Dissertation Course Name P20107

Title Tourist-Monkey Interactions at Iguazú National Park

Student Number 12037727 Surname Fahy

Other Names Martin

Course for which acceptable: MSc in Primate Conservation

Date of Submission 06/09/2013

This dissertation is submitted in part fulfilment of the regulations for an MSc degree.

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Tourist-Monkey Interactions at Iguazú National Park, Argentina

Martin Fahy

MSc Primate Conservation

Dissertation 2013

Abstract

Interactions between tourists and black capuchin monkeys, Sapajus nigritus, at Iguazú

National Park in Argentina involve tourists feeding monkeys, while monkeys also enter hotel rooms to obtain food. I collected behavioural data on interactions using ad libitum sampling over 86 days, and collected ranging data on the group over a period of 43 days. I estimated the home range and core area of the group using 95% and 50% fixed kernel analysis. I compared the home range of the monkeys with ranging data collected in 2010. Subadult male monkeys were involved in significantly more interactions than any other age/sex class, with a mean 40(SE ±3.1) interactions per individual over the study period. The home range of the group shifted southwards from 2010 to 2013, decreased in area from 103.14ha to

98.88ha. The monkeys visited tourist areas more frequently in 2013. Tourist interactions and hotel foods may be influencing the ranging patterns, sleeping site choice and group fission dynamics of the monkeys. Steps should be taken to discourage tourists from feeding monkeys at the park, and deterrents should be implemented to try to prevent monkeys from accessing the hotel building.

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Acknowledgements

I owe a debt of gratitude to a number of people who have contributed to this project in a variety of ways. Many thanks go to my supervisor, Dr. Kate Hill for her guidance, patience and assistance. Dr. Kimberly Hockings offered advice in the planning stage and helpful comments on draft sections of the dissertation. Dr. Giussepe Donati and Prof. Anna Nekaris provided support with data analysis and ranging software. Thanks also to Magdalena Svensson for her help during the year and the write-up.

Many thanks to Dr. Barbara Tiddi and Dr. Brandon Wheeler for first introducing me to the capuchins at Iguazú, for bringing me back to work on their projects and for providing funding to make the project possible. They also provided much help with the project planning, methods and analysis, as well as data from previous field work. I am indebted to Dr. Paula Tujague and Patricia Casco for collaboration in the field and in data collection. Gracias to the other researchers and assistants at Iguazú for their hard work and help in the field: Dr. Ilaria Agostini, Dr. Celia Baldovino, Dr. Romina Pfoh, Ester Bernaldo de Quieros, Tabitha Allen, Candelria Sanchez Fernandez, Allesandro Turchi, Julia Kern, Melissa Unger, Isabella Bollini, Tatiana Iretskaya, Riccardo Tiddi, Fransisco Silva and Fermino Silva.

Thanks to the Administraciones de Parques Nacionales for permission to study at Iguazú and for providing accommodation and facilities at the CIES. Thank you to Eduardo Mosquito Lestani for making life at CIES easier and more fun.

The project was helped by financial support from the Santander Student Project Award, so my gratitude goes to Santander, and to Loredana Faraon for facilitating the grant process.

A huge thanks to Maja Szybicka for her practical and emotional support throughout the project, and for putting me up and putting up with me during the last weeks of the write up.

My mother and father have always given me huge support in pursuing my goals, and have enabled me to carry out my studies. My sincerest gratitude goes to both of them.

Lastly, thanks to the Macuco monkeys for being so intelligent, persistent, awkward and determined to eat Pringles that I got enough interaction data to complete the project.

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Table of Contents

Abstract ...... i

Acknowledgements...... ii

Table of Contents...... iii

List of Tables ...... v List of Figures ...... v

Chapter One – Introduction ...... 1 1.1 The Human-Primate Interface ...... 1 1.2 Primates and Tourism ...... 2 1.3 Commensal Capuchins ...... 3 1.4 Study Aims ...... 4

Chapter Two - Materials and Methods ...... 5 2.1 Study Site ...... 5 2.2 Study Species...... 7 2.2.1 Sapajus nigritus...... 7 2.2.2 Study Group ...... 8 2.3 Rationale...... 9 2.3.1 Predictions ...... 10 2.4 Data Collection……………………………………………………………………………………………………………………….11 2.4.1 Tourist Interaction Sampling ……………………………………………………………………………………..11 2.4.2 Ranging data collection...... 12 2.5 Data Analysis...... 12 2.5.1 Interaction Analysis...... 12 2.5.2 Ranging Analysis...... 13

Chapter Three - Results ...... 14 3.1 Monkey-Tourist Interactions...... 14 3.1.1 Group-Level Interactions...... 14 3.1.2 Individual Interactions...... 14

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3.2 Ranging Analysis...... 16 3.2.1 Home Range and Core Area ...... 16 3.2.2 Sleeping Site Locations...... 17 3.2.3 Use of tourist area and location of interactions...... 17

Chapter Four - Discussion ...... 20 4.1 Data Collection and Sampling Bias...... 20 4.2 Monkey-Tourist Interactions...... 20 4.2.1 Group-Level Interactions...... 20 4.2.2 Influence of Sex and Age...... 21 4.2.3 Individual Differences...... 22 4.3 Ranging Patterns...... 24 4.2.1 Home and Core Range...... 24 4.2.2 Seasonal Influence – Fruit Availability...... 25 4.2.3 Influence of Platforms...... 26 4.2.3 Sleeping Site Locations...... 27 4.2.3 Location of Interactions...... 28 4.2.3 Human Foods Consumed...... 29 4.4 Group Fission...... 30 4.2.3 Subgroups...... 30 4.2.3 Dispersal...... 31 4.5 Aggression...... 31 4.6 Researcher Interference ...... 32 4.7 Mitigation Efforts...... 33

Chapter Five – Conclusion and Recommendations ...... 35 6.1 Conclusions ...... 35 6.2 Recommendations ...... 36

References ...... 37

Appendices ……………………………………………………………………………………………...... 43

Appendix I. Ethogram of Monkey Behaviours...... 43

Appendix II. Total Interactions per Individual and Mean Interactions per Age/Sex Class...... 44

Appendix III. List and Map of Sleeping Sites...... 46

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Appendix IV. Map of Platform Sites...... 48

Appendix V. Ethics Clearance Form……...... 49

List of Tables

Table 1. Individual interactions by sex and by age……………………………………………………………………15

List of Figures

Figure 1. Iguazú National Park...... ………………………………………………………………………5 Figure 2. Map of study site showing tourist areas and researcher trails...... 6 Figure 3. Timing of Interactions...... ……………………………………………………………………14 Figure 4. Mean (±SE) individual interactions per age/sex class...... ……………………………………15 Figure 5a. + 5b. Macuco home range and core area..…………………………………………………………………16 Figure 6. % Overlap of home range and core area...... ……………………………………………………..17 Figure 7. Location points of group centre 2010 and 2013...... … ……………………………18 Figure 8. Location of interactions and food obtained ……………………………………………………………….19 Figure 9. Types of human foods consumed ……………………………………………………………………………….19 Figure 10. Subadult male Dali approaches tourists …………………………………………………………………...21 Figure 11. Juvenile male Astor grinning and squealing ………………………………………………………………23 Figure 12. Subadult male Sergio on hotel balcony …………………………………………………………………….28 Figure 13a. + 13b. Subadult male Tito with sandwich and juvenile male Maverick with potato chips…………………………………………………………………………. .29 Figure 14a + 14b. . Signs warning against feeding animals …………………………………………………………33

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Chapter One – Introduction

1.1 The Human-Primate Interface

The study of the human-nonhuman primate interface has been identified as a major focal point of primatological research for this century (Fuentes & Hockings, 2010). As human populations continue to expand, there is an increasing ecological overlap between humans and primates (hereafter primates) through the expansion of agricultural and urban areas, and increased tourism to wildlife areas (Fuentes & Hockings, 2010). Consequently, the study of human- primate interactions should contribute to the development of management strategies that promote primate conservation (Fuentes & Hockings, 2010; Lee, 2010).

Humans and primates are increasingly brought into close contact in tourism settings (Fuentes et al., 2007), and these interactions are considered a threat to primate groups in many parts of the world (Fuentes & Gamerl, 2005; Maréchal et al. 2011). Tourism to natural areas is a growing industry which has the potential to provide benefits for local economies and protection for primate populations (Serio‐Silva, 2006). However tourism may impact on primates by increasing levels of aggression (Brennan et al., 1985; Fuentes & Gamerl, 2005), increasing stress levels (Behie et al., 2010) and by altering activity budgets (Saj et al., 1999), ranging patterns (Sabbatini et al., 2008) and habitat use (de la Torre et al., 2000). Problems associated with tourism are exacerbated when people feed primates (Fa, 1992; Orams, 2002).

Therefore, proper understanding of primate-tourist interactions is essential for the development of appropriate management strategies to ensure that wild populations and humans can coexist. Studies on tourism’s effects on the behaviour and socioecology of primates mostly concentrate on Old-world primates such as: great apes (Johns, 1996; Kalilova et al. 2010), macaques (Fuentes et al., 2007) and vervet monkeys (Saj et al., 1999). However the impacts of tourism on Neotropical species remain understudied (but see: Behie et al., 2010; de la Torre et al., 2000; Grossberg et al., 2003; McKinney, 2011 & Treves & Brandon, 2005). Primates are under threat throughout the Neotropics, due mainly to habitat loss, habitat fragmentation and hunting (Estrada, 2009). The impact of tourism on wild populations of Neotropical primates is a factor which merits further investigation.

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1.2 Primates and Tourism

Primate behaviour has been impacted in a number of ways at sites where tourism brings people into close contact with wild populations. This may take the form of aggressive behaviours directed towards humans or conspecifics (Grossberg et al., 2003; Fuentes & Gamerl, 2005; McCarthy et al., 2009). Humans acting aggressively towards primates can also be a problem at some sites (Hsu et al., 2008; Maréchal et al., 2011).

There are numerous examples of primates harassing and attacking tourists for food. Barbary macaques (Macaca sylvanus) in Gibraltar and long-tailed macaques (M. fascicularis) in Bali are both accustomed to receiving food from people and regularly bite tourists (Fuentes et al., 2007). At Mt. Huangshan in China, Tibetan macaques (Macaca thibetana) directed more aggressive behaviours towards humans when tourist densities increased (McCarthy et al., 2009). In an extreme case, aggression from Tibetan macaques resulted in ten human deaths at a Buddhist temple in China (Zhao & Deng, 1992). These aggressive encounters increase the risk of disease transmission between primates and humans (Jones-Engel et al., 2005).

Intragroup aggression has also been shown to be influenced by tourist interactions and provisioning. Provisioning may lead to violent contests for food, as has been observed in Formosan macaques (Macaca cyclopis) (Hsu et al., 2008), Tibetan macaques (McCarthy et al., 2009) and Barbary macaques (Maréchal et al., 2011). This increased aggression can have serious consequences for primate groups, with tourism pressure resulting in increased infant mortality rates in Tibetan macaques (Berman et al., 2007).

Provisioning can alter primates’ ranging patterns, as clumped food resources may reduce the amount primates need to travel in search of natural foods. This pattern has been observed in vervet monkeys (Chlorocebus pygerythrus) in Uganda (Saj et al., 1999), Kenyan baboons (Papio cynocephalus) (Altmann & Muruthi, 1988) and Barbary macaques in Gibraltar (O’Leary & Fa, 1993).

Interactions with tourists can alter activity budgets and lead to increased stress levels for wild primates. Pygmy marmosets (Cebuella pygmaea) in Ecuador showed reduced levels of play behaviour and altered use of forest strata in response to high tourist numbers (de la Torre et al., 2000). Reduced feeding and increased vigilance rates were correlated with tourist proximity in a silverback gorilla (Gorilla gorilla gorilla) in Central African Republic. Physiological (faecal cortisol levels) and behavioural (self-scratching rates) indicators of stress were positively related to the number of interactions between tourists and Barbary macaques (Macaca sylvanus) in Morocco (Maréchal et al., 2011). Howler monkeys (Alouatta pigra) in Belize that were exposed to tourists

2 had higher cortisol levels than monkeys in areas without tourists (Behie et al., 2010). Tourist interactions could therefore negatively impact on the health and reproductive capacity of animals through increased stress levels (Maréchal et al., 2011).

1.3 Commensal Capuchins

Capuchin monkeys (Cebus and Sapajus spp.) are small-bodied omnivores that a have wide distribution from Honduras to Argentina (Fragaszy et al., 2004). Capuchins interact with humans in a number of ways throughout their range: as a food source, crop-foragers, tourist attractions, pets, cultural symbols or subjects of entertainment (Fragaszy et al., 2004). In Europe and North America capuchins are commonly kept as pets, perform in films and television, and have been trained as helper animals for the severely disabled.

As very adaptable primates with a high degree of behavioural flexibility, capuchins can readily incorporate human food into their diet, such as provisioned or discarded food (Sabbatini et al., 2008) and agricultural crops (Galletti & Pedroni, 1994). Bearded capuchins (Sapajus libidinosus) living in an urban park in Brasília adjusted their activity budget and ranging patterns according to the number of visitors to the park. The monkeys spent less time travelling and feeding on wild foods when visitor numbers were higher, and spent 31.5% of their feeding time consuming provisioned food (Sabbatini et al., 2008). When tourism infrastructure was developed in an agro- forestry nature reserve in Costa Rica, white-faced capuchins (Cebus capucinus) became rapidly accustomed to consuming non-natural discarded foods and handouts from tourists (McKinney, 2011). The provisioned group spent less time foraging for insects and more time resting than a non- provisioned group in the area (McKinney, 2011).

Few studies exist on the impact of tourism on wild capuchins, though some studies have examined their crop-feeding behavior. Successful crop feeding primates such as baboons, vervet monkeys and macaques often tend to exploit other sources of human food (Else, 1991), and this behavior is indicative of species that can persist in anthropogenically altered habitats. Tufted capuchins (Sapajus spp.) in Brazil dramatically increased their reliance on crop consumption when wild fruit production was lowest, indicating that crops served as a fallback food (de Freitas et al., 2008; Siemers, 2000). Conversely, another studied group consumed more crops when high levels of fruit were available in the forest (Galetti & Pedroni, 1994), illustrating that capuchins can exploit clumped non-natural food sources whether or not natural food is scarce.

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The population of black capuchin monkeys (S. nigritus) at Iguazú National Park in Argentina has been studied for over twenty years (Brown & Zunino, 1990; Janson, 1996; Di Bitetti, 1997). Interactions between tourists and monkeys from the most intensively studied group, the Macuco group, have become a concern for researchers (Janson et al., 2012): many of these interactions involve tourists feeding monkeys. The monkeys regularly visit a hotel within the park where they may receive handouts, or enter empty rooms and obtain food from inside (personal observation). These interactions pose potential dangers for visitor safety and may impact on the monkeys’ behaviour and health.

1.4 Study Aims

The aims of this study are to:

1.) Describe the pattern of tourist-monkey interactions and hotel visits by monkeys at Iguazú National Park.

2.) Assess whether age and sex influence the likelihood of individual monkeys to interact with tourists and/or visit the hotel.

3.) Compare the amount of human food monkeys obtain at the hotel to other tourist areas.

4.) Identify the Macuco group’s home range and area of core use, and identify the extent to which the group uses the tourist area.

5.) Compare ranging patterns from 2010 to 2013 to investigate whether tourist area use has increased.

6.) Develop recommendations for management strategies to reduce the negative impact of tourist-monkey interactions.

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Chapter Two – Materials and Methods

2.1 Study Site

The study took place at Iguazú National Park in the province of Misiones, Argentina (2540’S, 5430’W) (Fig. 1.). The 60,000ha national park is part of the Upper Paraná Atlantic forest, and is characterised by semideciduous forest (Giraudo et al., 2003). The climate is humid subtropical with an annual precipitation of 1500-2100mm, and no marked dry season (Brown & Zunino, 1990). Iguazú National Park and Urugua-í Provincial Park are the two largest protected areas in Misiones, forming a vital part of the “Green Corridor”, a network of protected areas extending throughout the province and into Brazil (Di Bitetti et al., 2006). These protected areas are an important reservoir for the Argentine capuchin population, which is threatened by habitat degradation and forestry conversion (Di Bitetti, 2003). Fleshy fruits and arthropods, the preferred foods of the study animals, show marked seasonality and are most scarce during the winter months of May-August (Brown & Zunino, 1990; Di Bitetti & Janson, 2001).

Fig. 1 – Iguazú National Park

Selective logging took place at the site until it was designated a national park in 1937 (Hirsch, 2009). The largest trees have been removed, and much of the remaining forest is characterised by a

5 thick understory of bamboo. The dense vegetation hinders researcher access through much of the forest. A trail network is used to follow monkeys at the site. Trails are separated by approximately 200m, and were mapped by Janson and colleagues (Fig. 2).

Fig. 2 – Map of study site showing tourist areas and research trails

The waterfalls in the national park are one of the biggest tourist attractions in South America, attracting over one million visitors in 2011 (APN, 2012). There is an extensive tourist infrastructure which includes roads, train tracks, walking trails, a large hotel, a water treatment plant, shops, cafes and steel walkways. Visitor numbers are increasing annually and can reach several thousand in a day (APN, 2012.

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Capuchin monkeys are the only primates that inhabit the site. Potential and confirmed monkey predators occurring at the site include: black hawk-eagles (Spitzaeus tyrannus), ornate hawk-eagles (Spitzaeus ornatus), jaguars (Panthera onca), pumas (Puma concolor), ocelots (Leopardis paradilis), jaguarundis (Puma yagouaroundi), margays (Leopardus wiedii) and tayras (Eira barbara) (Janson et al., 2012). Several poisonous snake species also pose a threat to the monkeys here.

2.2 Study Species

2.2.1 Sapajus nigritus

There is some dispute over the taxonomy of capuchin monkeys. Traditionally both tufted and non-tufted capuchins were considered a single genus, Cebus (Groves, 2001). I have followed Lynch-Alfaro et al. (2012), who argued that the capuchins should be split into separate genera, Cebus for non-tufted and Sapajus for tufted capuchins.

The range of the black capuchin extends from the south east coast of Brazil to the northern tip of Misiones in Argentina. In Brazil, it occurs south of the Rio Doce, in the states of Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo, Paraná, Santa Catarina and Rio Grande do Sul (Kierulff et al., 2008). Sapajus nigritus is listed as near threatened by the IUCN, due to an ongoing decline in the population of less than 30% over three generations (Kierulff et al., 2008). Habitat loss, habitat degradation and hunting are considered the species’ major threats (Kierulff et al., 2008).

There is an extensive body of research on the capuchin monkeys at Iguazú because the population has been studied on an ongoing basis for over 20 years. A variety of behavioural and ecological studies have been carried out on topics including: feeding ecology (Brown & Zunino, 1990), the social role of grooming (Di Bitetti, 1997), vigilance and social monitoring (Hirsch, 2002) sleeping site choice (Di Bitetti et al., 2001), infanticide (Ramírez-Lorens et al., 2008) and intergroup encounters (Scarry, 2013).

Fruit makes up the main part of the diet from October to March, while insects are heavily relied on during the austral spring (Brown & Zunino, 1990). Palm fruits (Sygarus romanzzoranum), bamboo shoots (Chusquea ramosissima), figs (Ficus spp.), leaf bases of epiphytes and exotic fruit species (Hovenia dulcis and Citrus spp.) are the most important food sources during winter (Di Bitetti, 2001a). The monkeys spend 70-90% of the day foraging, spending more time looking for invertebrates than feeding on fruit (Di Bitetti, 2001a). Males eat more animal foods, and search for

7 more invertebrates in woody microhabitats than females, who eat more fruit than males (Agostini & Visalberghi, 2005).

Groups have a core area of home range use, with peripheral areas that shift in relation to fruit availability (Di Bitetti, 2001a). Capuchins at Iguazú occur at densities of 16 individuals/km2, and groups have an average home range size of 161 ± 77 ha (Di Bitetti, 2001a). Home ranges of groups partially overlap, and intergroup encounters are characterised by aggression (Di Bitetti, 2001a). The resource holding potential of groups is related to the number of adult males in the group, and demographic changes can result in a shift in home range (Scarry & Tujague, 2012).

Feeding platform experiments have been used in a range of studies at Iguazú. The use of feeding platforms allows researchers to manipulate the spatial location and abundance of food within the monkeys’ range, in order to test the ecological significance of changes in social behaviour due to the presence of feeding platforms (Janson, 1996). Factors investigated using feeding platforms have included spatial memory (Janson, 1998), home range use (Di Bitetti, 2001) and the function of alarm calls (Wheeler, 2009). Provisioning experiments have not had a significant effect on birthrates or infant survival rates in the provisioned groups relative to non- provisioned groups at the site (Di Bitetti & Janson, 2001a; Ramírez-Llorens et al., 2008).

2.2.2 Study Group

The Macuco group currently consists of 26 members, with two adult males, three adult females, five subadult males (2 natal), four subadult females, eight juvenile males, one juvenile female, two infant males and one infant female. The group has been studied since 1991 and are well habituated to observers, allowing full day follows. Long-term demographic data are available for the group, as they have been censused at least twice a year since first studied (Janson et al., 2012).

The Macuco group has split three times since studies began. All group fission events were associated with alpha male takeovers, though not all takeovers have resulted in group fission (Janson et al., 2012). Alpha male takeovers are associated with the disappearance of infants from the group due to infanticide, and infanticide avoidance may influence the formation of new groups (Janson et al., 2012). The group first fissioned in 2004, and again in 2005, with the newly formed groups moving to new areas, while the Macuco group remained in their traditional home range (Ramírez-Llorens et al., 2008). From November 2009 to January 2010 a period of intense fighting amongst males in the Macuco group led to the formation of another group (Spot group). The

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Macuco group subsequently suffered a loss of resource holding potential, won significantly fewer intergroup encounters and shifted their core area of home range use (Scarry & Tujague, 2012).

2.3 Rationale

The tourist-monkey interactions at Iguazú pose a number of potential problems for both the animals and for visitors to the park. Monkeys at Iguazú may become accustomed to harassing visitors in order to obtain food, as has happened at other sites (Else, 1991; Fa, 1992, Fuentes et al., 2007). Increased contact with humans could expose both monkeys and humans to the risk of disease transfer, particularly if aggression escalates to biting levels (Chapman et al., 2005). The consumption of non-natural foods could lead to the disruption of normal activity budgets, health problems such as diabetes (Kuhar et al., 2013) or parasite exchange (Chapman et al., 2005).

Human perceptions of primates influence the likelihood that primates will be considered as suitable pets (Duarte-Quiroga & Estrada, 2003; Ceballos-Mago & Chivers, 2010). Visitors to urban parks in Brazil where monkeys receive food from humans described capuchins as “amusing”, “intelligent” and “cute” (Sabbatini et al., 2006). With the huge numbers of visitors at Iguazú, the perception of capuchins as animals that interact with humans could have a potential knock-on effect and fuel the primate pet trade. Indeed, capuchins are already sometimes kept as pets in the region around Iguazú (Di Bitetti, 2003).

Several factors may be contributing to the extent that the Macuco group enters into the tourist area and interacts with tourists. The sex and age of monkeys may be an important factor in determining which individuals are more likely to interact with tourists and/or approach the hotel in search of food. In a number of cases, male primates have been found to participate more often than females in interactions with tourists. Adult and subadult male long-tailed macaques (Macaca fascicularis) were the predominant age/sex classes involved in aggressive interactions with humans at a temple in Bali (Fuentes & Gamerl, 2005). Subadult male and juvenile Barbary macaques in Gibraltar were the most likely age class to initiate interactions with humans (O’Leary and Fa, 1993).

The Macuco group has undergone demographic changes in recent years that have influenced the ranging patterns of the group (Scarry & Tujague, 2012). This may have had the effect of increasing the Macuco groups’ reliance on the more touristic area of their home range. The group may be expected to visit tourist areas more frequently now than it did in the past.

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Capuchin groups at Iguazú adjust their ranging patterns seasonally in accordance with food distribution and availability (Di Bitetti, 2001a). Fruit and arthropod production at Iguazú is lowest between May and August (Brown & Zunino, 1990), and this period also coincides with the high season for tourism (July-August). Therefore, more food may be available in tourist areas at the time of year when the natural foods are scarce.

2.3.1 Predictions

1.) Juvenile and subadult male monkeys will be involved in more direct tourist interactions than other age/sex classes.

2.) Monkeys will obtain a greater amount of food when at the hotel than when at other tourist areas.

3.) The Macuco group will use the tourist area more intensively in 2013 than in 2010.

2.4 Data Collection

2.4.1 Tourist Interaction Sampling

Data were collected from May 1st to July 21st 2013, for a total of 83 days. The group were followed for approximately eleven hours each day, resulting in a total of 820 hours of observation. Data on tourist interactions and hotel visits were collected primarily by Martin Fahy, Dr. Paula Tujague and Patricia Casco. Supplementary information on tourist interactions was provided by a team of eight field assistants working on projects for Dr. Barbara Tiddi and Dr. Ilaria Agostini.

Researchers at Iguazú have a policy of preventing direct contact and food transfer between humans and monkeys, and preventing monkeys from gaining access to the hotel and restaurants in the park. Interference took the form of blocking monkey’s access to the hotel or cafes, advising tourists that feeding monkeys is not permitted, and informing park guards and hotel employees when monkeys were accessing the hotel. This interference influenced the nature of interactions, by reducing the amount of food the monkeys received and reducing the number of times they accessed the hotel.

Data on tourist-monkey interactions were collected using ad libitum sampling (Martin & Bateson, 2007). When monkeys were in tourist areas, all visible instances of contact between monkeys and people were recorded. Data were collected using digital voice recorders and subsequently transcribed into Microsoft Excel files. Individual monkeys were recognised based on

10 body size, sex, colour patterns and body features. Inter-observer reliability tests were carried out to ensure that all members of the research team could identify individuals accurately and record behaviours consistently (Martin & Bateson, 2007), only data from observers that scored ≥ 0.8 in reliability tests were included in the analysis.

Group-level interactions were recorded each time tourists and monkeys interacted, or whenever monkeys accessed or attempted to gain access to the hotel or restaurants. The date, time and location of each event were recorded, along with the identities and actions of all monkeys involved in the group-level interaction.

Individual interactions were recorded for each individual animal involved in a group-level interaction. If several monkeys were involved in a group-level interaction whereby some directly interacted and others did not directly interact, the group-level interaction was classed as direct. However, when calculating rates of individual interactions, only the monkeys that actively participated in an interaction were scored as having directly interacted.

Direct interactions were interactions in which monkeys actively participated in an interaction, i.e. by approaching or attempting to approach tourists and by accessing, or attempting to gain access to the hotel or cafes. Interactions were considered direct if researchers actively intervened to prevent food transfer or physical contact between people and monkeys, or prevented monkeys from accessing the hotel building.

Indirect interactions were interactions where monkeys did not actively participate in interacting with people, i.e. when tourists photographed monkeys, directed gestures and vocalisations towards monkeys but monkeys did not respond, or when monkeys interacted with coatis (Nasua nasua) for access to human foods.

For each interaction we recorded:

- The date, time, duration and location of interactions. - The ID of all monkeys involved in interactions. - Noises, gestures and approaches directed from tourists to monkeys and vice versa (see appendix I for ethogram of monkey behaviours). - Contact or attempted contact, including exchange of food items from tourists to monkeys. - Type of human foods consumed by monkeys. - Interference by researchers or park employees in interactions, or prevention of interactions by researchers (e.g. researchers blocking monkeys’ path to hotel).

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- All instances when monkeys gained access to the hotel building, or were prevented from gaining access by researchers or employees.

2.4.2 Ranging Data Collection

Ranging data in 2013 were collected for a total of 43 days from June 9th to July 21st, after an initial training period for field assistants. Universal Transverse Mercator (UTM) geographic coordinates of the group centre were taken at 30 minute intervals using a handheld Garmin 62S GPS unit. The group centre was considered to be the point at which the majority of group activity was occurring, estimated by visual observation of group spread (Scarry, 2013). When monkeys were travelling in inaccessible areas, group centre coordinates were estimated and projected using the GPS and/or in relation to the georeferenced trail system at Iguazú (Scarry, 2013). Ranging data for the Macuco group in 2010 were collected by Wheeler and Tiddi (unpublished data). I analysed data from the same dates in 2010 as were recorded in 2013 (9th June – July 21st, n=43 days). Group location in relation to the trail system, and direction of travel were recorded every thirty minutes. During both field seasons, the group was followed nearly continuously, though the group was occasionally lost by researchers, or became too fragmented to accurately judge group centre. This resulted in a total of 850 location fixes for 2010 and 899 location fixes for 2013.

2.5 Data Analysis

2.5.1 Interaction Analysis

I calculated the number of direct, indirect and total group-level interaction and the number of interactions for each individual. I calculated the mean number of individual interactions for each sex and for three age classes, juveniles (1-5 years), subadults (6-10 years) and adults (>10 years). Infants (<1 year) were excluded from the analysis. As there was only a single juvenile female (5 years old) in the study group, I excluded this age/sex class from statistical analysis of individual interactions.

I used the Shapiro-Wilk test to test the data for normality of distribution. I used a two-way ANOVA to test the influence of age and sex class on individual interactions. I used Fisher’s exact test to test for differences in the number of days the monkeys visited the tourist area over the two years. I examined the difference in amount of food obtained at different sites using Pearson’s chi-squared test. All statistical analyses were carried out using SPSS 17. Significance levels were set at p<0.05, and standard errors are reported for all mean values.

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2.5.2 Ranging Analysis

I downloaded and edited GPS co-ordinates using Garmin Base Camp software. I created waypoints based on group location in relation to the trail system for ranging data recorded in 2010. I used Ranges7 software for the ranging analysis, and created range maps using ArcGIS 10.0.

I estimated home range using 95% fixed kernel analysis, which gives a more accurate reflection of home range use than Minimum Convex Polygon methods (Grueter et al., 2009; Pimley et al., 2005). I excluded areas that the monkeys do not use from the analysis, e.g. car park, tennis courts and swimming pool. The area of core use was determined using 50% fixed kernel analysis (Hadi et al., 2012; Scarry & Tujague, 2012). I chose kernel analysis because it can be used to show the intensity of use of different areas within an animal’s home range (Kernohan et al., 2001). I analysed the overlap of total home range and core range overlap for the group in 2010 and in 2013.

I compiled a list of all known sleeping sites for the group during the study period in 2013 (May 1st – July 21st, n = 58), and compiled a list of sleeping sites used during the roughly the same period in 2010 (May 19th – July 28th, n= 52). I compared the frequency of sleeping site use over both years, and counted the number of times the group used a site on consecutive nights. Some sleeping sites were in close to proximity to others (<100m), and the group often slept dispersed over an area of over 100m. For this analysis I considered sleeping sites that fell within a 100m radius of each other as a single sleeping location.

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Chapter Three –Results

3.1 Monkey-Tourist Interactions

3.1.1 Group-level Interactions

A total 209 group-level interactions were recorded, with 52% (n=109) involving direct interactions and 48% (n=100) being indirect. Monkeys received food in 26% (n=55) of events, and researchers intervened in 26% (n=55) of events. More interactions were recorded during the middle of the day than in the evening or the morning (Fig. 3).

50 n = 98 45 % Interactions 40 35 n = 68 30 25 n = 43 20 15 10 5 0 Morning (7:00-11) Afternoon (11-15) Evening (15-18:30)

Fig. 3 – Timing of interactions

3.1.2 Individual Interactions

Within the 209 group-level interactions, a total of 471 individual interactions were recorded, of which 226 were indirect and were 245 direct. The mean number of total interactions per individual was 20.8(±2.8), with a range of 0-48 interactions per individual. There was a mean of 10.6(±1.5) direct interactions per individual, with a range of 0-29. Subadult males had the highest interaction rate of all age/sex classes, with a total mean of 40(±3.1) interactions, and a mean 20.4(±1.7) direct interactions.

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Table 1. Individual interactions by sex and by age Age/Sex Indirect Direct Total

Whole group (n= 23) 226 245 471 Males (n= 15) 139 191 330 Females (n=8) 87 54 141 Adults (n= 5) 53 20 73 Sub-Adults (n=9) 118 148 266 Juveniles (n=9) 55 77 132

25.00 n = 5

20.00

n = 2

15.00 n = 8 n = 3 SE)

n = 4 ±

10.00 Mean ( Mean 5.00

.00 Juv M S-Ad M Ad M S-Ad F Ad F

Age/Sex Class Indirect Direct

Fig. 4. Mean (±SE) individual interactions per age/sex class

Two-way ANOVA tests showed there was no significant interaction between the effects of age and sex on individual indirect interactions, (F2, 22 = 3.894, p = 0.065), or on direct interactions (F2,

22 = 2.590, p = 0.126). When age and sex were examined separately, the number of indirect interactions between capuchins and tourists was significantly influenced by age, (F2, 22 = 6.463, p = 0.008), with subadults involved in more interactions than other age classes. Sex did not have an effect of the number of indirect interactions per individual (F1, 22 = 0.685, p = 0.491).

Sex had a significant effect on the number of direct interactions (F1, 22 = 4.499, p = 0.049), with males involved in more direct interactions than females. Age also had a significant effect on the number of direct interactions (F2, 22 = 5.300, p = 0.016), with subadults involved in more direct

15 interactions than both juveniles and adults. Subadult males participated both in more indirect and direct interaction than any other age/sex class (Fig. 4).

3.2 Ranging Analysis

3.2.1 Home Range and Core Area

The Macuco group’s area of home range and core range shifted considerably between 2010 and 2013 (Figs. 5a + 5b). The total home range slightly decreased in area from 103.14ha in 2010 to 98.88ha in 2013. A large area the northern part of the home range used in 2010 was not visited by the group in 2013. There was an overlap of 60.62 ha of the home ranges over the two study periods. The home range in 2013 encompasses a larger amount of the tourist area than the range over the same months in 2010.

Fig. 5a. Macuco home range Fig. 5b. Macuco core are

The core area used decreased from 40.9ha to 26.9ha, indicating that the group used a smaller area more intensively in 2013 than in 2010. The tourist area was not a part of the group’s core range in either year, but the area beside the hotel was part of the core range in 2013 (Fig. 5b). There was an overlap of 13.95ha of the core areas over the two study periods (Fig. 6).

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70 2010 2013 60 50 40 30 20 10 0 Home range overlap (%) Core range overlap (%)

Fig. 6. % Overlap of home range and core area

3.2.2 Sleeping site locations

The Macuco group used 9 sleeping sites during the study period in 2010, and 11 during 2013. The group used sleeping sites within 200m of the hotel on six occasions in 2010, and on 21 occasions in 2013. The group slept at the same site on consecutive nights three times during 2010 and 12 times in 2013 (see appendix IV for map and list of sleeping sites).

3.2.3 Use of tourist areas and location of interactions

The Macuco group visited the tourist area more frequently in 2013 (60% of study days, n=25) than in 2010 (20% of study days, n = 8). Fisher’s exact test shows that the difference in the amount of days over the two study periods was significant (two-tailed, p = 0.035). Furthermore, tourist areas were more intensively used in 2013 than 2010 (Fig. 7).

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Fig. 7. Location points of group centre 2010 and 2013

The hotel was the site with the highest number of group-level interactions (27%, n=57). The monkeys obtained food at the hotel more often than in at all other locations, accounting for 52.7% of all feeding events (Fig. 8). Monkeys obtained food in 50.9% of group-level interactions at the hotel. The monkeys obtained food at the hotel significantly more often than at any other location (Pearson’s chi-squared test, p = 0.000). Bread, biscuits and potato chips were the most commonly consumed foods (Fig. 9).

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60.0 % Group interactions 50.0 % Food obtained 40.0

30.0

20.0

10.0

0.0 Sheraton Fortin Cafe Paseo sup - Cataratas Dos Herm Other Hotel Faro Station Cafe

Fig. 8. Location of interactions and food obtained

16

14

12

10

8

6

4

2

0 Bread Biscuits or Chips Fruit Unknown Others Juice Crackers (candy, etc.)

Fig. 9. Types of human foods consumed

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Chapter Four – Discussion

4.1 Data Collection and Sampling Bias The ad libitum method was used due to constraints on data collection in the field. Scan sampling would have provided a more robust measure of interaction rates among monkeys and tourists (Altmann, 1974). Focal sampling would have enabled me to investigate whether monkey behaviours and activity budgets were affected by tourist presence (Martin & Bateson, 2007). However, due to difficulties with sampling and field assistant training I was unable to carry out reliable scan sampling, or perform a sufficient number of focal samples while monkeys were in the tourist area. The ad libitum method was deemed appropriate to maximise data collection and enable the sharing of data with Dr. Tujague.

While all individuals were recognisable by the author, data collection by assistants may have been subject to bias. Juveniles were less easily distinguishable than adults, and may be underrepresented in the data set. This age class may therefore have been more likely to be involved in interactions than is represented by the data.

The presence of researchers probably had an effect on the behaviour of tourists at the site. Tourists may have been less likely to feed or try to initiate direct contact with monkeys in the presence of researchers. As researchers also frequently spoke with visitors and explained the rules and rationale for avoiding feeding monkeys, it is highly probable that the rate of interactions is higher when researchers are not present. While a less biased account of monkey-tourist interactions may have been gathered had researchers not intervened, researcher intervention is a factor which affects tourist-monkey interactions at the site, whether or not tourist behaviour has been the topic of study.

4.2 Monkey-Tourist Interactions 4.2.1 Group-Level Interactions

Tourists and monkeys interacted frequently during this study, with a total of 209 group-level interactions recorded. Over half (52%) of group-level interactions involved monkeys directly interacting with tourists. Indirect interactions involved tourists photographing, calling, whistling, gesturing and shouting at monkeys. Even seemingly innocuous indirect interactions may have an impact on primate welfare. Rates of scratching among Barbary macaques‘ of self-scratching rates

20 were correlated to tourist presence, whether or not tourists interacted directly with monkeys (Maréchal et al., 2011).

Fig. 10. Subadult male Dali approaches tourists

More interactions took place in the middle part of the day (47%), than in the morning (21%) or the evening (32%). This is most likely as a result of tourist presence generally being highest during this period. The location of interactions varied depending on the time of day, with more interactions occurring at the hotel in the morning and evening, while interactions at other locations occurred more frequently in the middle of the day.

4.2.2 Influence of Sex and Age

Two-way ANOVA tests showed no significant interaction between age and sex on numbers of individual interactions, i.e. the two sexes did not differ significantly in their number of interactions based on age class. However males did directly interact significantly more often than females, and subadults directly interacted significantly more than juveniles and adults. Adults and juveniles did not differ significantly in their levels of direct interactions. Sex did not have a significant influence on the levels of indirect interactions. As indirect interactions arose from monkeys simply being in tourist areas, and did not require any participation by monkeys, sex was not expected to influence levels of indirect interactions. Subadults had significantly higher levels of indirect interactions than other age classes, which was an unexpected result. Subadults may also have tended to forage closer to tourist trails than other age classes, resulting a higher number of indirect interactions among subadults.

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Based on the results of other studies of human-monkey interactions (O’Leary & Fa, 1993; Sabbatini et al., 2006), I predicted that juvenile and subadult males would engage in more direct interactions than other age/sex classes. The results show that this prediction proved accurate in the case of subadult males, as they were involved in significantly more direct interactions than all other sex/age classes. However, juvenile males showed similar levels of direct interactions to other age/sex classes. Juvenile and subadult males were the only age/sex classes to have a higher mean number of direct interactions than indirect interactions. As there is only a single juvenile female in the group, I was unable to compare the number of interactions between male and female juveniles. All subadult males had high numbers of direct interactions, but there was more variation among the number of direct interactions for juvenile males.

Male capuchins consume more animal foods than females, and adopt a more opportunistic, higher-risk foraging strategy than females (Agostini & Visalbergi, 2005; Fragaszy et al., 2004). Males and juveniles are more likely to respond to novel foods than females and adults (Visalberghi et al., 2003). These foraging traits predispose young male capuchins to engage in potentially risky activities, such as consumption of non-natural foods, entering buildings and approaching humans. As there are only two fully adult males in the group, the degree of difference between adult and younger males in tourist interactions is difficult to assess. The low sample size meant that individual differences in interaction levels had a strong effect on the outcome for the different sex and age classes.

4.2.3 Individual Differences

Primates show strong inter-individual differences in their rates of interactions with tourists. For example, nine bearded capuchins from a group of 26 were involved in 86% of interactions with visitors in a Brazilian urban park (Sabbatini et al., 2006). In this study, eight (5 subadult and 2 juvenile males and one subadult female) out of 23 monkeys accounted for 67% of all direct interactions (appendix I). The degree to which individuals benefit from consuming human foods may vary according to age and social factors such as rank. Dominant individuals displace subordinates from preferred feeding trees (Di Bitetti & Janson, 2001b), and this ability to monopolise natural foods may mean that dominant individuals have less of an incentive to interact with tourists for food than subordinates do.

The number of times individual monkeys directly interacted with tourists ranged from zero to 29 (appendix II). Some individuals that frequently interacted with tourists altered their behavioural patterns when many tourists were present. Behaviours that were frequently

22 observed in response to high tourist presence included: heightened vigilance, squeal vocalisations, self-scratching, grinning and eyebrow-raising. Scratching is used as a behavioural measure of stress in primates (Troisi et al., 1991) while the squeal vocalisation and grinning indicate submissiveness (Di Bitetti, 2001b). While I lack the focal data to compare to rates of these behaviours during interactions to baseline rates, it was evident that these behaviours occurred at a heightened frequency among certain subadult and juvenile males during tourist interactions. Interactions in which monkeys expected, but did not receive food may have contributed to heightened stress levels and resulted in the expression of these behaviours.

Fig. 11. Juvenile male Astor grinning and squealing

Three individuals were never seen directly interacting with tourists. One of these was SRP, an adult male that frequently travels on the periphery of the group, sometimes leaving the group for a number of days. That he was never observed in any direct or indirect interactions suggests that he avoided tourist areas, while his peripheral position in the group possibly contributed to his absence from interaction data. The two other individuals that were never involved in direct interactions were SOL, a subadult female and her two year-old juvenile son, EBN. EBN was the only juvenile that did not participate in direct interactions, which suggests that interaction behaviour among young juveniles could be subject to maternal influence.

The foraging tactics of juvenile male capuchins are subject to a greater degree of social influence than those of females (Agostini & Visalbergi, 2005). As foraging strategies in capuchins are influenced by social learning (Fragaszy & Perry, 2003), it is likely that social influence plays a role in the probability that a monkey will participate in tourist interactions. Juvenile males that

23 associate more often with subadults might be expected to have higher levels of interactions than more socially peripheral juveniles. This possibility could be explored using social network analysis to investigate whether individuals that participate in more interactions show high levels of affiliative behaviour, measured through proximity and grooming matrices (Tiddi et al., 2011).

‘Traditions’ in animal species can be defined as long-lasting behavioural patterns shared by group members in part via social learning (Fragaszy & Perry, 2003). Traditions exist in capuchins as social behaviours and foraging techniques that are distinct to particular groups (Boinski et al., 2003). As the occurrence of tourist interactions and hotel incursions has increased in recent years, a tradition of tourist interaction may become established in the Macuco group.

Dominant individuals may exert a strong influence over other group members behaviours through social learning. In experimental conditions, the foraging technique of a dominant male capuchin was the same technique primarily adopted by all other group members in a foraging task (Dindo et al., 2009).While the dominant male of the Macuco group, ERN, interacted less than all subadult males, he participated in more direct interactions than any adult female. ERN was still a subadult when he became the dominant male, and his takeover coincided with the group split that altered the Macuco group’s ranging patterns (Scarry, 2013). If ERN interacted with tourists as a subadult dominant male, this may have facilitated the spread of this behaviour through the group.

4.3 Ranging Results 4.3.1 Home and Core Range

The Macuco group’s use of their home range has changed in the period from 2010 to 2013. The group now appears to have begun to exploit areas to the west of the southern end of their historic range, and has abandoned a large section of the northern part of their historic range (Fig. 5a). The tourist area is now more often and more widely visited than in 2010. While the total home range differed little in size over the two years, the core area used by the monkeys shrank, from 40.9ha in 2010 to 26.9 ha in 2013. The monkeys used a smaller area more intensively than previously. None of the core area falls within the main tourist area, though a portion is beside the hotel, where the monkeys have a sleeping site (see section 4.5).

These ranging results should be approached with caution due to the relatively short amount of time that ranging data were collected for. It is likely that the number of location fixes collected

24 during this study underestimates the true extent of the home range. In a study where ranging data were collected over a two-year period (2008-2010), the Macuco group had a total home range of 179.6ha (Scarry & Tujuage, 2012), which is larger than the range estimated during this study (104ha in 2010, 99ha in 2013).

As the ranging patterns of capuchins are subject to a high degree of seasonal influence (Di Bitetti, 2001a), the size and intensity of use of the home range would likely change if data were collected over a longer period. By comparing the range over the same period in the different years, I should have an accurate estimate of the relative intensity of use of the areas during the winter months.

Much of the northern part of the group’s range from 2010 is now used by another group, the Spot group, which was formed as a result of the Macuco group’s fission in early 2010 (Scarry & Tujague, 2012). Both groups use much of the same area, with the Spot group regularly visiting the core range of the Macuco group. The Spot group now appears to maintain exclusive access to much of the Macuco group’s former range. This has possibly increased the Macuco group’s reliance on the tourist area, though the degree to which tourist foods have influenced this shift of range remains unclear.

The Macuco group used the tourist area significantly more frequently and more intensively in 2013 than in 2010. The benefit to group members of interacting with tourists shows high inter- individual variation. Naturally occurring foods within the tourist area may be the most important factor in attracting the group to these areas, while non-natural foods had stronger influence on the behaviour of certain individuals, particularly subadult males. As data on tourist interactions were not systematically collected during 2010, the frequency of interactions cannot be directly compared between the two study periods. However, field notes from 2010 indicate that monkeys accessed the hotel and interacted with tourists on relatively few occasions.

4.3.2 Seasonal Influence – Fruit Availability

The ranging patterns of the monkeys are subject to a number of influences, with fruit availability being the most important factor in determining where the monkeys travel (Di Bitetti, 2001a). Exotic species such as Citrus spp. and Hovenia dulcis occur in greater densities around the tourist area than in other parts of the group’s range (Hirsch, 2009). Therefore the group visited the tourist area more often when these species were in fruit (May- June), which in turn led to a higher number of tourist interactions during these months than during July.

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During much of July, the monkeys fed on fruiting cupai trees (Copaifera langsdorffii ). These trees were mainly concentrated near the centre of the group’s core range, north of the tourist area. The period that the monkeys fed most often on cupai coincided with the period when the tourist area was visited least. It is interesting to note that despite there being a number of these trees situated in the centre of the group’s range, the monkeys had not previously been observed feeding on cupai trees in over a decade of prolonged study (Di Bitetti, 2001b; Baldovino personal comment).

While the majority of the group did not visit the tourist area for several days during July 2013, some monkeys sometimes still interacted with tourists at the hotel during this time. These events occurred when an individual or subgroup left the main group and travelled to the hotel. That the group did not visit the tourist area when high levels of fruit were available in other areas indicates that fruit availability has a stronger effect on group ranging than tourist food, though human foods may be a strong enough attractant for individuals or subgroups to leave the group, even when lots of natural foods are available.

4.3.3 Influence of Platforms

Another factor that influences the ranging patterns of the group during the study period is the use of feeding platforms for provisioning experiments. Feeding platforms have been shown to exert a strong influence on the activity and ranging of capuchins at Iguazú (Janson, 1996; 1998; Di Bitetti, 2001a). The Macuco group was subject to feeding platforms in both 2010 and 2013 (appendix V). In 2010, some platforms were situated in the northern part of the group’s range, while in 2013 the platforms were situated further south. As the core area in both years includes all feeding platforms used in each, it is apparent that these platforms exert a strong influence on where the group ranges. Consequently, the intensity of use of the core area is as least partly determined by the position of these platforms.

In 2010, more platforms were used, and more food was provided than in 2013 (Wheeler & Hammerschmidt, 2013). The group visited platforms less consistently in 2013, and is likely that the ranging patterns in 2010 were more heavily influenced by the platforms than in 2013. Platforms are never situated within 500m of the tourist area or the hotel, and it is likely that the use of platforms reduced the amount of use of tourist areas by the group, by providing an alternative incentive to use other parts of their range. Gathering data in seasons when provisioning experiments are not taking place would provide additional insight into how often the group would visit tourist areas in the absence of feeding platforms.

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4.3.4 Sleeping Site Choice

The group’s sleeping patterns differed considerably across the study periods in 2010 and 2013. The most frequently used site in 2013 was in close proximity to the hotel, and accounted for 36.2% of all sleeping sites used in 2013, while the most commonly used site in 2010 accounted for 19% of sites. The monkeys slept in the same area on consecutive nights more frequently in 2013 (20.68% of nights, 12 times) than in 2010 (3.85% of nights, twice). In 2013, they slept next to the hotel on consecutive nights six times, and used another site in the centre of their core range six times.

The changes in the monkeys’ sleeping patterns over the two study periods reflect the differences in their ranging habits. The two most frequently used sites in 2010 were in the northern part of the group’s territory, which they no longer use. The group used a smaller core area of activity during this study more intensely than in 2010. Consequently, their sleeping site choice is concentrated in and around this core area, and the group frequently returns and reuses the same site on consecutive nights.

Group members occasionally sleep on the hotel roof, possibly because of warm air from heating vents. This strategy has also been observed in Chacma baboons (Papio ursinus) in South Africa, that choose roofs as sleeping sites, because they provide both comfort and easy access to human food sources (Hoffmann & O’Riain, 2012). Proximity to food sources is one of the factors that influences primates’ choice of sleeping site (Anderson, 1998). Most interactions that occur at the hotel take place in the morning and the evening, with monkeys frequently approaching the hotel shortly after waking and before sleeping.

Whether the monkeys often slept near the hotel as a result of group members choosing to approach the hotel, or individuals approached the hotel because the group happened to be sleeping in the area, is not clear from these data. However as monkeys sometimes chose to sleep on the hotel building, it appears that the hotel is exerting some influence on the sleeping patterns of the group.

4.3.5 Location of Interactions

More group-level interactions took place at the hotel than at any other site. The nature of interactions at the hotel was often different to interactions at other areas. All interactions at the hotel were considered direct interactions, as accessing the hotel necessitated deliberate movements

27 away from the forest and onto the building. By contrast, interactions at other locations could occur when monkeys foraged on natural foods, and did not necessarily require deliberate interactions by monkeys. Having gained access to the hotel building, monkeys could traverse balconies and enter rooms when no people were present, while all interactions in other areas did involve people. As skilled object manipulators (Fragaszy et al., 2004), capuchins’ ability to open doors and windows increases their aptitude for hotel raids.

The amount of food the monkeys received at the hotel was greater than at all other sites, with food obtained in 50.9% of group-level interactions at the hotel. Food was given by guests, taken from balconies or obtained after monkeys entered rooms. As monkeys went out of view of observers when they entered rooms, it is likely that they received food at the hotel more often than was recorded. As the area with the highest number of interactions and the highest probability of obtaining food, the hotel seems to have a greater influence on the monkeys’ activity than interactions in other areas.

Fig.12 Subadult Male Sergio on Hotel Balcony – Photo by Paula Tujague

Away from the hotel, interactions were concentrated around two cafés, a train station, and various tourist trails. Both cafés have tables situated outside, in proximity to the forest edge. Interactions at cafes in occurred most commonly during the middle of the day, when tourist numbers were particularly high in these areas, (e.g. 75%of interactions at Fortin café occurred between 11.00 -15.00). Whether this arose as result of the group deliberately timing cafe

28 visits to coincide with meal times, or the high frequency of interactions was due to more tourists being present at these times is unclear. Yellow baboons (Papio cynocephalus) and vervet monkeys in Kenya that visited hotels were reported to concentrate raiding activities around meal times (Else, 1991).

4.3.6 Human Foods Consumed

The most commonly consumed human foods were bread, biscuits, potato chips and fruit. Capuchins have a destructive foraging strategy that involves high levels of food processing, and enables them to consume difficult to access foods such as hard-shelled nuts and well protected invertebrates (Janson & Boinski, 1992). These foraging traits may aid capuchins in accessing human foods that are protected in some way, such as packaged or canned drinks.

Figs 13a + 13b. Subadult male Tito with sandwich and juvenile male Maverick with potato chips

Photos by Brandon Wheeler and Paula Tujague

The non-natural foods that the monkeys consume contain high levels of sugar, salt and other additives not found in wild foods. If monkeys consume these foods over a prolonged period, and these foods make up a substantial part of their diet, they could suffer from diet-related health problems. Obesity is reportedly a problem among long-tailed macaques that are provisioned at a tourist site in Bali (Lane et al., 2010), while capuchins are also susceptible to diabetes (Kuhar et al., 2009). Foraging on discarded foods could also expose capuchins to infection risk. Humans and primates are susceptible to many of the same species of gastrointestinal parasites, with examples being Giardia, Ascaris and Strongyloides (Chapman et al., 2005).

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4.4 Group Fission 4.4.1 Subgroups

The level of fission-fusion dynamics among primate groups occurs along a continuum, from highly cohesive to obligatory fission-fusion societies (Aureli et al., 2008). Along this continuum, differences may be found within species and within groups. Black capuchins in Brazil regularly form temporary subgroups, with smaller subgroups tending to contain less dominant individuals (Lynch- Alfaro, 2007). Males had a higher rate of foraging success in smaller subgroups, though subgroup composition did not alter the foraging success of females (Lynch-Alfaro, 2007). The temporal and spatial distribution of food sources may influence subgroup composition, with anthropogenic food sources potentially influencing the composition of subgroups (Hockings et al., 2012).

Capuchin groups at Iguazú are usually cohesive, but may divide into temporary subgroups for hours or days (Di Bitetti, 2001). The Macuco group frequently formed subgroups during the study period, and subgrouping tends to occur more often during the winter (Di Bitetti, 2001). Subgroups were sometimes encountered at tourist areas or the hotel, while the majority of the group travelled in other areas. Monkeys often left the main part of the group and accessed the hotel, or were separated from the main group as result of staying on the hotel. These subgroups tended to be comprised mainly of subadult males, the age/sex class that participated in the highest number of tourist interactions.

Another factor that may encourage the group to temporarily fission is the female estrous cycle. Subgroups formed more often when one or more females were in estrous. Males sometimes separated from the group with an estrous female, possibly to reduce sexual interference from other males. These pairs or subgroups were found in tourist areas and at the hotel on a number of occasions. Fission-fusion allows group members to avoid majority decisions that are not in their favour (Aureli et al., 2008). Food received at the hotel seems to be a stimulus that encourages the Macuco group to temporarily fission.

4.4.1 – Dispersal

Single individuals, usually subadult males, sometimes separated from the group and were found alone at the hotel, or in other tourist areas. Some of these males are at the age when capuchins usually disperse from the natal group (mean 6.5 years, Janson et al., 2012). Capuchins

30 usually disperse further than one group away, though little is known about the fates of dispersing males (Janson et al., 2012). Dispersal is a highly risky time for male primates, as they may encounter hostility in joining new groups, lack knowledge about food resources in new areas, and be subject to increased predation risk as a result of travelling alone (Boinski et al, 2005; Janmaat et al, 2009).

Easily accessible human foods may offer young males a less risky alternative to dispersal. Provisioning has decreased the rate of dispersal among long-tailed macaques in Bali (Lane et al., 2010), and a similar situation could arise at Iguazú. Indeed, this scenario is not without precedent. In 2006 a subadult male dispersed from the Macuco group, but rather than join a new group, he spent most of his time in the tourist area eating provisioned food (Wheeler, personal communication). There is a danger that a similar situation could arise again.

4.5 Aggression There are numerous examples of primates becoming aggressive towards tourists at sites where provisioning occurs (Lee et al., 1986; Fuentes et al., 2007; Zhao & Deng, 1992). The capuchins at Iguazú do not engage in overtly aggressive behavior with tourists yet, though monkeys occasionally threatened tourists. If the frequency of interactions with tourists continues to increase, it is likely that monkeys will become more forceful in their attempts to obtain food.

While food transfer from tourists to monkeys was usually voluntary on behalf of the tourists, monkeys sometimes ‘stole’ food from people’s hands or from tables. This level of boldness suggests that there is a real possibility that monkeys will become ever more aggressive towards people, possibly resulting in biting. One of the dangers that this situation presents is disease transfer, particularly as primates are the third most common vector of rabies in South America (Machado et al., 2012). Between 1991 and 1998, eight human deaths from rabies in the Brazilian state of Ceará were transmitted from marmosets (Callithrix jacchus) (Favoretto et al., 2001), while also in Brazil free ranging black capuchins tested positive for rabies antibodies, but showed no clinical signs of disease (Machado et al., 2012).

Tourist provisioning commonly results in heightened levels of aggression within primate groups through increased competition for clumped resources (Berman et al., 2007; Fuentes & Gamerl, 2005). During this study, competition for human foods caused aggressive interactions on several occasions. These were usually mild cases of aggression, e.g. brief chases or threatening vocalisations, and did not involve physical contact. However, in one case an adult female bit a juvenile female, resulting in a a severe laceration. The victim was observed not using the leg for a

31 number of days after the injury. This is the type of aggressive interaction that could impact greatly on group stability or individual fitness.

Monkeys competed with coatis for human food on nine occasions during the study. Coatis at the site are currently even more forceful than monkeys in obtaining human foods, and often succeed in taking food from backpacks, tables and people’s hands. Monkeys typically come to the ground to chase and compete with coatis for the food. Both species are armed with powerful canines, and there is a risk of serious injury as a result of this competition.

4.6 Interference of Researchers The interference of researchers had an effect on the nature of monkey-tourist interactions. Researchers intervened in 26% of all group-level interactions, resulting in reduced opportunities for monkeys to obtain food. Even when researchers did not directly intervene in interactions, their very presence may have influenced the behaviour of tourists towards monkeys. Additionally, the presence of researchers may have had a deterrent effect on whether or not monkeys chose to involve themselves in interactions.

Interference generally took the form of researchers blocking the monkeys’ path from the forest edge to the hotel, and attempting to scare monkeys using clapping, shouting, and whistles and water pistols. Monkeys occasionally responded with facial threats, or with submissive gestures and vocalisations (appendix I). They became rapidly accustomed to researcher intervention, and avoided or dodged researchers, showing great persistence in trying to gain access to the hotel and cafés.

While the number of contact interactions and amount of food obtained was considerably reduced by researchers, the fact that monkeys persisted in accessing the hotel, and received human food on 55 occasions during the study period, illustrates how difficult it will be to try and reduce tourist monkey interactions. During the approximately 8 months of the year when researchers are not following the group, they will obtain human food more regularly and easily. Researcher intervention may be futile in trying to alter these behaviours.

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4.7 Mitigation Efforts Some steps have been taken to try and reduce the amount of contact between visitors and animals at the park. Bins have been fitted with latches that prevent animal access, and there are signs that advise visitors against the dangers of feeding wildlife (Figs. 13a + 13b). During the high tourist season in 2011 an education campaign was implemented to discourage visitors from feeding wildlife. Tourist guides are particularly important in influencing the behaviour of visitors (Grossberg et al., 2003), and in 2013 an education seminar for guides took place.

Figs.14a + 14b. Signs warning against feeding animals

The selective removal of trees that monkeys use to access tourist areas is another tactic that has been used. In 2011, trees between a café and the forest edge were removed, and visits to the café subsequently decreased. While this strategy was temporarily successful in reducing visits to the café, the monkeys adapted their own strategies, and began to cross to the café along the ground.

During the winter the group consumes large quantities of fruit from exotic species such as Hovenia dulcis and Citrus spp., (Brown & Zunino, 1990). There are plans to remove all introduced species from the area (UNESCO, 2012), which if implemented could increase monkeys’ reliance on

33 non-natural foods and increase interaction numbers. However the removal of these exotics could also serve to push the group’s ranging patterns away from the tourist area, as exotics are more heavily concentrated near the falls than in other parts of the park (Hirsch, 2009).

34

Chapter Five – Conclusions and Recommendations

5.1 Conclusions The Macuco group has shifted their home range to the south and west of their former extent. The group now uses a smaller area more intensively than it previously did, and the tourist area is now more frequently visited than in 2010. The group interacts frequently with tourists, and tourist interactions are unequally distributed among group members. Subadult males interact with tourists more than other age/sex classes. Individuals in the group vary widely in their propensity to interact with tourists. Most interactions in which the monkeys receive food occur at the hotel, and the hotel exerts a greater influence on the ranging patterns of the group than other tourist areas do.

The interactions between monkeys and tourists, particularly those at the hotel, may be affecting patterns of subgroup formation in the Macuco monkeys. The group’s choice of sleeping sites may also be influenced by food available at the hotel. If these patterns persist, it is likely that the numbers of tourist-monkey interactions will increase, particularly as juvenile males in the group grow into subadults. This raises the possibility that monkeys will become physically aggressive towards people, with the risk of injuries for visitors. The consumption of human foods could also have a negative effect on the health of the monkeys.

35

5.2 Recommendations Visitors to the park should receive educational material to discourage them from interacting with and feeding animals. This could take the form of a brochure that is handed out with park tickets.

Park guards should patrol the outside feeding areas at the cafes, particularly at lunch time, in order to prevent interactions between tourists and monkeys.

Fines should be imposed on visitors and guides that break park rules by feeding wildlife.

Park authorities and the hotel management should work to reduce the availability of foods at the hotel. Doors and windows to rooms should be locked in order to prevent monkeys from accessing hotel rooms from balconies.

Food in hotel rooms should be stored in containers that prevent monkeys from easily accessing food in hotel rooms.

A mechanism to prevent monkeys from climbing onto the hotel should be developed. This could take the form of a curved barrier that blocks access to the roof and balconies, or a low voltage electric wire.

36

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Appendix I

Ethogram of capuchin monkey behaviours and vocalisations in to be recorded during tourist interactions, adapted from Dr. Tiddi’s protocol and Di Bitetti (2001b).

Behaviour Definition Scratching Scratching a part of its own body Urine washing Urinating on hands and rubbing it on feet-palm and/or tip of tail Body shaking Shaking rapidly its own body Approach Moving towards tourists to within 3m Monitor Looking at tourists and continuously focusing the gaze on tourists for >10 seconds Threat Opening the mouth wide so that the canines are visible, lays the ears back, and stares at recipient (=open mouth, bared teeth), while sometimes slapping the ground/branch and curving the tail over the back Eyebrow raising Eyebrows are raised up and backwards, and the fur over the crown is flattened. Grin The monkey has a grin on its face: the corners of the mouth are rhythmically drawn backwards with closed jaws, sometimes baring some teeth. Eyebrows may be raised.

Submission/Scream Long, high-pitched call that can be staccato or undulated Squeal A high-pitched oscillating vocalisation, similar to scream but with less intense Food call A series of pure tone syllables that sound like whistles Alarm call A hiccup-like vocalisation

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Appendix II

List of Individual Monkeys and Interaction Numbers

Age Individual Sex Class Born Indirect Direct Total ERN M Ad 2002 17 9 26 SRP M Ad 2002 0 0 0 THE F Ad 1992 18 5 23 EST F Ad 2000 11 4 15 YOL F Ad 1993 7 2 9 SRG M S-Ad 2005 15 25 40 TIT M S-Ad 2005 9 18 27 EDU M S-Ad 2006 17 22 39 MAG M S-Ad 2006 23 19 42 DAL M S-Ad 2007 19 29 48 ING F S-Ad 2005 13 9 22 SOL F S-Ad 2005 3 0 3 MAW F S-Ad 2005 14 9 23 OFE F S-Ad 2006 5 17 22 COR F Juv 2008 16 8 24 MAV M Juv 2008 5 14 19 RIK M Juv 2008 5 9 14 FEN M Juv 2009 2 7 9 OMA M Juv 2011 6 8 14 AST M Juv 2011 12 21 33 EBN M Juv 2011 2 0 2 LEN M Juv 2012 6 7 13 ZIS M Juv 2012 1 3 4 Total 226 245 471

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Mean interactions per age/sex class

Age/Sex Class Indirect Direct Total Juv M Mean 4.50 9.25 13.75 N 8 8 8 SD 3.93 6.45 9.95 SE 1.39 2.28 3.52 S-ad M Mean 17.40 20.40 40.00 N 5 5 5 SD 5.50 3.85 6.96 SE 2.46 1.72 3.11 Ad M Mean 7.00 7.00 14.00 N 2 2 2 SD 9.90 9.90 19.80 SE 7.00 7.00 14.00 Juv F Mean 16.00 8.00 24.00 N 1 1 1 SD . . . SE . . . S-ad F Mean 9.25 8.25 17.50 N 4 4 4 SD 4.79 5.91 9.68 SE 2.39 2.95 4.84 Ad F Mean 10.33 5.33 15.67 N 3 3 3 SD 5.13 2.08 7.02 SE 2.96 1.20 4.06 Total Mean 9.61 10.74 20.83 N 23 23 23 SD 6.80 7.37 13.69 SE 1.42 1.54 2.86

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Appendix III List and Map of Sleeping Site Locations

Sleeping site locations in 2010 and 2013

Site/Area 2010 2013 Hotel area 6 21 Basales 8 14 COC 5 7 Apepu 10 0 R13 Paralela 9 0 Boq 400 5 3 Boq 100 0 5 Quilmes 5 0 BN Grappa 1 2 R15 3 0 Dos Hermans 0 2 M13 C4S 0 1 Send Verde 0 1 Therm Ma 0 1 Anchico 0 1

46

Sleeping site locations in 2010 and 2013

47

Appendix IV Map with Platforms and Core Areas

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Appendix V

Ethics Clearance Form

Faculty Ethics form HSS.E2 Faculty of Humanities and Social Sciences

Application for ethics approval for a research project involving human participants

Undergraduates and Foundation Degree Students: Before completing this form, the ethics review checklist (school form HSS.E1) should have been completed to establish whether this additional application for ethics approval is required. If ethics approval is required, you should complete this form, sign it and submit it to the Faculty Research Ethics Officer, Maggie Wilson at [email protected]. A decision form, E3 will then be returned to you by e-mail.

Master’s Students: You should complete this form before you start your project and submit it to your supervisor. If he or she is unable to sign it at this stage, the form will be referred to the Faculty Research Ethics Officer, as above, who may seek further information and clarification from you. A decision form, E3, will then be returned to you by e-mail.

All students should refer to the University Code of Practice on Ethical Standards for Research involving Human Participants, available at www.brookes.ac.uk/res/ethics and Faculty guidelines, which are included in the relevant on-line module or course handbook. You should bind a copy of the approved form in your final project or dissertation submission.

1. Name of Principal Investigator Martin Fahy (Student):

E-mail address: [email protected]

2. Name of Supervisor and e-mail Dr. Catherine Hill address:

E-mail address: [email protected]

3. Working Project Title: Tourist-Monkey interactions at Iguazú National Park, Argentina.

4. Project Type (please specify course Master’s MSc in Primate and give module number): project Conservation P20107 Master’s dissertation

Undergraduate project:

Undergraduate dissertation:

Foundation degree project:

49

5. Background and rationale of The research will investigate the nature proposed research: and frequency of interactions between capuchin monkeys (Sapajus nigritus) and tourists at Iguazú National Park. These interactions have become a source of concern to park authorities and researchers at the site, and pose potential dangers to the safety of both monkeys and visitors. The goal of the research is to provide suggest possible management strategies in order to minimise the severity and potential negative impact of these interactions.

6. Methods of data collection: Data collection will involve following the monkey group and making behavioural observations on (Please attach a copy of your draft the monkeys. The monkey group is well questionnaire, interview schedule or habituated to human observers, and data observation guidelines) collection will be carried out in conjunction with several other behavioural studies on the monkeys. The research will examine the ratio of monkey:human initiated interactions; classify the types of foods consumed by monkeys during tourist encounters; collect ranging behaviour on the monkey group; and classify tourists by age/sex profiles. The monkeys’ behaviour will be the focus of the study, rather than the tourists.

7. Participants involved in the research: Other behavioural researchers and field assistants will be involved in data collection. Including source and method of recruitment)

8. Potential benefits of the proposed The research should contribute to the body of research: knowledge on primate-tourist interactions, and will propose management strategies to decrease the levels of interactions between monkeys and tourists at the site.

9. Potential adverse effects of the The study will carried out as part of routine, proposed research and steps to be ongoing behavioural observation of the monkey taken to deal with them: group, and should not induce any psychological stress in the animals or tourists. (These could include possible psychological stress or anxiety)

10. Plan for obtaining informed consent: N/A

(Please attach copy of information sheet and consent form)

Note; consent forms are not needed for questionnaires

11. Steps to be taken to ensure No data on the identities of any humans involved confidentiality of data: in interactions will be recorded.

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(Please outline steps to be taken to ensure confidentiality, privacy and anonymity of data during collection, storage and publication of data)

All materials submitted will be treated confidentially.

I have read and understood the University’s Code of Practice on Ethical Standards for Research involving Human Participants

Signed: Principal Investigator Martin Fahy /Student

Signed: Supervisor

Date:

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