivity sampled.
Cover and Connectivity
The results of the study demonstrated a moderate relationship between the
level of canopy cover and connectivity in each location. Areas that have a high degree of
connectivity have a greater proportion of overlapping branches and leaves, which
would presumably result in a higher level of canopy cover. We also expected the
relationship to work both ways, because trees with a lot of leaves and branches would
have greater canopy cover and a higher probability of overlapping with the nearest
canopy to it. However, the correlation that we discovered was moderate, suggesting
that there are several factors that interfere with the relationship between canopy cover
and connectivity.
The dry season in Panama has resulted in the deciduous trees of the park
shedding all or most of their leaves. On several occasions during the field observations
we recorded data from sites with many deciduous trees with interconnected canopies
but low levels of canopy cover due to the branches being bare (Fig 5). Areas with high
densities of deciduous trees would explain the points on the upper leftmost corner of
21
the graph in Fig. 4 where there is a low percentage of canopy cover but a high level of
connectivity. It is much rarer however for there to be areas that have very high levels of
canopy cover but low levels of connectivity. Fig. 4 shows a lower number of plotted
points in the lower rightmost corner of the graph, which represents the points where
there would have been high canopy cover but lower connectivity. Therefore, canopy
connectivity is not a reliable predictor of canopy cover but canopy cover is a more
reliable indicator of canopy connectivity. This statement can further be extrapolated to
suggest canopy cover as the moderating variable between canopy connectivity and
tamarin sightings.
Figure 5. An area in the park showing a higher degree of connectivity but low canopy
cover.
22
Limitations & Considerations
Our field observations took place during the months of March and April 2016,
during the dry season in Panama. The mixture of deciduous and evergreen trees within
the study site resulted in several areas that had mostly bare trees with minimal canopy
cover in our results. During the rainy season, the forest structure of these areas would
change and would likely affect the distribution of S. geoffroyi. Furthermore, the
relationship between canopy cover and canopy connectivity would presumably change
as the deciduous trees of the park grew leaves and increased the level of canopy cover.
The findings of this research are therefore limited to providing insights on the preferred
habitat of S. geoffroyi and the relationship between primary canopy cover and
connectivity during the dry season in Panama.
Many of our limitations in the field stemmed from difficulty in locating S.
geoffroyi. The tamarin is a very small species of primate, with an adult body weight of
approximately 500 grams and body length of only 23 cm (Defler, 2004). They were
therefore quite difficult to observe when they were remained still within the canopy.
Also, if they were in the highest level of the forest canopy or if the tree that they were in
had large leaves or very thick leaf cover it was more difficult to spot the tamarins or
even maintain them within our line of sight. During our field research, we realized
that listening for the cries of S. geoffroyi was very helpful in helping us locate them. In
many cases, we heard them cry out and were able to find them when we searched very
carefully throughout the area. Our sense of hearing was therefore an invaluable tool in
conducting our research. However, the calls of S. geoffroyi sound very similar to the calls
of many birds within the park. Many times we searched for the tamarins in an area
before realizing we had been hearing birds. It is also possible that we heard S. geoffroyi
but assumed it was a bird. In areas with high densities of birds or at times of the day
23
when birds were most active, we may have missed the calls of S. geoffroyi. Furthermore,
many of the trails in the park are located within earshot of busy roads and even
construction sites. The noise of any nearby vehicles or power tools could have drowned
out the cries of S. geoffroyi and led us to miss several sightings. Our results may have
underestimated the population density of S. geoffroyi in any locations that were close to
a road.
While conducting our research, we were informed by several members of the
park staff that a number of the tamarins had just given birth to their young, and
vocalized less often than usual so as to attract less attention from potential predators. It
is therefore very likely that we missed tamarin groups that had infants with them due to
our not being able to hear them.
Our research method involved performing focal follows on any groups of S.
geoffroyi that we were able to locate. In some cases however, our focal follows were cut
short. In several occasions we found them in areas that had very thick undergrowth. The
park had many areas of thick bamboo, shrubs, and thorny vines that were difficult to
walk through at a rapid enough pace to keep up with the tamarins. If the undergrowth
was very thick we were sometimes left behind by the tamarins or lost sight of them
when trying to search for alternative paths through the forest. The presence of stinging
ants and wasps hindered our progress through the undergrowth as well. In some cases
we were also limited by the opening hours of the park. During several of our afternoon
sightings we were forced to conclude our observations early to ensure that we were out
of the park by the time it closed at 5 pm. Therefore, the lengths of our focal follows are
varied significantly and we were unable to collect even amounts of data on each group
of tamarins that we sighted.
24
Conclusion
In summary, this study explored the element of animal space use through
observations and analysis of S. geoffroyi. By focusing on canopy cover and connectivity
in the primary canopy, we were able to understand that the forest canopy structure
indeed plays a role in the tamarins’ habitat selection within their home range. Our
findings showed with a moderate significance that S. geoffroyi take canopy cover as one
of the factors in determining their habitat. This conclusion is crucial in understanding
and managing tamarin population. As the intensity and length of the dry season has
been increasing in Panama over recent years (Sr. Sixto, personal communication,
February 4, 2016), more trees may remain leafless for a longer period of time, resulting
in a lower overall level of canopy cover in forests. An increase in number of evergreen
tree species during the dry season may be of interest to parks and organizations
concerned with mitigating the potential decrease in S. geoffroyi population. Our
research also demonstrated the possibility of a correlation between the presence of
tamarins in an area and the level of canopy connectivity. Further research extended to
include the subcanopy may be beneficial in finding this correlation. Overall, although
canopy cover is but a single factor out of many in determining habitat selection of the
tamarins, this study helps conceptualize the causal relationship between an
environmental factor and a species’ habitat selection and can be modeled to explore
other factors that may influence the space use by different species.
25
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