Distribution of monkeys (Alouatta palliata) in Bella Vista and Limones, Chiriquí,

Emma Sutherland and Tara Jagadeesh

Host information: Universidad Autónoma de Chiriquí Address: Host contact: Dr. Ariel Rodríguez-Vargas Phone: (507) 730 - 5300 Email: [email protected]

April 2017 Hours spent in the field: 104 hours Hours spent working in Panama: 50 hours Hours spent traveling: 120 hours Total: 270 hours

Table of Contents

1

I. Introduction 3 Background 3 Area of study 4

II. Methods 5 Data collection 7 Data analysis 9

III. Results and discussion 6 Biological data 10 1. Distributions and density 10 2. Demography 12 3. Behavior 13 Social data 14 1. Perceived threats 14 2. General observations 15 3. Future conservation ventures 16

IV. Conclusion 20

V. Works Cited 23

VI. Figures and tables 26

VII. Appendices 33

Introduction

2 Background

The Mantled Howler (Alouatta palliata) is part of the and is one of six of monkeys found in Panama. Its distribution ranges from eastern to the Pacific coasts of and (Mann 2005). Howler monkeys are an arboreal, diurnal species. Of all of the species, A. palliata consistently lives in the largest groups, with ≥10 individuals (Chapman and Balcomb 1998).

They are frugivores, usually eating young but preferring mature fruits when they are available (Estrada 1984). They are found in a wide range of habitats but prefer evergreen and semi-evergreen forest due to consistent food production throughout the year (Chapman &

Balcomb 1997). Although they prefer these forests, the most important indicator for selection of habitat by howlers is density of tree cover (Stoner 1996). This is important in the context of , which increasingly poses a threat to species worldwide. However, howlers have been shown to adapt to changing environments (Clarke et al. 2001), and can alter their diet depending on food availability in the area (Christóbal-Azkarate & Arroyo-Rodríguez 2007). This flexibility allows howler monkeys to more readily persist in regions affected by anthropogenic disturbance in comparison to other, more sensitive species.

Despite their flexibility in habitat selection, these monkeys face a variety of threats.

Deforestation is occurring in Panama at a rate of 0.71% (27,050 hectares) per year, causing habitat loss and fragmentation of the remaining habitat (“Panama Forest Information and Data”).

Fragmentation exacerbates the effects of habitat loss not only by reducing habitat area but also by increasing landscape patchiness, decreasing patch size, and increasing patch isolation (Fahrig

2003). Compared to continuous forest, these forest patches have a greater degree of edge effects which expose organisms within a patch to the novel conditions of the surrounding environment

3 (Murcia 1995). This can have negative effects on the forest community by introducing invasive species and increasing exposure to pollution and predators (Robinson et al. 1995). In these fragmented landscapes, decreases in habitat area, connectivity between fragments, and canopy heights have led to declines in howler monkey abundances (Anzures-Dadda & Manson 2006).

Fragmentation also alters habitat quality; forests that are fragmented lack large trees and thus have less area of top food resources in comparison to continuous forests (Arroyo-Rodríguez and

Mandujano 2006). Decreased patch sizes are associated with lower population size of howler monkeys, likely due to lower food availability (Arroyo-Rodríguez & Dias 2010). In a population viability analysis of A. palliata in Los Tuxtlas, Mexico, Mandujano and Escobedo-Morales

(2008) concluded that in fragments smaller than 15 ha there is a 60% chance of extinction.

Highly fragmented landscapes with little connectivity and smaller patches still therefore pose a threat to howler monkeys. Other documented threats to howler monkeys include hunting by humans (Peres 1997), hunting by domestic dogs (Raguet-Schofield 2008; De Oliveira et al.

2008), and capture for the pet trade (Duarte-Quiroga & Estrada 2003).

Area of Study

The Burica peninsula is located in Chiriquí, Panama and is shared by both Panama and

Costa Rica. Within this peninsula, we focused our study on two areas: the towns of Bella Vista and Limones. The majority of our field time was spent in Bella Vista, beginning at the town center and extending to the tip of the peninsula. The rest of our study was conducted around the town of Limones (Figure 1, Figure 2). The local economies of both Bella Vista and Limones rely heavily on agriculture and to a smaller extent, tourism. As a consequence, much of the land has been deforested in favor of pasture and cropland. There are a few features that distinguish the

4 two towns and thus allow for an interesting comparison. Bella Vista is foremost dominated by cow pasture, with some small-scale personal crops. Along the coast, however, there are 3 ecotourism projects. These projects have contributed to the protection and reforestation of the vegetation along the coast. Limones, on the other , has much less cow pasture but instead has a palm oil plantation that was established in the last 5-6 years. Interestingly, much of

Limones is still surrounded by fragments of forest larger than those of Bella Vista. The human population of the entire corregimiento of Limones was 948 in the year 2000 and 1,040 in 2010, indicating a population growth of 9% (“Población de la Republica”).

The landscapes of Bella Vista and Limones reflect larger global trends in land use changes. In developing countries, livestock production is the fastest growing agricultural subsector, accounting for 33% of agricultural GDP (Steinfeld et al. 2006). This increase is in response to both global and local demands for meat and dairy products, which have increased with urbanization, population growth, and income (Delgado 2005). The greater demand for livestock consequently drives the conversion of forests into pasture, which is further exacerbated by the increased need for cropland for feed. The expansion of pasture/cropland and a correlating decrease in forest cover of countries in the Neotropics that encompass ranges was noted by Kowalewski et al. (2015) (Figure 3A). Along with cattle production, there have also been trends of increasing soybean and oil palm production in these countries (Figure 3B).

With growing demands for alternative energy sources, biofuels are a popular option. Oil palm is an attractive biofuel feedstock given its low cost of production and its high yields (Carter et al.

2007). It is also increasingly used for vegetable oils in replacement of oils with high animal and trans fat contents. Oil palm plantations are often cultivated as commercial monocultures which use herbicides and pesticides, thereby contributing to further biodiversity loss.

5 With these changes in land use present in the Burica peninsula, it is necessary to assess the abundances of Howler monkeys and their ability to survive in areas with a low percentage of forest cover and high fragmentation. Punta Burica is currently home to three species of monkeys:

Mantled Howler (Alouatta palliata), Central American Squirrel Monkey (Saimiri oerstedii), and

White-headed Capuchin (Cebus capucinus). A fourth species, Geoffrey’s (Ateles geoffroyi), once inhabited the area but disappeared sometime in the last 50 years. Our subject species, A. palliata, is listed as Least Concern by the IUCN Red List of

(Cuarón et al. 2008). Although they are considered one of the more abundant primate species in

Panama, with increased human activity and deforestation on the peninsula it is necessary to assess their conservation status in the area. The conservation status of the Mantled Howler monkey was last assessed in 2008, and there has never been a comprehensive population study of the species on the Burica peninsula. In order to analyze the impacts of land use changes on A. palliata, a point of reference needs to first be established. Despite their status as Least Concern, we therefore believe it is important to study A. palliata.

Our research contributes to a greater assessment of the conservation status of both the

Mantled Howler monkey and the Central American Squirrel Monkey on the entire Burica peninsula, to be conducted by our supervisor, Dr. Ariel Rodríguez-Vargas, a researcher at the

Universidad Autonoma de Chiriquí (UNACHI) specializing in primate ecology and conservation. Through our study, we sought to answer two questions:

1. What is the geographical distribution, demography, and behaviour of A. palliata in Bella

Vista and Limones?

2. What are the perceptions of the local communities towards monkeys and the conflicts

between the two?

6

Methods

Data collection

Research was conducted in the areas surrounding the villages of Bella Vista and

Limones, in the Barú district of the Chiriquí province. For each study area, interviews and direct observation were conducted. We conducted research in Bella Vista in four stages between early

January and late February 2017. We began by conducting semi-structured interviews with residents in the village and in the area south of the town leading to the tip of the peninsula.

Informants were first asked whether they had sighted monkeys in the past year. With the help of pictures, we asked them to specify which of the three species found in the region they had seen.

In the case of howler monkeys, we asked them to describe the location, number of individuals, and gender makeup of the groups they had sighted. They were also asked to report any locations where others had told them that howler monkeys could be found. Finally, we asked questions about their perception of the threats facing monkeys in the area, and their general opinion of monkeys. The interview questions can be found in Appendix 1. In total, 15 interviews were conducted in the Bella Vista area.

During each period of fieldwork, we used the information from interviews to establish the locations which had a high likelihood of containing monkeys. We began by verifying each location where a howler monkey group had been reported. Once we had surveyed these locations, we then surveyed along the gallery forest. These wooded areas alongside streams tended to be a good environment to find howler monkeys, which we were informed typically avoid open areas such as pastures and beaches. During the morning (7:00-11AM) and the

7 evening (3:00-7:00PM), we slowly walked through these areas and listened for monkey howls and barks. We also watched and listened for disturbances in the trees caused by howler monkey movement. We used these indirect observations to help us locate and directly observe howler monkeys. Once we made an encounter we recorded the number, age class (adult, juvenile, or baby), and sex of the monkeys in the group. We then recorded the date, time, and GPS location of the observation. We also characterized the behavior of the group according to four behavior types (Table 1). Finally, we recorded information about the group’s habitat, such as forest type.

The full set of observation criteria can be found in Appendix 2. In total we recorded 21 encounters with howler monkeys in the Bella Vista study area.

We conducted research in Limones during one weekend in mid-March using the same methodology. During this time, we obtained five interviews and three direct observations of howler monkeys. The rest of the data points for Limones were recorded by our supervisor, Ariel

Rodríguez-Vargas, on separate occasions.

The data we collected from our interviews was then used to inform a presentation to the community appropriate to its social context. This presentation took place April 19th, 2017. The first goal of the presentation was to present our quantitative results regarding howler monkey distributions, demography, and behavior and to explain what we had been doing in the community over the duration of the study. The second goal was more educative. In the morning, we held a presentation for the students at Bella Vista elementary school, introducing the concepts of conservation and of habitat loss to 22 students aged 5-11. With ideas from the students, we drew a concept map of the ways in which they can protect monkeys in their own community. In the later presentation for all members of the community, we also spoke about the importance of

8 monkeys in the ecosystem, and the ways in which protecting monkeys can positively impact humans as well.

This research was conducted according to the standards of McGill University and the Tri-

Council Policy Statement: Ethical Conduct for Research Involving Humans (TCPS 2). The

Course on Research Ethics (CORE) certification was obtained by members of the research team

(see Appendix 3).

Data analysis

In order to produce a visual representation of howler monkey sightings, we used ArcMap version 10.3.1. The area around Bella Vista was shown using the aerial satellite image available from ESRI, which was used as a basemap. We input the GPS points for each sighting and scaled the label according to the total number of individuals in the group.

Using these maps, we calculated the area of the corresponding forested area. We chose to omit non-forested areas (such as pastures, beaches and residential areas) since these are not suitable habitat for howler monkeys. The area of forest cover was measured by drawing polygons instead of using a forest cover map. Most raster maps of forest cover found online provided exact values for the forested area, but lacked detail for the Burica peninsula due to limited resolution. As a result, many did not include the gallery forest around Bella Vista.

Analyzing the satellite image and tracing the forested areas ourselves allowed us to achieve a closer representation of the forested areas being utilized by howler monkeys. The surveyed area around Bella Vista measured to be 7.74 km2. Consequently, the forested areas identified for the purposes of calculating density occupy only 30% of the study area. This signifies that one-third of the region around Bella Vista currently has the possibility of supporting howler monkey

9 populations. For each stream, the number of males, females, juveniles, and babies was totaled.

Density was then calculated by dividing the number of individuals by the area of the forest cover.

To produce the map for Limones, we used the three points which we collected during the two days we spent in Bella Vista and integrated a dataset gathered by our internship adviser, Dr.

Ariel Rodríguez-Vargas. Due to our limited data points, we did not attempt to analyze this map and present it only for the use of future studies.

Results and Discussion

Biological data

Geographical distribution

The map of Bella Vista clearly illustrates the fragmentation of the forest around Bella

Vista, as well as the howler monkey’s dependence on the forested areas (Figure 4). The overall density of howler monkeys in the total forested area is 63 individuals/km2, and the density for the entire region including non-forested area is 9 individuals/km2.

Figure 5 illustrates the forested area in and around Bella Vista in relation to the closest stream. The density of each area of these patches of forest is indicated. For the total area between

Quebrada del Medio and the tip of the peninsula, including forested and non-forested area, the population density was 19 individuals per km2. A high variance in density can be observed between the different streams. While Quebrada Resbalosa is connected to a relatively large area of continuous forest as well as two private reserves (Tigre Salvaje and Mono Feliz), it has one of the lowest population densities (28 individuals/ km2). It is probable that the groups counted in the

10 area surrounding Quebrada Burica, which had a density of 218 individuals/ km2, benefit from food availability and protected forest at Mono Feliz.

The population density of A. palliata can be affected by a variety of factors. A literature review by Chapman et al. 1998 analyzes over 80 population studies of howler monkey populations in order to understand the effect of habitat productivity on population characteristics.

The high variability in population densities suggested that recent events such as habitat alteration, hunting, food tree crop failure, and disease had a high impact on the groups (Chapman

& Balcomb 1997). Especially relevant is a long-term study on Barro Colorado Island, which illustrates the high variability of a single population over time, from an estimated 1500 individuals to less than 900 (Milton et al 1996). In cases where several groups were studied within the same area, increased levels of protection and food availability favored higher population density, however, long-term studies should be favored in order to understand the dynamics of howler monkey populations (Chapman & Balcomb 1997). Given the proximity to human populations, recent deforestation in the area, and the fragmentation of the habitat, it is likely that recent events in the history of the population have had an impact on population density. Without a detailed understanding of these events, it is difficult to establish their impact on individual groups in the study area. A long-term study comparing population density across time could yield a better understanding of the population dynamics of A. palliata in Bella Vista.

The data collected in Limones yielded a preliminary exploration of the howler groups in the area. While further study is required to verify and quantify the total number of groups in the region, a map was produced to illustrate the information available thus far (Figure 6). Although these points have not been analyzed to interpret the possible reoccurrence of troops, this

11 information can be used for future research. Table 4 summarizes the points which were gathered in the region, in the case where the groups could be verified and counted.

Behavior

Our results showed that out of the 19 encounters we had with A. palliata and recorded behavior, 53% occurred while howler groups were resting, 21% while some members of the group were resting and others were eating, 16% while the entire group was eating, and only 10% while the entire group was traveling (Figure 7). The breakdown of behavior by time of day was largely variable, but we did see a few trends. We found that the howlers we encountered mostly spent the morning resting and traveling, rested during midday, and spent the evening resting and eating (Table 2). The only time we observed howler groups traveling was during the morning, and a majority of eating encounters took place during the evening.

Our behavior results suggest that A. palliata spends a majority of the time resting, followed by eating, and finally spends a short amount of time traveling. This is consistent with other studies that show howler monkeys to be a relatively inactive species, likely due to their low-calorie diet (Milton 1980). A review of the literature surrounding the diet of Alouatta conducted by Kowalewski et al. (2015) found that howlers spend on average 19.7 ± 6.9% of the time eating, a finding that is consistent with our own results.

Because our encounters were biased towards the early morning and the evening, this may have skewed the behavior results. These were the times that the monkeys tended to howl, and we found them extremely hard to encounter during the times they were not howling. For this reason, we preferred to focus our sampling efforts to the morning and the evening, using midday to conduct interviews. Based on the few encounters we had during midday, we found that the

12 howlers preferred to rest during this time, likely due to the heat. We only encountered traveling groups during the morning, suggesting that the howlers spend most of the day within a small range. However, howler monkeys repeatedly use a few routes to travel between feeding and sleeping sites, so given our biased sample timing, we may have missed other times that howlers travel, such as afternoon or late evening. The small amount of encounters we had with traveling groups is consistent with the literature that documents that day range of all howler monkeys species is on average less than 600m (Kowalewski et al. 2015). Finally, most of the eating encounters were observed during the evening. However, given our low sample size for the behavior data these results should only be considered as preliminary observations. The behavior of howler monkeys in Bella Vista and Limones must be furthered studied with a greater sample size in order to test for any statistically significant trends.

Demography

The average group size that we encountered in Bella Vista was 6.8 ± 4.6, and in Limones was 8.1 ± 3.4 (Table 3). In La Pacifica, mean group size of A. palliata in fragmented habitat was 12.6 (Clarke & Zucker 1994). A 23-year study of A. palliata on Barro Colorado

Island, Panama found that mean group size in continuous forest was 19.0 ± 6.0 (Ryan et al.

2008). In La Pacifica, Costa Rica mean group size of A. palliata in fragmented habitat was 12.6

(Clarke & Zucker 1994). Comparing our results to these studies, we can thus see a potential impact of fragmentation on group size in our areas of study. Mean group size was slightly larger in Limones, due perhaps to a lesser degree of habitat fragmentation in the area compared to Bella

Vista. Group sizes more closely match the fragmented forests of La Pacifica, and are much

13 smaller than that of Barro Colorado Island. It is important to consider, however, the limitations of our study. Given our time limitations, we could not follow the groups for very long. It is possible, therefore, that some of the howler groups we encountered were merely subgroups that split off to forage. This would bias our results towards smaller group sizes, when in reality the groups may have been larger. Nevertheless, we can still say something about the presence of a lot of small groups. It has been documented that when resources are clumped at low densities (as is the case in landscapes with high fragmentation), howler monkeys are found in smaller subgroups (Chapman 1990).

Social data

Perceived threats

Through our interviews, we identified several perceived threats to howler monkeys: deforestation, capture for sale, capture for use as personal pets, hunting by humans for sport, hunting by humans for food, hunting by dogs, and climate change. In both Bella Vista and

Limones, we found that the most common perceived threat was deforestation (Figure 8). Capture for sale and hunting by dogs were the second most common perceived threats. We learned from three people that it was more common to keep monkeys as pets in the past, but over the last 15 years this has decreased. Six of our interviewees said that howler monkeys are not kept as pets in the area at all. In general, people in the area don’t really keep howler monkeys as pets. It is more common to keep the squirrel monkeys as a pet, but even this has decreased in the last 15 years.

14 In Limones, none of our interviewees mentioned the second most common perceived threats in Bella Vista (capture for sale and hunting by dogs). Instead, they perceived hunting by humans for food and for sport as the other threats to howler monkeys in the area. It is important to note that all five of our interviewees perceived deforestation to be a threat. This is may be due to the close proximity of Limones to an oil palm plantation, which may be a more evident form of deforestation since it occurred more recently than the deforestation of Bella Vista. However, this may also be an effect of small sample size and thus should not be too greatly emphasized without further study.

General observations

The preferred monkey of our interviewees in Bella Vista was a tie between the squirrel monkey or all three types (Figure 9). Howler monkeys and capuchins were both least favorite, with only one person voting for each. Despite this tie, we heard many negative opinions towards the capuchins throughout our interviews; seven people told us that the capuchins are bothersome because they eat crops and eggs and are often aggressive. There were much less negative views towards the howler monkeys, which were only disliked by three people because they are considered ugly and noisy. In general, people are pretty indifferent to howler monkeys, neither disliking nor particularly liking them.

In Limones, a majority of people said that they liked all three types equally. While the squirrel monkey and the capuchins tied for second favorite, no interviewee voted for the howler as their favorite. Interestingly, absent from our interviews in Limones were the strong negative feelings towards capuchins that we found in Bella Vista, with only one person mentioning instances of them eating crops. We hypothesize that this may be because a greater degree of area

15 around Limones is residential, lacking the livestock and crops that are more typical of Bella

Vista. Capuchins may thus be less of a nuisance to people in Limones. We must again, however, take into account our small sample size of interviews for Limones; the opinions of the few we interviewed may not accurately represent the views of the entire town.

Future conservation ventures

For the social part of our project, we strove to understand the social context of Bella

Vista and Limones and the relationship of the local communities to monkeys. Although the purpose of our study was neither to identify nor implement conservation strategies, the information that we gathered is the preliminary step in doing so in the future. For that reason, we believe it is important to discuss what the process of implementing those conservation strategies should entail. This requires a brief discussion of approaches to conservation.

The concept of conservation has continuously evolved throughout history. Early conservation movements emphasized an intrinsic value of nature, advocating for its preservation as a pristine environment untouched by humans. This is in contrast with later movements which had a greater focus on the instrumental value of nature. Gifford Pinchot, the first Chief of the

United States Forest Service, was a principal advocate for this, saying that “the purpose of

Forestry, then, is to make the forest produce the largest possible amount of whatever crop or service will be most useful, and keep on producing it for generation after generation of men and trees” (Pinchot 1998). In these early approaches, the point of conservation then was to protect nature in order to maximize its use for humans both for the present and for the future.

16 The idea of the instrumental value of nature has remained in modern concepts of conservation, which emphasize placing an economic value on the services that an ecosystem provides. The idea behind this is that in this post-neoliberal capitalist world, people will only care about protecting nature if they understand the costs associated with its loss. The ecosystem services concept thus seeks to maximize the costs and benefits associated with the loss or protection of a particular ecosystem: for example, assessing whether a piece of forest will have greater economic value to the greatest number of people in its intact state, which provides services such as carbon sequestration and water purification services, or in its conversion to timber (Collard et al. 2014).

The problem with the preservationist approach is that ecosystems are not static and pristine; they are dynamic and change over time even without human intervention. Both preservation and neoliberal conservation are furthermore problematic in that they often come at the expense of local communities. In its commodification of nature, neoliberal conservation often feeds resource extractive processes in developing countries. Neoliberal conservation advocates for partnership of conservation with corporations (Kareiva et al. 2012), promising increased public participation and property rights to local communities, in addition to green business practices. In reality, these approaches are detrimental to communities, often displacing local people while simultaneously excluding them from the benefits of the conservation projects, which are received instead by external actors (Igoe, J. & Brockington 2007). A prime example of this was the protection of the Panama Canal watershed, outlined by Carse (2012). In the 1970s, concerns over water supply for the Panama Canal necessitated a management approach that emphasized forest conservation. This management focused largely on protecting the forests around the Canal and addressing the deforestation activities of the people who lived in the

17 watershed. For example, forest guards were employed by the Panamanian government in order to protect the watershed from campesino farmers. Further ignoring the local context and the key processes important to the swidden agricultural system, a law was passed delineating rastrojo

(land burned post-crop growth) older than 5 years as protected forest. As a result, campesinos began to clear rastrojo earlier than they normally would have, decreasing the productivity of the land. Although protected areas strive to integrate conservation with ecosystem services (in this case, increasing the retention of water in order to increase the economic return of the Canal), they thus often negatively impact local communities. The failure of protected areas has been documented: in Thailand, for example, local support for Marine Protected Areas was minimal because they were perceived to have negative impacts on fisheries and agricultural livelihoods

(Bennett & Dearden 2014). Without community support, conservation efforts are more likely to fail. Conservation projects are thus successful when they are designed for the particular social and economic context of an individual community (Brooks et al. 2013). Furthermore, they must be designed not simply for but also with the local community; this involves public participation, allowing all potentially impacted actors the chance to voice their opinions and take part in decision making (Webler & Tuler 2000).

For these reasons, we believe that future attempts to implement conservation strategies in

Bella Vista and Limones should involve directly working with the community. As we saw firsthand, there is a huge economic dependence on cattle farming, which requires a lot of both space and time. In an attempt to protect monkeys, then, it is important not to overlook the needs of the local community. Significant barriers exist which may hinder the accessibility of conservation initiatives. Limited access to internet and electricity, as well as physical isolation, can make promotion and organization of projects difficult. In Bella Vista, the roads leading to

18 the homes further from the town are not usable throughout the entire year, further isolating those families. In some cases, conservation is not a priority simply because individuals feel that they have other, more serious concerns. In other cases, individuals care deeply about wildlife but lack the time and resources to carry out larger-scale projects within their community. Part of implementing conservation strategies may thus involve education, which is why for our presentation we focused on the importance of protecting forest both for the ecosystem and for its importance to the humans who live there. Future projects can also focus on starting dialogues between community members and allowing various stakeholders to contribute to conservation efforts in ways which are suitable to their capabilities and interests.

According to AMBIENTE Law 1, article 23 for rivers and streams in Panama a strip of forest must be left equal to the width of the channel on both sides, and this can never be less than

10 meters. Although from the map we can see that the streams on the area are still forested, when we surveyed alongside them we found that in most cases this law was not followed, with pasture often ending close to the edge of the streams. The lack of compliance to and enforcement of this law is evidence of the need to involve the local community in protecting the environment. Within both Bella Vista and Limones, we encountered a few people dedicated to the conservation of monkeys. We spoke with one man in Limones who had constructed a ladder bridge above the main road in order to connect the forests near his house to the forest across the street. Acts like these done by community members serve as important stepping stones to implementing conservation projects throughout the community.

19 Conclusion

In the context of a study area with a great degree of habitat loss combined with a high diversity of wildlife, it is important to assess the impacts of these land use changes on individual species. Howler monkeys are an interesting subject due to their flexible diet which allows them to persist in areas of anthropogenic disturbance. For this reason, there are still populations of mantled howler monkeys living in the Burica peninsula. However, we found that the fragmentation of the habitat in our study areas is indeed affecting A. palliata.

Maps were produced for Bella Vista and Limones, illustrating the geographic distribution of our sightings, as well as some points gathered by Dr. Ariel Rodriguez-Vargas. These show the monkey troops’ dependence on forested areas and highlight the high proportion of deforested area for both regions. These maps can also be used as an educational tool. For Bella Vista, the forested area covered 30% of the region between Quebrada del Medio and the tip of the peninsula, showing high fragmentation. Troops were present in both gallery forest and areas of continuous forest. Monkey sightings were dispersed across the forested area, and population density showed high variability between different regions of the study area. The significance of these density values is difficult to evaluate based on a single population study, and a long-term study would be useful to understand the dynamics of the troops around Bella Vista. In addition to showing the current state of A. palliata distributions and densities in Bella Vista and Limones, our maps thus serve as an important preliminary record to be compared against in future studies.

Although howler monkeys are a highly adaptable species, they are still unable to survive past a certain degree of habitat loss and fragmentation (Mandujano and Escobedo-Morales 2008). For example, inbreeding can occur in fragmented forests due to a loss of forest connectivity

(Oklander et al. 2010). The level of inbreeding is an interesting topic that could be explored in

20 future studies in order to give insight into the connectivity of the forest fragments. For our study we divided the area into fragments based on streams, but its likely that there is still a degree of connectivity and gene flow between the forests of these streams due to the forested areas along the coast.

The average group size that we found was similar to those found in other fragmented landscapes and much smaller than those of continuous forests, indicating that fragmentation indeed is having an effect on group size in Bella Vista and Limones. Our behavior data matches what is typically found in the literature, indicating that behavior (time spent eating, resting, and traveling) is not influenced by decreased habitat. In a study examining the effects of fragment size on various behavioral factors of howler monkeys, no correlation between fragment size and distance traveled daily was found (Bicca-Marques 2003). Rather than travel further to find food, howler monkeys adapt their diet to the area they inhabit.

Finally, the analysis of our interviews in Bella Vista shows a preference for squirrel monkeys, a dislike for capuchins, and an indifference towards howler monkeys. The dislike towards capuchins due to their tendency to eat crops could be used to help make the case for reforestation, since crop raiding is known to occur by both capuchins (Mckinney 2010, Freitas et al. 2008), and howler monkeys (Bicca-Marques 2009) when habitat is decreased. This point was also brought up by a community member during our presentation. Furthermore, deforestation is the most common perceived threat to howler monkeys in the area. However, this was only mentioned by 50% of our interviewees as a threat, possibly indicating the need for more education on the subject. Unfortunately, our sample size for Limones was too small to make any real conclusions regarding the opinions of the community towards monkeys.

21 Finally, we recommend the continued involvement of community members in the identification and implementation of conservation strategies. We hope that our results and observations can be a helpful preliminary step in empowering the communities in the Burica peninsula to manage and protect their environment. The students and community members that we encountered during our research exemplified the immense potential in this area, and we are interested to see how Bella Vista and Limones will respond to growing environmental challenges.

Acknowledgements

We would like to offer our deepest thanks to the communities of Bella Vista and Limones for participating in this project and offering us their time and knowledge during our research.

We would also like to thank the Universidad Autónoma de Chiriquí for enabling this project. We would especially like to thank Ariel Rodríguez-Vargas for offering his support and expertise, as well as the time taken to guide and assist us in carrying out our work.

We would like to offer special thanks to David Teichmann; Shawn, Shena, Reina and Lily Lockwood; Edwin Castillo; Silvia and Junior Ramírez; Mixila and Veronica Gonzalez; and Manuel and the staff of the Centro Educativo de Bella Vista.

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24 activities of human-commensal white-faced Capuchins (Cebus capucinus). American Journal of Primatology, 73(5), 439-448. doi:10.1002/ajp.20919 Méndez-Carvajal, P. G., Santamaría, M., & Moreno, R. A. (2005). An observation of agonistic behavior in howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama. Neotropical Primates, 13(1), 30-32. Milton, K. 1980. The foraging strategy of howler monkeys. Columbia University Press, New York. Milton, K. 1996. Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler monkey (Alouatta palliata) population in Panama. J. Zool. Lond. 239: 39-63. Murcia, C. 1995. Edge effects in fragmented forests: implications for conservation. Trends in Ecology & Evolution 10(2): 58-62. doi:10.1016/s0169-5347(00)88977-6 Oklander, L.I., Kowalewski, M.M., & Corach, D. 2010. Genetic consequences of habitat fragmentation in black-and-gold howler (Alouatta caraya) populations from Northern Argentina. Int J Primatol 31:813–832. “Panama Forest Information and Data.” Retrieved January 28, 2017, from http://rainforests.mongabay.com/deforestation/2000/Panama.htm Peres, C. A. 1997. Effects of Habitat Quality and Hunting Pressure on Arboreal Folivore Densities in Neotropical Forests: A Case Study of Howler Monkeys (Alouatta spp.). Folia Primatologica 68(3-5): 199-222. doi:10.1159/000157247 Pinchot, G. 1998. Breaking new ground. Washington (D.C.): Island Press.

“Población de la Republica.” Retrieved January 28, 2017, from http://www.contraloria.gob.pa/INEC/archivos/A2114.pdf Raguet-Schofield M. 2008. The effects of human encroachment and seasonality on the risk of mantled howler monkey (Alouatta palliata) predation by dogs on Island, . American Journal of Physical Anthropology 46: 176 Robinson, S. K., Thompson, F. R., Donovan, T. M., Whitehead, D. R., and Faaborg, J. 1995. Regional Forest Fragmentation and the Nesting Success of Migratory Birds. Science 267(5206): 1987-1990. doi:10.1126/science.267.5206.1987 Ryan, S. J., Starks, P. T., Milton, K., & Getz, W. M. 2008. Intersexual Conflict and Group Size in Alouatta palliata: A 23-year Evaluation. International Journal of Primatology, 29(2), 405-420. doi:10.1007/s10764-007-9172-2 Steinfeld H, Gerber P, Wassenaar T, Castel V, Rosales M, & Haan C. 2006. Livestock’s long shadow: environmental issues and options. UN Food and Agriculture Organization, Rome. Stoner, K. E. 1996. Habitat selection and seasonal patterns of activity and foraging of mantled howling monkeys (Alouatta Palliata) in Northeastern Costa Rica. International Journal of Primatology 17(1): 1-30. doi:10.1007/bf02696156 Urbani, B. 2003. Utilización del estrato vertical por el mono aullador de manto (Alouatta palliata, Primates) en Isla Colón, Panamá. Antropology 4:29–33 Webler, T. & Tuler, S. 2000. Fairness and Competence in Citizen Participation: Theoretical Reflections from a Case Study. Administration & Society 32: 566-593. World Commission on Environment and Development. 1987. Our common future. Oxford:

25 Oxford University Press.

Figures and Tables

Figure 1: Our study area within Panama

Figure 2A: Bella Vista study area Figure 2B: Limones study area

26

Figure 3A: Increase in pasture/cropland and Figure 3B: Increase in soybean and oil corresponding decrease in forest cover palm production in countries with howler (Kowalewski et al. 2015) monkeys (Kowalewski et al. 2015) (Kowalewski et al. 2015)

Figure 4: Map of Bella Vista

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Figure 5: Map of Bella Vista by stream

Figure 6: Map of Limones

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Percentage of encounters spent resting, traveling, or eating

Traveling 10%

Eating 16%

Resting 53%

Eating/Resting 21%

Figure 7: Behavior of howler monkeys by percentage of encounters.

Amenazas percibidas a los monos aulladores en Bella Vista 8

7

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0 Deforestación Captura para la Captura para Cacería por la Cacería por la Cacería por Cambio venta mascota gente para gente para perros climático comida deporte

Tipo de amenaza

Figure 8A: Perceived threats to howler monkeys in Bella Vista

29 Amenazas percibidas a los monos aulladores en Limones 6

5

s 4

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0 Deforestación Captura para la Captura para Cacería por la Cacería por la Cacería por Cambio venta mascota gente para gente para perros climático comida deporte

Tipo de amenaza

Figure 8B: Perceived threats to howler monkeys in Limones

Favorite type of monkey in Favorite type of monkey in Bella Vista Limones Howler 12% Capuchin 20% Capuchi All 3 n 38% 12%

All 3 Squirrel 60% 20% Squirrel 38%

Figure 9: Monkey preference by species in Bella Vista and in Limones.

30 Table 1: Description of behavior categories Type of behavior Description Resting The entire group was resting only.

Eating The entire group was eating only.

Resting/Eating Part of the group was resting and part of the group was eating.3 Traveling The entire group was moving through the trees to a different location.

Table 2: Behavior of howler monkeys by time of day. Resting Eating/Resting Eating Traveling Morning 7AM-11AM 4 2 0 2 Midday 11AM-3PM 3 0 1 0 Evening 3PM-7PM 3 2 2 0

Table 3: Average group size in different areas of study Location Mean number of monkeys per group (± SD) Bella Vista 6.8 ± 4.6

Limones 8.1 ± 3.4

La Pacifica – bosque fragmentado 12.6 (Clarke & Zucker 1994)

Isla Barro Colorado – bosque continuo 19.0 ± 6.0 (Ryan et al. 2008)

31 Table 4: Demography and area of streams in Bella Vista

32

Appendix 1: Semi-Structured Interviews

1. Fecha 2. Nombre 3. Localidad de la entrevista (con punto GPS) 4. ¿Cuántos años tiene? 5. ¿Cuántos años tiene de vivir en esta zona? 6. ¿Ha visto monos este último año? 7. ¿Qué clases de monos ha visto este último año (Mono aullador, mono tití, mono carablanca)? 8. ¿Hay clases de monos que ha desaparecido de la zona? 9. ¿Dónde ha visto los monos aulladores? 10. ¿En cual tipo de medio ambiente ha visto monos aulladores? 11. ¿Bosque nuevo, bosque secundario, rastrojos, bananales, bosque de galería, platanares, cocoteros, otras frutales (caimito, guaba, mango), cercas vivas? 12. ¿Cuales tipos de árboles comen los monos? ¿Comen las hojas o las frutas? 13. ¿Cree usted que los monos aulladores son a veces capturados para la venta o para mascotas? ¿Sino, en el pasado? ¿Hace cuánto tiempo? 14. ¿Cree usted que la deforestación afecta a los monos aulladores? ¿En su opinión, hay otras cosas que pueden afectar a los monos? 15. ¿Conoce de otras lugares donde se encuentran monos? 16. ¿Usted tiene comentarios adicionales?

Opiniones 1. ¿En general, le gusta usted la presencia de los monos en el área? ¿Todos tipos carablancas, titíes y aulladores? 2. ¿Cual es su tipo de mono favorito? ¿Porque lo prefiere? 3. ¿Hay razones porque no le gustan los monos? 4. ¿Cree que en general, la gente en el área le gustan los monos? 5. ¿En su opinión, cuáles beneficios tiene la presencia de los monos?

Appendix 2: Direct Observations

1. Date 2. Time 3. GPS point 4. Elevation 5. GPS device 6. Description of location (property owner, district, county) 7. Site ownership or jurisdiction (Private, municipal, federal) 8. Land use of area 9. Description of environment (Proximity to paths, bodies of water and open areas. Type of forest, possible sources of food)

33 10. Individuals in groups 11. Number of females 12. Number of males 13. Number of juveniles 14. Number of infants 15. Total 16. Behavior 17. Eating? How many? 18. Resting? How many? What type(s) of trees? 19. Other activities? How many? What type(s) of trees? 20. Did the group travel? If so: 21. New time 22. Type(s) of tree 23. New GPS point 24. Other observations: Mother separate from group? Parasites?

Appendix 4: CORE certification

34

35