RESPIRATORY DISEASE IN THE NORTH AMERICAN CAPTIVE ORANGUTAN POPULATION ______
A Thesis
Presented to the
Faculty of
California State University, Fullerton ______
In Partial Fulfillment
of the Requirements for the Degree
Master of Arts
in
Evolutionary Anthropology ______
By
Megan Kathryn Fox
Thesis Committee Approval:
Sara E. Johnson, Chair John Bock, Department of Evolutionary Anthropology John Patton, Department of Evolutionary Anthropology
Fall, 2017
ABSTRACT
All species within the genus Pongo are Critically Endangered; the Bornean orangutan (Pongo pymaeus), the Sumatran orangutan (Pongo abelli), and the recently classified species from Batang Toru (Pongo tapanuliensis). The North American
Orangutan Species Survival Plan (SSP) and zoological institutions that house orangutans work to educate the public regarding the threats these species face and support various conservation and research projects that are working to promote their survival into the future. Unfortunately, there are a number of health challenges that face the captive orangutan population. Respiratory disease is the leading cause of death in North
American captive orangutans between the ages of 8-40 years. Conditions under which respiratory disease occur are not well understood. This project aims to identify factors that influence the presence of respiratory disease in the North American captive orangutan population. A survey was disseminated to accredited North American zoological institutions housing orangutans to determine overall prevalence of disease, species and sex differences, as well as intrinsic and extrinsic environmental risk factors.
Results show that respiratory disease affects 20.78% of this study population (n = 154) and male orangutans are nearly 2.4 times more likely to have respiratory disease than females. No significance is found at the species level for presence or absence of respiratory disease. Symptoms associated with diagnosis of disease are compiled with the goal of increasing early detection and treatment.
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TABLE OF CONTENTS
ABSTRACT ...... ii
LIST OF TABLES ...... vii
LIST OF FIGURES ...... x
ACKNOWLEDGMENTS ...... xiii
Chapter 1. STUDY OVERVEW ...... 1
Overview of Respiratory Disease in Captive Orangutans ...... 1 Overview of Chapters ...... 4
2. ORANGUTAN OVERVIEW ...... 7
Orangutans Past and Present ...... 7 History of Past Populations ...... 7 Current Populations ...... 8 Orangutans in the Wild ...... 12 Wild Orangutan Overview ...... 12 Female Philopatry and Male Dispersal ...... 14 Orangutan Sociality ...... 15 Social Organization ...... 15 Variation between Bornean and Sumatran Populations and Age/Sex Classes ...... 17
3. FEMALE ORANGUTANS ...... 20
Female Behavior ...... 20 Female Social Behavior ...... 20 Female Philopatry and Relatedness ...... 21 Female Ranging Patterns and Home Ranges ...... 21 Female Reproduction ...... 23 Female Associations during Fecundity, Mating Preferences, and Female Choice ...... 23 Female Reproductive Parameters ...... 25
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Concealed Ovulation, Age of First Parturition, Interbirth Intervals, and Signs of Pregnancy ...... 25 Mother-Infant Relationships and Parental Investment ...... 26 Male Avoidance and Infanticide ...... 27
4. MALE ORANGUTANS...... 32
Male Behavior...... 32 Bimaturism and Behavior ...... 32 Flanged Males and Unflanged Males ...... 32 Male Bimaturism and Development ...... 34 Male Secondary Sexual Characteristics ...... 34 Male Reproductive Tactics ...... 36 Forced Copulations, Copulatory Behavior, and Reproductive Success ...... 36 Male Dispersal and Vocalizations ...... 39 Dispersal and Ranging Patterns ...... 39 Vocalizations ...... 39
5. ORANGUTAN ECOLOGY ...... 41
Introduction to Orangutan Ecology ...... 41 Influence of Environment on Orangutan Behavior and Sociality ...... 42 Geographic Variations between Populations ...... 44 Species and Sub-Species ...... 44 Variation in Environment and Food Availability ...... 44 Variation in Morphology ...... 45 Variation in Life-Histories ...... 46 Variation in Sociality ...... 46 Culture and Social Learning ...... 47 Orangutan Culture ...... 47 Social Learning ...... 48 Vocalizations and Communication ...... 50 Gestures ...... 50 Orangutan Vocalizations ...... 51 Long Calls ...... 52
6. ORANGUTAN CONSERVATION ...... 55
Conservation Overview ...... 55 Influences on Conservation ...... 57 Orangutans and Geographic Variation ...... 57 Logging and Orangutans ...... 57 Illegal Hunting ...... 60 Palm Oil and Oil-Palm Plantations ...... 61 Vulnerability of Female Orangutans ...... 62 Conservation Efforts ...... 62
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7. ORANGUTANS IN CAPTIVE ENVIRONMENTS IN-SITU AND EX-SITU . 64
Rehabilitant Orangutans/Numbers ...... 64 The Association of Zoos and Aquariums (AZA)...... 65 The Orangutan Species Survival Plan (SSP) ...... 67 Captive Orangutans and Management ...... 68
8. ORANGUTANS AND RESPIRATORY DISEASE ...... 71
Orangutans and Air Sacculitis ...... 71 Project Significance, Objectives, and Preliminary Research ...... 73 Significance of Project ...... 73 Project Objectives ...... 73 Preliminary Research ...... 74 Factors that Influence Respiratory Disease ...... 75 Predisposing Factors for Respiratory Disease ...... 75 Other Risk Factors/Obesity ...... 76
9. METHODS ...... 78
Institutional Animal Care and Use Committee (IACUC) Process/Approval ...... 78 Orangutan Species Survival Plan (SSP) Approval and Endorsement ...... 79 Development and Dissemination of Survey ...... 80 Data Management ...... 82 Studbook and Historical Data/Keyword Searches ...... 83
10. RESULTS ...... 85
Current North American Orangutan Population and Research Population ...... 85 Research Question, Hypotheses, and Predictions with Results ...... 88 Demographics and Body Size ...... 93 Hypothesis 1 ...... 94 Prediction 1 ...... 94 Hypothesis 2 ...... 102 Prediction 1 ...... 102 Hypothesis 3 ...... 106 Prediction 1 ...... 106 Environment ...... 111 Hypothesis 4 ...... 111 Prediction 1 ...... 111 Prediction 2 ...... 111 Hypothesis 5 ...... 112 Prediction 1 ...... 113 Prediction 2 ...... 113 Genetics ...... 118 Hypothesis 6 ...... 118
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Prediction 1 ...... 118 Physical and Behavioral Symptoms ...... 122 Additional Information from Survey Results ...... 126
11. DISCUSSION ...... 129
Significance of the Prevalence of Respiratory Disease in Multiple Populations of Captive Orangutans ...... 129 Similarities in the Prevalence of Respiratory Disease between the North American and European Captive Orangutan Population ...... 130 Previous Medical Assessment of the North American Captive Orangutan Population ...... 131 Prevalence in Rehabilitation Centers ...... 131 Prevalence of Types of Respiratory Disease ...... 132 Interpreting Results Regarding Demographics and Body Size ...... 132 Species, Ecology, Obesity, Respiratory Disease, and the Thrifty Genotype Hypothesis ...... 132 Wild Orangutan Weights ...... 135 Captive Orangutan Studies on Life-History Variations ...... 136 Prevalence of Respiratory Disease by Species between Studies ...... 136 Sex, Extreme Sexual Dimorphism, Respiratory Disease, and the Thrifty Phenotype Hypothesis ...... 137 Interpreting Results Regarding Environment ...... 139 A Captive Environment ...... 139 Environmental Factors as Possible Risk Factors for Respiratory Disease in the Current Study ...... 140 Interpreting Results Regarding Family History ...... 143 Most Commonly Reported Symptoms of Respiratory Disease ...... 145 Concluding Remarks...... 146 Future Work ...... 148
APPENDIX: LIST OF CONTRIBUTING INSTITUTIONS ...... 151
REFERENCES ...... 153
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LIST OF TABLES
Table Page
1. Demographics of the Current North American Orangutan Species Survival Plan Population ...... 86
2. Demographics of the Current Research Population ...... 86
3. Number of AZA Institutions Completing Surveys ...... 87
4. Orangutan Living or Deceased According to Species ...... 87
5. Orangutan Living or Decease According to Sex ...... 87
6. Presence or Absence of Respiratory Disease in the North American Captive Orangutan Population ...... 90
7. Diagnoses of Respiratory Disease and Types in the North American Captive Orangutan Population ...... 91
8. Frequency of Occurrence of Diagnosed Respiratory Disease and Types ...... 91
9. Presence or Absence of Respiratory Disease in Captive Orangutans by Species in the Study Population ...... 98
10. Respiratory Disease in Captive Orangutans by Species among the Affected Study Population ...... 98
11. Kaplan-Meier Case Processing Summary for Males ...... 99
12. Kaplan-Meier Overall Comparisons for Males ...... 99
13. Kaplan-Meier Case Processing Summary for Females ...... 101
14. Kaplan-Meier Overall Comparisons for Females ...... 101
15. Crosstabs Body Condition and Activity Level when Symptoms First Appeared 105
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16. Crosstabs Current Study Population, Current Body Condition, and Activity Level ...... 105
17. Crosstabs Current Body Condition and Species ...... 106
18. Crosstabs Current Activity Level and Species ...... 106
19. Presence or Absence of Respiratory Disease in Captive Orangutans by Sex in the Current Study Population ...... 108
20. Presence or Absence of Respiratory Disease in Captive Orangutans by Sex in the Affected Population ...... 109
21. Logistic Regression for Presence or Absence of Respiratory Disease by Species and Sex...... 109
22. Kaplan-Meier Case Processing Summary by Sex ...... 109
23. Kaplan-Meier Overall Comparisons by Sex ...... 109
24. Logistic Regression for Presence or Absence of Respiratory Disease, Number of Moves, and Rearing History ...... 112
25. Logistic Regression for Presence or Absence of Respiratory Disease and Place of Birth ...... 114
26. Logistic Regression for Presence of Respiratory Disease, Indoor and Outdoor Access, and Shifted Before Cleaning ...... 114
27. Logistic Regression for Presence of Respiratory Disease and how Many Months a Year the Individual is Kept Indoors ...... 115
28. Crosstabs Respiratory Disease and Indoor/Outdoor Access ...... 116
29. Crosstabs Respiratory Disease and Shifted for Cleaning ...... 117
30. Crosstabs Respiratory Disease and Months Indoors ...... 118
31. Logistic Regression for Presence or Absence of Respiratory Disease and Family History of Respiratory Disease ...... 119
32. Family History of Respiratory Disease in the Current Study Population ...... 120
33. Family History of Respiratory Disease and Presence or Absence of Respiratory Disease in Orangutans ...... 120
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34. Crosstabs Family History of Respiratory Disease ...... 120
35. Family Relationships and Respiratory Disease in the Current Study Population ...... 121
36. Family Relationships and Presence or Absence of Respiratory Disease in Orangutans ...... 122
37. Presence or Absence of Physical and Behavioral Symptoms ...... 123
38. Frequency of Physical and Behavioral Symptoms ...... 124
39. Severity of Physical and Behavioral Symptoms ...... 125
40. Age at Respiratory Diagnoses...... 127
41. Age of Sexual Maturity, Flange, and First Menses ...... 127
42. Family History of Respiratory Disease and Orangutans that Have or Had Air Sacculitis ...... 128
43. Logistic Regression for Presence or Absence of Respiratory Disease and Stress before Illness ...... 128
44. Was there Stress before Illness? ...... 128
45. Did this Individual Experience Stress before Illness? What Type of Stress? ...... 128
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LIST OF FIGURES
Figure Page
1. Current Distribution of Bornean Orangutans...... 11
2. Current Distribution of Sumatran Orangutans ...... 11
3. Current North American Orangutan SSP population by sex ...... 86
4. Current research population by sex ...... 86
5. Current North American Orangutan SSP population by species ...... 87
6. Current research population by species ...... 87
7. Percent of current research population living or deceased ...... 88
8. Presence or absence of respiratory disease ...... 90
9. Presence of respiratory disease ...... 91
10. Frequency of respiratory disease ...... 91
11. Presence of air sacculitis ...... 92
12. Frequency of air sacculitis ...... 92
13. Presence of rhinitis...... 92
14. Frequency of rhinitis ...... 92
15. Presence of pneumonia ...... 92
16. Frequency of pneumonia ...... 92
17. Presence of bronchitis ...... 92
18. Frequency of bronchitis ...... 92
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19. Presence of sinusitis ...... 93
20. Frequency of sinusitis ...... 93
21. Presence of other ...... 93
22. Frequency of other ...... 93
23. Cross sectional loess smooth of male and female orangutan body size for age by species, using current age in years and current weight in KG ...... 97
24. Cross sectional loess smooth of male orangutan body size for age by species, using current age in years and current weight in KG ...... 97
25. Cross sectional loess smooth of female orangutan body size for age by Species, using current age in years and current weight in KG ...... 98
26. Number of captive orangutans with or without respiratory disease by species ...... 99
27. Kaplan-Meier curves for survival functions of males by species, using age at first diagnosis and age in years for censored data ...... 100
28. Kaplan-Meier curves for hazard functions of males by species, using age at first diagnosis and age in years for censored data ...... 100
29. Kaplan-Meier curves for survival functions of females by species, using age at first diagnosis and age in years for censored data ...... 101
30. Kaplan-Meier curves for hazard functions of females by species, using age at first diagnosis and age in years for censored data ...... 102
31. Cross sectional loess smooth curves for male and female captive orangutans, using current age in years and current weight in KG...... 108
32. Kaplan-Meier curves for survival functions for male and female captive orangutans, using age at first diagnosis and age in years for censored data ...... 110
33. Kaplan-Meier curves for hazard functions for male and female captive orangutans, using age at first diagnosis and age in years for censored data ...... 110
34. Bar chart for orangutans with or without respiratory disease and number of moves ...... 112
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35. Bar chart for orangutans with or without respiratory disease and months kept indoors ...... 115
36. Bar chart for orangutans with or without respiratory disease and indoor/outdoor access ...... 116
37. Bar chart for orangutans with or without respiratory disease and shifted for cleaning ...... 117
38. Bar chart for orangutans with or without respiratory disease and family history of respiratory disease ...... 121
39. Bar chart for age of orangutans at first diagnosis of respiratory disease ...... 127
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ACKNOWLEDGMENTS
I would like to thank Dr. Sara E. Johnson for her continued support and assistance with this project, Dr. John Bock, Dr. John Patton, and Dr. Raffaella Commitante for their participation as part of my thesis committee, along with the other faculty at CSUF for their support. I would also like to thank Candace Sclimenti and the Los Angeles Zoo and
Botanical Gardens. This has been a project long supported and encouraged by both Dr.
Joe Smith and Dr. Nancy Lung, Orangutan SSP Veterinary Advisors, and by Lori Perkins and Carol Sodaro, along with the Orangutan SSP Steering Committee, all striving to improve the lives of orangutans. I would also like to thank all of the AZA institutions that contributed their time and information for this project, who are also all working towards the conservation and survivability of orangutans. I would also like to acknowledge Michael Jenkins and other family and friends for their love, assistance, and support. Dr. Roberto A. Delgado, Jr. and Dr. Graham L. Banes for their review and comments. To all who support orangutan well-being and conservation, your passion is an inspiration. To all of the orangutans who have been affected by respiratory disease, both directly and indirectly. And of course, to Minyak, the inspiration for my interest in this topic and my good friend, you will always be missed.
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CHAPTER 1
STUDY OVERVIEW
Overview of Respiratory Disease in Captive Orangutans
In a survey conducted by the Orangutan Species Survival Plan (SSP) in 2012, respiratory infections were ranked number one when institutions were asked to list the top three most serious health issues facing captive orangutans in North America.
Respiratory disease is the leading cause of death in North American captive orangutans between the ages of 8-40 years old (Orangutan SSP Health Survey, 2012). Because individuals in this range are of reproductive age, this can have a profound effect on the captive breeding population. Among these respiratory diseases, air sacculitis continues to be associated with significant levels of mortality and morbidity within this population
(McManamon, Swenson, Orkin, & Lowenstine, 1994). Air sacculitis is an infection of the laryngeal air sac (McManamon et al., 1994) and is also sometimes referred to as an air sac infection or throat sac infection. Air sacs are found in many primate species and are sac-like extensions of the larynx or parts of the vocal tract and vary in size and their configuration depending on species (Hewitt, MacLarnon, & Jones, 2002) but are most developed in great apes (Cambre, Wilson, Spraker, & Favara, 1980). Air sac infections appear to be more common among orangutans than other primate species (Cummins,
1985) and 42% of North American zoological institutions report having diagnosed air sacculitis within a ten-year period (Orangutan SSP Health Survey, 2012). Upper
2 respiratory disease has also been described as a significant cause of morbidity in the
European population of captive orangutans (Zimmermann et al., 2011) and among orangutans at rehabilitation centers (Lawson, Garriga, & Galdikas, 2006). Yet given the significance of respiratory disease in the North American and other populations, the cause or causes of respiratory disease and how disease develops is still not well understood (Zimmermann et al., 2011). Managing orangutans with respiratory disease can prove challenging and understanding the conditions under which these diseases occur is not well understood. There is a strong need to address the issues that surround the high prevalence of respiratory disease in the captive population of orangutans. Understanding what predisposing factors may influence the onset of respiratory disease is needed.
Previous studies on the prevalence and predisposing factors of upper disease in captive orangutans were conducted in zoos across Europe (Zimmermann et al., 2011).
The European study reported that Bornean orangutans (13.8%; n = 11) were more often affected by chronic respiratory signs than Sumatran orangutans (3.6%; n = 4) and that males (15.8%; n = 12) were more often affected than females (3.9%; n = 3) with chronic respiratory signs (Zimmermann et al., 2011). Zimmermann et al. (2011) report that air sacculitis was more common among hand-raised orangutans (21%; n = 21) than mother- reared orangutans (5%; n = 5) and that orangutans with respiratory disease were more often related to other orangutans with respiratory disease (93%; n = 14) than healthy orangutans (54%; n = 42) in their study population. Zimmermann et al. (2011) also investigated various environmental factors, none of which showed to have any statistical influence on the prevalence of respiratory disease. This project aims to identify some of
3 the factors that influence the presence of respiratory disease in the North American captive orangutan population.
Variations observed between the species of orangutans due to their ecological adaptations could potentially influence differences observed in respiratory disease at the species level. Bornean forests are recognized as being less productive than Sumatran forests (Marshall et al., 2009). Due to these ecological variations, Bornean orangutans consume more fallback foods (Taylor, 2009). Given the potential of Bornean orangutan’s ability at storing fat, the possibility of obesity affecting Bornean orangutans versus
Sumatran orangutans in captive environments is of interest. The “thrifty genotype hypothesis” posits that humans, particularly hunter-gatherers, have adapted to times of food scarcity by adapting the ability to better store fat in lean times, hence being advantageous in these environments (Neel, 1962). However, this adaptation becomes a disadvantage when food becomes more available across space and time, leading to issues with obesity (Neel, 1962). This thrifty gene could be cause for a higher prevalence of obesity in captive Bornean orangutans (van Schaik, Marshall, & Wich, 2009.), possibly affecting prevalence of disease in this population, including respiratory issues. This study not only investigates the prevalence of respiratory disease between these species, but also investigates body size as measured though body condition scores, activity level scores, and measured weights.
This study also investigates differences in the prevalence of disease between the sexes. The significant sexual dimorphism observed between flanged male and adult female orangutans is associated with male-male contest competition which is driven by the competition for fertile females (Utami Atmoko, Singleton, van Noordwijk, van
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Schaik, & Mitra Setia, 2009). This extreme sexual dimorphism is indicative of the strength of this male-male competition (Strier, 2017). An alternative male mating strategy among orangutans is also fueled by this male-male competition (Utami Atmoko et al., 2009). Flanged male orangutans also have other secondary sexual characteristics such as large canines, and they have large throat sacs that deliver their long-distance calls
(Strier, 2017). Given the variation in size that exists between flanged male and adult female orangutans, if increased body size does in fact influence the prevalence of respiratory disease then it would be expected that male orangutans would be affected more often than females.
This project also investigates intrinsic environmental factors that may influence the onset of disease including family history and stress level and extrinsic environmental factors including rearing history and housing conditions. Additionally, this project will provide information on the types of symptoms most commonly experienced that will also contribute to the possible early treatment and diagnoses of respiratory disease in captive orangutans. Because of the possible complications of air sac infections, such as pneumonia and sepsis, it is extremely important that orangutans are monitored closely for any signs of disease and be treated promptly (Lowenstine & Osborn, 2012). Identifying the risk factors involved will greatly enhance the ability of zoological institutions to act preemptively to treat disease and ultimately assist in the overall care, management, and survivability of the individuals involved and hence the population as a whole.
Overview of Chapters
It is important to first understand orangutans and their evolutionary history and current status, both in the wild and in captive environments. This paper provides an
5 overview of orangutans and their natural history that will assist in elucidating results of this research to provide a framework for how some of these results can be interpreted. In addition, it is also important to have an understanding of the real threats facing these species in the wild. Captive management continues to grow in importance because many species, including orangutans, face significant conservation threats. Zoological institutions continue to provide valuable assistance and knowledge to the conservation of many different species due to the growing number of conservation initiatives where animals need to be managed in environments such as rehabilitation centers.
The first chapter of this paper provides an overview of orangutan populations past and present, orangutans in the wild, and orangutan social behavior. The second chapter is specific to female orangutans and behavior, reproduction, and reproductive parameters.
Chapter 3 focuses specifically on male orangutans, their behavior, bimaturism, and development, reproductive tactics, male dispersal and vocalizations. These two chapters are important in understanding the sex differences that exist among orangutans, such as extreme sexual dimorphism (Utami Atmoko et al., 2009), as these differences are marked and could provide some insight into the difference in the prevalence of respiratory disease between males and females. In chapter 4 orangutan ecology is discussed in depth. Due to the geographic variations observed among orangutan populations (e.g. morphological, sociality, diet, inter-birth intervals, and life-histories) having an understanding of these differences is of importance when investigating potential variations in the prevalence of respiratory disease in the different species of orangutan.
Chapter 5 addresses the conservation issues that wild orangutans face. This chapter provides a necessary understanding of the significance issues these species face and helps
6 to gain an appreciation and perspective of why captive management is becoming even more critical. Chapter 6 focuses on the North American orangutan population and on the framework in which North American zoological institutions are based within the broader umbrella of the Association of Zoos and Aquariums (AZA). How these zoos work together in captive breeding and management programs is discussed. This chapter also discusses the role of rehabilitation centers in situ. Chapter 7 is an overview of respiratory disease in orangutans and the current project and describes the significance and the objectives of this project. This chapter also includes the hypotheses and predictions for the current study. Chapter 8 covers the methods of this project and chapter 9 discusses the results from this research. In conclusion, chapter 10 is the discussion of how the results of this research elucidate factors contributing to the development of respiratory disease in captive orangutans, how this information can be disseminated and utilized, and how future research can continue to assist in our continued pursuit to provide and care for the Critically Endangered genus Pongo.
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CHAPTER 2
ORANGUTAN OVERVIEW
Orangutans Past and Present
History of Past Populations
It appears orangutans first originated and became a distinct species approximately
2-3 million years ago on the mainland of Asia, along the Himalayan Range (Rijksen &
Meijaard, 1999). The orangutan was distributed throughout areas of the expansive
Sundaland plateau, near the Asian continent south of the Himalayas, up until the end of the Pleistocene (Rijksen & Meijaard, 1999). The orangutan diverged from a common ancestor 9-13 million years ago (Hobolth, Dutheil, Hawks, Schierup, & Mailund, 2011) with other estimates at 15-19 million years ago (Slattery, 2014). Estimates of hominid evolution overlap but do remain controversial and inconsistent between various methods used (Slattery, 2014). Recent findings have described the dispersal of males as being the key factor in gene flow within the genus Pongo (Nater et al., 2011; Nietlisbach et al.,
2012; van Noordwijk et al., 2012) and have also been able to describe factors involved in the current and historical distribution of the orangutan (Nater et al., 2014). Orangutans once inhabited regions far greater than where they are found today. Their range once incorporated areas in Burma, India, China, Vietnam, Java, Borneo, and Sumatra (Delgado
& van Schaik, 2000) and covered a distribution range of 1.5 million square kilometers
(Rijksen & Meijaard, 1999). The pattern of distribution of the orangutan is thought to
8 have been influenced by three factors; the courses of rivers and land forms, habitat and forest distribution, and human encroachment (Rijksen & Meijaard, 1999). It is suggested that the dramatic decline in population numbers and in the geographic distribution of the orangutan was in large part due to ecological factors and the strong impact of human colonization (Delgado & van Schaik, 2000). It is suggested that anthropogenic threats were equally responsible for the steep decline in orangutan populations and distribution patterns (Delgado & van Schaik, 2000). Extinction and significant loss of a historical range are in line with the “overkill hypothesis”, with orangutans being particularly vulnerable to anthropogenic threats due to their slow movement and life histories
(Delgado & van Schaik, 2000).
Current Populations
Today, orangutans are only found in fragmented populations in the northern region of Sumatra and throughout Borneo (Delgado & van Schaik, 2000), though they appear to be absent in the southeast of this island (Groves, 2001). Within the orangutan population, there are three distinct species, the Bornean orangutan (Pongo pygmaeus), the
Sumatran orangutan (Pongo abelii) (Groves, 2001), and the recently classified Batang
Toru population in Sumatra (Pongo tapanuliensis) (Nater et al., 2017). Bornean orangutans are described as being more robust than their Sumatran counterparts, with maroon hair, a more protruding jaw, a face that is figure-8 shaped, and with males displaying flanges that face-forward and also have extensive laryngeal air sacs (as reviewed in Groves, 2001). Sumatran orangutans are described as more gracile than
Bornean orangutans, with cinnamon-colored hair, adult males displaying an obvious beard and mustache, females also having a beard, their faces being more oval with a non-
9 protruding jaw, and adult males having flanges that are flat (Groves, 2001). Currently, there are three recognized subspecies of the Bornean orangutan; P. p. pygmaeus in western Borneo—considered the Northwest population, ranging north of the Kapuas
River and historically ranging northeast into Sarawak, P. p. wurmbii in southern
Borneo—considered the Southwest Kalimantan population, ranging to the south of the
Kapuas River and to the west of the Barito River, and P. p. morio in eastern Borneo— ranging from Sabah in Malaysia south to the Mahakam River in East Kalimantan
(Groves, 2001). Significant research continues to shed light on the taxonomic identification of these species and on their evolutionary history. This aids in understanding the geographical variation observed between populations of orangutans.
Sumatran orangutans are only found in the north of this island (Groves, 2001; Wich et al.,
2008). The Leuser Ecosystem is considered the stronghold of the Sumatran population, with 91% of all remaining orangutans living inside of its borders (Wich et al., 2008). The
Batang Toru population south of Lake Toba is considered the most significant Sumatran orangutan population existing outside of the Leuser Ecosystem (Wich et al., 2008). This population has been newly classified as a species of orangutan (Pongo tapanuliensis) with fewer than 800 individuals surviving today (Nater et al., 2017). The Batang Toru population is in the most southern range of the extant Sumatran species (Nater et al.,
2017; Wich et al., 2016). The currently recognized Bornean and Sumatran orangutan are estimated to have diverged approximately 674 kya but the Batang Toru population and
Sumatran orangutans north of Lake Toba split approximately 3.38 mya (Nater et al.,
2017).
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Currently both the Bornean and Sumatran orangutan are listed as critically endangered (IUCN Red List, 2016). Recent populations estimates have increased from approximately 54,000 individuals (Wich et al., 2008) to 104,700 individuals remaining for the Bornean population (Ancrenaz et al., 2016) and from 6,600 (Wich et al., 2008) to
14,613 individuals remaining for the Sumatran population (Wich et al., 2016). For
Bornean orangutans, an estimated 86% population decline between 1973-2025 due to anthropogenic factors, including illegal hunting and habitat loss, qualifies this species listing as Critically Endangered (Ancrenaz et al., 2016). For Sumatran orangutans, if the population continues to decline as it has since 1985 through 2060, there will be a total population decline of 80% over these three generations, qualifying the listing of this species as Critically Endangered (Singleton, Wich, Nowak, & Usher, 2016). The new population estimates not indicate an actual increase in the population, but is rather the result of more extensive research and population modeling (Wich et al., 2016). The
Sumatran orangutan population estimate increase is due to a few different factors and is based off of new transect survey research (Wich et al., 2016). First, there were populations that had not yet been surveyed because they fell outside known distributions at higher elevations where orangutans had not been expected to live (Wich et al., 2016).
In addition, orangutans were also found in higher numbers within logged forest than had previously been expected and another population of orangutans was discovered west of
Lake Toba that had never been assessed (Wich et al., 2016). For Bornean orangutans, the increased population estimate is due to more current field data with a revised map of their geographical distribution using modeling and average population densities (Ancrenaz et al., 2016).
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It is important to understand the history of orangutan populations and their current conservation status to understand the significance and necessity for a better understanding of their captive care and management. As wild populations decrease and the numbers of orangutans in rehabilitation and rescue centers increase, the need to know the issues these species face in these types of environments become even more important.
Figure 1. Current Distribution of Bornean Orangutans (Google Maps; distribution data adapted from Banes, Galdikas, & Vigilant, 2016).
Figure 2. Current Distribution of Sumatran Orangutans (Google Maps; distribution data adapted from Nater et al., 2014).
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Orangutans in the Wild
Wild Orangutan Overview
The orangutan is the only great ape found outside of Africa. Highly sexually dimorphic, with males becoming twice the size of females, they are the largest tree dwelling arboreal species on the planet (Delgado & van Schaik, 2000). They are unique, with exceptionally interesting characteristics, and are the least known of all of the great ape species (Delgado & van Schaik, 2000). Orangutans are the most solitary of all the great apes species (Galdikas, 1985). The arboreal habits, long life-span, and slow life- history of the genus Pongo have a strong bearing on resulting slow rates of acquiring demographic data on the Bornean and Sumatran orangutan (Goossens et al., 2006). The dispersed social system of the orangutan also contributes to the difficulty of acquiring data on rarely observed interactions between individuals (Goossens et al., 2006). New data and information on the orangutan has recently been made available and is allowing researchers to reevaluate some previous notions regarding orangutans and their behavior.
Females have now been shown to display affiliations towards other females within their natal groups who have heavily overlapping ranges (van Noordwijk et al.,
2012). In terms of the reproductive lives of orangutans, it is complex and remains to be completely understood, however there have been some advances. Females display mate choice for various males at different times of reproductive fertility and age (Knott,
Thompson, Stumpf, & McIntyre, 2010; Utami, Goossens, Bruford, Ruiter, & van Hooff,
2002). There is likely one dominant male in an area that females prefer, and multiple females will converge on the same male at the same time likely due to his dominance ranking and their synchronized fertility (Pradhan, van Noordwijk, & van Schaik, 2012;
13 van Schaik, 1999). Females have very strong and lengthy relationships with their offspring, devoting considerable time and energy into each (Knott et al., 2010; van
Noordwijk, Willems, Utami Atmoko, Kuzawa, & van Schaik, 2013). There is significant geographic variation in reproductive parameters between orangutan populations, but overall female orangutans devote more time to each offspring than any other mammal or great ape (van Noordwijk et al., 2013). Males are highly unusual, displaying significant sexual dimorphism and coming in two very distinct and viable forms, the flanged and the unflanged male (Pradhan et al., 2012). This is highly unusual and unique among primates, and the variability of the development of these traits even more so (Pradhan et al., 2012). Different reproductive tactics are employed by these different morphs, and depending on certain factors, have successes and failures in copulatory and reproductive success (Banes, Galdikas, & Vigilant, 2015; Goossens et al., 2006; Utami Atmoko,
Goossens, Bruford, Ruiter, & van Hooff, 2002). Flanged and unflanged males also use distinct reproductive tactics, where most matings by unflanged males are forced copulations, though flanged males in Borneo also sometimes use this tactic as well
(Delgado & van Schaik, 2000). These males also behave differently towards one another, in terms of their gregariousness and tolerance towards one another (Utami Atmoko et al.,
2009). Only flanged males make the long call that can be heard from far away, which has recently been discovered to not only discourage other males from being in an area, but also to inform females of the whereabouts of that male and even to covey the direction of his travel plans (Delgado & van Schaik, 2000; Spillmann et al., 2010; van
Schaik, Damerius, & Isler, 2013).
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Evidence supports the idea that female orangutans have individualized relationships with males (van Schaik & van Hooff, 1996). There is also now evidence that females form bonds with maternal kin (van Noordwijk et al., 2012). Female preferences for males may also be more complicated and exist outside of reproductive behaviors (Mitra Setia, Delgado, Utami Atmoko, Singleton, & van Schaik, 2009). There appears to be a more complex social system with respect to patterns of association and relationships among orangutans than previously known (Mitra Setia et al., 2009). There is some evidence now that indicates orangutans live in loose communities that incorporate organization around a dominant flanged male (Mitra Setia et al., 2009). Long calls have also now been shown to assist in coordination of movement among orangutans as well (Mitra Setia et al., 2009; van Schaik et al., 2013). However, further study is needed to determine the full complexities of the orangutan social system and there will likely be variation between Sumatran and Bornean sites (Mitra Setia et al., 2009).
Female Philopatry and Male Dispersal
Most mammals display male-based dispersal patterns (Greenwood, 1980, as cited in Nietlisbach et al., 2012). Most orangutan behavioral studies, even though sample sizes for each are small, support female philopatry with many maturing females settling near the home range of their mother and also support male dispersal (Rodman, 1973;
MacKinnon, 1974; Rijksen, 1978; Galdikas, 1985; Mitani, 1989; van Schaik & van
Hooff, 1996; Singleton & van Schaik, 2002, as cited in Mitra Setia, et al. 2009). Most available behavioral observations suggest that dispersal patterns of orangutans are indeed male-biased, unlike the African great apes, and that the female-biased dispersal patters that are seen among these species evolved after the divergence from orangutans, possibly
15 reflecting a social “ancestral state” where other forms of great ape sociality derived
(Kappeler et al., 2002; Baker et al., 2004, as cited in Goossens et al., 2006). Proof of male dispersal and strong female philopatry in orangutans has recently been made available through genetic studies (Nater et al., 2011; Nietlisbach et al., 2012; van
Noordwijk et al., 2012). Nietlisbach et al. (2012), showed evidence for long-distance male-based dispersal in orangutans, which has been the driving force behind genetic flow among these populations. They suggest that female-based dispersal is tied to multi-male groups in the great ape evolutionary past and also suggest that the benefit of this type of grouping is for male coalitions with kin or non-kin, which is something not seen in orangutans. It is likely that the benefits to female orangutans for staying near female kin and hence in a familiar environment is of more importance than for males, which is likely also the case for gorillas living in uni-male groups with multiple females and their offspring (Harcourt & Stewart, 2007, as cited in Nietlisbach et al., 2012).
Having an understanding of wild populations of orangutans and their natural behavior is important to understand when working towards and understanding of captive orangutans and their care. Considerations must be made when managing species as to their specific adaptations, behavior, and sociality to ensure proper care and to address species-specific needs in a captive setting.
Orangutan Sociality
Social Organization
The arboreal habits, long life-span, and slow life-history of the genus Pongo have a strong bearing on resulting slow rates of acquiring demographic data on the Bornean and Sumatran orangutan (Goossens et al., 2006). The dispersed social system of the
16 orangutan also contributes to the difficulty of acquiring data on rarely observed interactions between individuals (Goossens et al., 2006). Flanged male orangutans are observed to display extreme hostility towards one another, though unflanged males are sometimes affiliative (Utami Atmoko et al., 2009). The extreme sexual dimorphism observed in orangutans is in line with behavior between flanged male orangutans, and points to female mating preferences for dominant flanged males as the force behind this strong male competition (Utami Atmoko et al., 2009). Sumatran and Bornean orangutans are the only species of ape where both sexes are non-gregarious (van Noordwijk et al.,
2012). Orangutans and chimpanzees are characterized as being individual-based fission- fusion species (van Schaik, 1999). Group-based fission-fusion societies exist when a species live in permanent social grouping that sometimes fission into smaller groupings, even just one individual (van Schaik, 1999). Individual-based fission-fusion societies are those where they can only be understood through patterns of associations and individuals are mostly solitary (van Schaik, 1999). In large bodied tree-dwelling fruigivores such as spider monkeys, chimpanzees, and possibly orangutans, individual-based fission-fusion are typically found particularly among females (van Schaik, 1999). Social benefits, rather than ecological, are likely at play in this type of organization (van Schaik, 1999).
Because orangutans are alone the majority of the time, as seen on both Borneo and
Sumatra, and most associations tend to be in large fruiting trees and serve social purposes, their sociality is considered to be individual-based fission-fusion (van Schaik,
1999; Malone, Fuentes, & White, 2012).
The majority of diurnal primate species live in groups, with significant variation in group size and structure (van Schaik, 1999). The social organization of orangutans has
17 just begun to be better understood and there continues to be contributions to this understanding. Past characterizations of the orangutan include solitary females who only occasionally spend time with males when fecund, who avoid one another and have no social bonds (Mitra Setia et al., 2009). Flanged dominant males have also been viewed as fiercely territorial with unflanged and non-dominant flanged males avoiding these larger males while sneaking around in their territories (Mitra Setia et al., 2009). Many of these characterizations are slowly becoming dispelled as new research continues to shed light on other elements of orangutan social life (Mitra Setia et al., 2009). Current data suggests that orangutans live in loose communities that are organized around a dominant flanged male (Mitra Setia et al., 2009).
Variation between Bornean and Sumatran Populations and Age/Sex Classes
Sumatran orangutans are found at higher densities and are observed to have more associations than in Borneo (van Schaik, 1999). Associations are observed at different rates between different age and sex dyads or groupings (Mitra Setia et al., 2009). Fecund females, females with offspring, and unflanged males have associations that often include social play (Mitra Setia et al., 2009). Fecund nulliparous females tend to be the most social of the possible dyads, with fecund females and unflanged males also being rather social (Mitra Setia et al., 2009). The least gregarious of all are the non-dominant flanged males who actively avoid other males and who are avoided by females and young (Mitra
Setia et al., 2009). There are social benefits from these associations but there are also grouping costs which are different between different age-sex classes, typically with females with mid-sized infants being less likely to be found in parties (van Schaik, 1999).
Predation risk is higher for youngsters than adults and they are therefore expected to
18 benefit more from proximity and associations with each other and adults (van Schaik,
1999). Adult orangutans are likely to obtain social benefits from grouping, such as mating opportunities and socialization, or potentially harassment protection (van Schaik,
1999). Sociality is likely different between various age-sex classes due to the various cost and benefits (van Schaik, 1999). Typically, orangutans with the smallest party sizes are non-dominant adult males and females with mid-sized infants (Galdikas, 1985).
Adolescents show similar patterns of associations as other categories and it is assumed that benefits for both adults and adolescents are social (van Schaik, 1999).
Feeding aggregations can be observed among orangutans when there are large fruiting trees, with an upwards of fourteen animals observed in one tree at a site in
Sumatra (Mitra Setia et al., 2009). More active associations are also observed and are referred to as travel bands (Sugardijito et al., 1987, as cited in Mitra Setia et al., 2009).
Party sizes of orangutans differ between sites in Sumatra and sites in Borneo, with
Sumatran females averaging between 1.5 and 2.0 and Bornean females averaging between 1.05 and 1.3 (van Schaik, 1999). If an orangutan was truly solitary, their party size would be 1.0 (Mitra Setia et al., 2009). Additionally, young independent orangutans show the highest rate of association of the age-sex classes at two separate sites in
Sumatra, but have the lowest rates of association at two sites studied in Borneo (Mitra
Setia et al., 2009).
Understanding the social behavior of orangutans is an important component to understanding the species as a whole. Managing captive populations of orangutans, or any species for that matter, must involve an understanding of their natural behavior to meet species-specific needs. The variation that exists among orangutan populations is
19 significant, as there are not only social and behavioral differences, but also ecological and morphological variations. These variations could play an important role in a number of aspects in their captive care and management. Adapted variations between species could contribute to variations in responses to captive environments, including lower activity levels, predilection to obesity, and susceptibility to disease.
20
CHAPTER 3
FEMALE ORANGUTANS
Female Behavior
Female Social Behavior
The belief that female orangutans are solitary and avoid one another, with the exception of brief consortships with males when fecund, needs to be reconsidered (Mitra
Setia et al., 2009). Female orangutans in Borneo are much less social than Sumatran orangutans, which reflects the difference in population density. Female orangutans form clusters with their female relatives, displaying patterns of distributions more similar to other primates, rather than just living near one another as once thought (Singleton, Knott,
Morrogh-Bernard, Wich, & van Schaik, 2009). Females form these clusters when they settle near their mother and form adjacent ranges (Singleton et al., 2009). These ranges and cluster sizes appear to have a pattern, as observed between various sites, showing that high orangutan density will support larger clusters and higher overlap in home ranges
(Singleton et al., 2009). In addition, females from different clusters do not have friendly interactions (Singleton et al., 2009). This pattern in female orangutan social organization has been observed both in Borneo (Gunung Palung) and in Sumatra (Suaq) (Singleton et al., 2009). In Sumatra, associations between adult females and young orangutans of various ages from the same clusters are common (Mitra Setia et al., 2009). Females also show affiliation with certain males over others, outside of female fecundity, suggesting
21 the potential for other social tendencies (Mitra Setia et al., 2009). In some orangutan populations, there does appear to be a more complex social environment than was once thought to exist among orangutans (Mitra Setia et al., 2009).
Female Philopatry and Relatedness
Female orangutans are philopatric (Nater et al., 2011; Nietlisbach et al., 2012; van
Noordwijk et al., 2012) and have recently been discovered to have social relationships with their maternal kin, but do sometimes live without related females nearby (van
Noordwijk et al., 2012). Behavior can be significantly different between related and unrelated females, suggesting potential risks with associating with unrelated females (van
Noordwijk et al., 2012). A study by van Noordwijk et al. (2012), found that related females tended to display tolerance while feeding at the same food patch and could have long lasting associations, in addition to encouraging their offspring to play and interact.
This study also showed that unrelated females did not have long lasting associations, were intolerant of one another while feeding, and actively discouraged their young from interacting. Agonistic interactions were also found to be much more common between unrelated females than related females (van Noordwijk et al., 2012), with females sometimes chasing away the offspring of another female nearby (van Noordwijk et al.,
2009).
Female Ranging Patterns and Home Ranges
Adult female orangutans have highly overlapping ranges at all study sites
(Singleton et al., 2009). The females that live in these overlapping ranges are believed to be close relatives, and indeed, recent data confirms relatedness of females within these clusters (Knott et al., 2008; Singleton et al., 2009; van Noordwijk et al., 2012). Females
22 within these clusters show higher affiliation rates and have social relationships with one another (Nater et al., 2011; Nietlisbach et al., 2012; van Noordwijk et al., 2012), with females displaying preference for associations with particular females, and where reproductive synchronicity has been observed (Singleton et al., 2009).
Adult female orangutans have home ranges of about 900 hectares that overlap heavily, particularly in areas of high density (Delgado & van Schaik, 2000). There are extreme variations in the approximation of female home ranges, with some ranges being fifteen times larger than others, and some of this variation is found between species and subspecies though some could come from variation in sampling methods (Singleton et al.,
2009). Females do not use all of their range with equal amounts of time and females likely vary in the size of their range within a population also (Singleton et al., 2009).
There are also core areas of these ranges that females spend more time in (Singleton et al., 2009). Female ranges overlap heavily at all sites, though they likely vary, with density playing a role and there is no home range territoriality (Singleton, et al. 2009).
However, there may be evidence of female territoriality within a given core area as evidenced by the higher likelihood of resident females to win fights within their core areas (Knott et al., 2008; Singleton et al., 2009). Even when female home range has been lost to deforestation, resident females refuse to leave (Knott et al., 2008; Singleton et al.,
2009).
Female orangutans have adapted to their environment in a number of ways. Their natural history is an important aspect to understanding the species as a whole. Ecological adaptations and sociality are significant when investigating potential differences between the sexes of these species as it relates to their captive care and management. A possible
23 contributing factor to an increase in overall body size and body weight among captive orangutans could be more limited space and decreased activity levels in zoo settings, combined with more consistent nutritional intake.
Female Reproduction
Female Associations during Fecundity, Mating Preferences, and Female Choice
Female orangutans seek out copulation consortships with dominant flanged males during the time of fecundity (Delgado & van Schaik, 2000). Fecund female orangutans in long-term studies have been shown to preferentially mate with flanged males versus unflanged males (Knott et al., 2010). Females who are sexually active have more associations with both flanged and unflanged males and tend to be around other females at this time, likely due to mutual interest in the same male (Mitra Setia et al., 2009).
Field observations on orangutans show a strong preference for females to form consortships with the dominant flanged male in a given area, and unflanged males typically force copulations with females, with much resistance from the females
(Galdikas, 1985; Schürmann & van Hooff, 1986). Recent paternity data from one site in
Borneo indicates the dominant flanged male in this area had significantly higher reproductive success than other males in this area during his period of dominance (Banes et al., 2015).
Females appear to show mate choice by preferring to initiate interactions with or resisting copulation attempts with certain males and not others which also indicates there may be relationships between individuals (Delgado & van Schaik, 2000). However, there are reports of females preferring unflanged males dependent on the state of the male dominance hierarchy. Utami et al. (2002) describe a Sumatran population where
24 reproductive females preferred flanged males, but more so during times of stability in the male hierarchy. During times of rank instability, Utami et al. (2002) found reproductive and non-reproductive females mating with both flanged and unflanged males. In this population, matings with unflanged males were more common and they were less resisted by females (Utami et al., 2002). Other data support more female promiscuity during times of rank instability (Banes et al., 2015). Additionally, Banes et al. (2015) suggest that their results support female choice. Female choice in orangutans could be particularly important given that they have very lengthy interbirth intervals and have few offspring (Banes et al., 2015).
Females with dependent offspring are less gregarious than females without dependent offspring (Mitra Setia et al., 2009). Females looking for a high-quality mate in sexually dimorphic species are met with challenges to find strategies that work to their favor without incurring the high cost of infanticide or other types of coercion (Knott et al., 2010). Female mate choice might exist due to infanticide avoidance mechanisms, but because there are no reports of such infanticidal incidents in this genus, this is speculation
(Delgado & van Schaik, 2000). Higher encounter rates between females and flanged males has been associated with higher mating frequencies which would appear to indicate female choice due to the “sit and wait” strategy of flanged male orangutans as opposed to the “go and find” strategy of unflanged males (Knott et al., 2010; Utami et al., 2002).
There is extreme male-male competition among orangutans, which is consistent with the extreme sexual dimorphism also observed in orangutans (Utami Atmoko et al.,
2009). Female mating preferences may result in the reproductive success of flanged males (Utami Atmoko et al., 2009b). Dominant flanged male orangutans are also better
25 equipped to maintain consortships with females, whereas unflanged males may lose their consorts due to interference by larger males (Utami Atmoko et al., 2009b). Intense male- male competition, female preference for dominant flanged males, and female resistance to unflanged males during fecundity are all linked to sexual selection among orangutans
(Utami Atmoko et al., 2009b). If female preference did not exist among orangutans, unflanged males would have the advantage given their better mobility, it is therefore female mating preferences that contribute to strong male-male competition (Utami
Atmoko et al., 2009b).
Female Reproductive Parameters
Concealed Ovulation, Age of First Parturition, Interbirth Intervals, and Signs of Pregnancy
Orangutans are the only great ape with concealed ovulation (Knott et al., 2010).
There are no obvious sexual swellings or any other type of visual indicators of female orangutan receptiveness (Delgado & van Schaik, 2000; Utami et al., 2002). Because there is no visible estrus swelling or indications of ovulation, observers must rely on behavioral changes of the female that might indicate a change in her receptivity
(Schürmann & van Hooff, 1986). The average age of a female orangutan at first reproduction is 15.5 years old, as compared to gorillas at 10.1 years old, chimpanzees at
13.5 years old, and human hunter-gatherers at 19.7 years old (as reviewed in Wich et al.,
2009). The gestational range for orangutans is between 223-267 days (Rowe, 1996).
Interbirth intervals for orangutans are the longest for any other primate at 7.7 years (Wich et al., 2009). In captive environments, interbirth intervals are shorter than for wild populations at 5.5 years (Wich et al., 2009). Of all of the great ape species, orangutans have the slowest life history with chimpanzees and gorillas respectively following behind
26
(Wich et al., 2009). Hunter gatherers display the shortest interbirth interval and the highest age of first reproduction (Wich et al., 2009). Pregnancy swellings, swelling of the labia during pregnancy, can be observed within a few weeks after conception
(Schürmann & van Hooff, 1986).
Mother-Infant Relationships and Parental Investment
Parental investment in the orangutan is the female’s responsibility, whereby the female carries the fetus for over eight months and then cares for her offspring for an additional six years and the male simply inseminates the female (Schürmann & van
Hooff, 1986). Orangutans have the longest interbirth interval of any other mammalian species and other apes of 6-9 years (van Noordwijk et al., 2009) and this is linked to high infant survivability (Knott et al., 2010). Female orangutans invest heavily in their offspring (Knott et al., 2010) and females have strong associations with their infants (van
Noordwijk et al., 2009). This would appear to show that young orangutans need more time to grow and to develop needed skills to survive without their mothers care (van
Noordwijk et al., 2009). However, studies have shown similarities between young chimpanzees and orangutans in their development so it is possible that the solitary lifestyle of orangutans may play a role in their long interbirth intervals, though this requires further study (van Noordwijk et al., 2009). Bornean orangutans have the longest period of lactation compared to any other land mammal (van Noordwijk et al., 2013). In a study of a population of orangutans in Borneo, they found that females have an energy balance that allows them have subsequent offspring without much recovery time between births and that this is observed even in the absence of a stable food supply (van
Noordwijk et al. (2013). Infants in this study also began supplementing their intake of
27 milk with other foods at the age of 1-1.5 years old and the average lactation period for females was 6.5 years (van Noordwijk et al., 2013). Compared to other great apes, orangutans have late weaning ages also, with Bornean orangutans weaning between 5-7 years and Sumatran orangutan weaning between 6-8 years, whereas chimpanzees wean at
4-6 years (Watts & Pusey, 1993; Boesch & Boesch-Achermann, 2000, as cited in van
Noordwijk et al., 2009) and gorillas at 3-4 years (Watts & Pusey, 1993; Robbins et al.,
2007, as cited in van Noordwijk et al., 2009). Variation also exists between populations of orangutans in later development, though there are similarities in earlier phases, but this is yet to be well understood (van Noordwijk et al., 2009).
Male Avoidance and Infanticide
Infanticide has not been observed in the orangutan with one exception taking place in a captive environment (Knott et al., 2010). The slow reproductive rates and low encounter rates between orangutans potentially lowers the risk of infanticide, however it also reduces the chances of infanticide being observed (Knott et al., 2010). The life- history of orangutans predict the high potential of infanticide within this genus (van
Schaik & van Hooff, 1996). Female orangutans with infants avoid the long-calls of unfamiliar males which supports the theory of infanticide risk in orangutans (Knott et al.,
2010). For protection against infanticide, lactating females possibly hone in on known flanged males by using their long calls to locate them (Delgado & van Schaik, 2000).
Females in general may also avoid males by tracking their long calls, however unflanged males are not as easy to avoid and often harass lone females to force copulations
(Delgado & van Schaik, 2000). Loose associations between flanged males and females
28 may be explained by the potential threat of infanticide by new dominant males entering an area (Delgado & van Schaik, 2000).
Observations of the sexual behavior of Sumatran female orangutans are in line with the infanticide avoidance hypothesis (Delgado & van Schaik, 2000). To gain the protection of a flanged male against infanticide, fecund females should initiate and preferentially mate with flanged males and avoid and resist mating attempts with unflanged or subordinate males during times of this fecundity (Delgado & van Schaik,
2000). Additionally, females should support new males who takeover dominance in a particular area and when there is no dominant male should behave promiscuously and reduce their resistance to mating with both flanged and unflanged males during times of instability (Delgado & van Schaik, 2000) which has been observed (Utami et al., 2002).
Beaudrot, Kahlenberg, and Marshall (2009) argue against the adaptiveness of infanticide in orangutans. They conclude that if infanticide did exist in orangutans, it likely would have been observed at this point. In addition, Beaudrot et al. (2009) also explain that there is not enough evidence that females use counterstrategies for infanticide, other than maybe promiscuity and that the three requirements for infanticide to be a male adaptive strategy are not met by either the Bornean or the Sumatran orangutan. It is also argued that because orangutan males cannot be certain they will sire the subsequent offspring, that there are no associations that last year-round, and there is a long waiting time for potential female conception, males would not benefit from committing infanticide
(Beaudrot et al., 2009).
Given that female orangutans have the longest inter-birth interval of any mammal species, their low reproductive rate has direct implications for the conservation of these
29 species. Populations of orangutans can be heavily impacted by small declines as populations of orangutans do not quickly recover from these losses. Female orangutans have their first offspring later in life than other great apes and invest heavily in each offspring. Slower life histories of orangutans could be reflective of developing nutritional independence more slowly than other great apes (van Noordwijk & van
Schaik, 2005). Long interbirth intervals can be indicative of slow infant development and a late weaning age (van Noordwijk & van Schaik, 2005). Understanding wild orangutan reproduction and development are important aspects to understanding their captive care and management.
The long period of lactation and slow life histories observed in orangutans could potentially provide safe-guards and protection against forms of disease, including respiratory illness. The solitary life-style of orangutans could also inhibit protections against disease, particularly during younger years in development when infant orangutans would likely only be exposed to their mother and would therefore have limited exposures.
However, females with new infants and weaned offspring have been observed to form
“nursery groups” where their offspring are allowed to socialize with each other (van
Schaik, 1999). It is believed that these associations provide opportunities for socialization and protection against harassment (van Schaik, 1999). It is possible these associations could also provide exposures to assist in developing a healthy immune system.
In captive environments, shortened lactation periods due to food abundance could increase risk for certain illnesses, including respiratory disease, and risks could increase over a lifetime. Hand-rearing in captive environments could pose similar risks given
30 minimal access or no access at all to mother’s milk. In rehabilitation centers, orphaned orangutans no longer have any protections from nursing, and may have had virtually none from very early on in life. The lack of mothers milk, coupled with increased exposure due to social groupings kept in captive environments and in rehabilitation centers, could all contribute to the propensity of respiratory disease observed in captive settings and rehabilitation centers.
Slow life histories and late weaning ages of orangutans could also make young dependent orangutans vulnerable to disease if the mother becomes pregnant before weaning has occurred, if mother’s milk continues to provide antibodies or other helpful bacteria over time. Observed active avoidance of female orangutans with dependent offspring towards male orangutans could be indicative of the risks associated with forced copulations by becoming pregnant prior to the current offspring being nutritionally independent.
The thrifty phenotype hypothesis is a model to help understand the relationship between early life experience and outcomes later in life (Wells, 2007). The thrifty phenotype hypothesis also posits that fetuses adapt to environmental conditions within the womb that are directly associated with the mother’s nutritional status and consumption during pregnancy (Hales & Barker, 1992; Wells, 2007). If pregnant female orangutans have had nutritional deficits, the fetus will adapt to these conditions. If then, once born, nutritional quality increases, this could lead to increased susceptibility to certain disadvantageous conditions such as obesity (Hales & Barker, 1992; Wells, 2007).
It is then possible to speculate, at least for rehabilitant orangutans who were born to wild female orangutans, nutritional intake at these rehabilitation centers likely exceed what
31 had been adapted for, hence leading to possible increased susceptibility to certain health problems. It is also possible that early nutritional conditions have some effect on later adult health outcomes. Though there is evidence from animal studies to support a connection between fetal growth and later life outcomes, postnatal growth rates are also shown to influence the adult phenotype (Wells, 2007).
32
CHAPTER 4
MALE ORANGUTANS
Male Behavior
Bimaturism and Behavior
Orangutans are highly sexually dimorphic (Schürmann & van Hooff, 1986).
Bimaturism is also observed between adult males of the genus Pongo and the age at which secondary sexual characteristics develop varies significantly (Utami et al., 2002).
Large cheek flanges, enlarged laryngeal sacs, long hair on the arms and back, long calling, and a heavier weight than unflanged males, are all indicative of the secondary sexual characteristics displayed by male orangutans (Harrison & Chivers, 2007; Knott &
Kahlenberg, 2007, as cited in, Pradhan et al., 2012).
Flanged Males and Unflanged Males
There are major differences observed between flanged and unflanged males with respect to their associations with one another. Flanged males are intolerant of other flanged males when they encounter one another, but are more likely to avoid each other
(Utami Atmoko et al., 2009). Flanged males are aggressive towards one another when they do have encounters, though these instances are somewhat rare (Utami Atmoko et al.,
2009). Flanged males’ intolerance of one another is observed with or without the presence of females in the area (Utami Atmoko et al., 2009). When these encounters do occur, fighting can be intense and can result in major injuries, residual scaring and
33 injuries are often seen (Utami Atmoko et al., 2009). Fighting appears to be more severe among Bornean males, however there is a lack of data to support this claim (Utami
Atmoko et al., 2009). Non-linear dominance hierarchies exist between flanged males and there is one clearly dominant flanged male in an area, as seen in Sumatra and this is also likely the case in Borneo as well (Utami Atmoko et al., 2009).
Relationships between flanged and unflanged males are described as being
“marked by imposed tolerance” and unflanged males are always subordinate to flanged males (Utami Atmoko et al., 2009). Flanged males who are in association with a female will tolerate unflanged males as long as they maintain a respectful distance (van Schaik & van Hooff, 1996). These unflanged males will try and attempt matings when the flanged male is otherwise distracted (van Schaik & van Hooff, 1996). Unflanged males typically hang out around flanged males, at a distance, especially if the flanged male is in association with a female but rates of aggression towards these unflanged males also increase during these times (Utami Atmoko et al., 2009). Unflanged males are known to be more tolerant of each other and have more regular associations, sometimes traveling together and associating with females together, but this decreases as they age (Utami
Atmoko et al., 2009). Aggression rates increase among these males when there is a female present and aggressive encounters between unflanged males are less common than by flanged males towards unflanged males (Utami Atmoko et al., 2009). There have also been observations of male-male homosexual behavior in unflanged male wild orangutans and male adolescents (Fox, 2001).
Understanding the morphological variation that exists between wild male orangutans is important to understanding the potential variation observed in captive
34 settings. Variations in the development of males could also have implications for their captive care and management and possible susceptibility to disease.
Male Bimaturism and Development
Male Secondary Sexual Characteristics
Unflanged males are males who have yet to develop secondary sexual characteristics. One Sumatran orangutan was proven to stay in arrested development for twenty years after siring offspring and eventually developed flanges when it was possible for him to overtake the dominant flanged male in the area (Utami Atmoko & van Hooff,
2004; te Boekhorst et al., 1990, as cited in Pradhan et al., 2012). No cases have been reported showing that once a male orangutan develops flanges that this can be reversed
(Dunkel et al., 2013). However, there are reports of male orangutans having shriveled flanges potentially due to old age or not having good body condition due to food scarcity
(Dunkel et al., 2013).
The development of secondary sexual characteristics varies between Bornean and
Sumatran males (Pradhan et al., 2012). Sumatran males can take years to develop and there is the possibility that some Sumatran males never develop these characteristics
(Dunkel et al., 2012). This flexibility in development is unique among male primates
(Dunkel et al., 2013; Pradhan et al., 2012). Developmental arrest appears to be less common among the male Bornean orangutan (Pradhan et al., 2012). It is more difficult for flanged Bornean males to monopolize matings than for flanged Sumatran males, which is suggested to play a role in this variation (Pradhan et al., 2012). Flanged males appear to be more common in Borneo than Sumatra and this could influence reproductive success (Delgado and van Schaik, 2000). The model designed by Pradhan et al. (2012)
35 suggests that in populations with high despotism the presence of flexible developmental arrest will exist, which is consistent with the observed behavioral data between Sumatran and Bornean males. Other data also shows that dominance for Bornean males is more unstable and is shorter lived than for Sumatran males (Pradhan et al., 2012). The differences observed in arrested development between populations have not been tested, however the study by Dunkel et al. (2013) did give more evidence that these predictions are true. The differences observed in flanged versus unflanged males in Borneo and
Sumatra is likely not an artifact of methods used but rather suggest real differences between these populations, though more data are needed from Bornean sites to confirm these generalities (Dunkel et al., 2013).
The proximate reasons for developmental arrest are still unclear and the hypothesis that this arrest is stress induced is not supported (Maggioncalda, Czekala, &
Sapolsky, 2002). Maggioncalda et al. (2002) found that stress hormones are much higher in male adolescents that are in the process of developing than in juvenile, adult, or arrested males. They concluded that developmental arrest could potentially be an adaptation in some male orangutans to actually avoid stress during their adolescent or sub-adult years. Thompson, Zhou, and Knott (2012) found that testosterone levels among developing males were significantly higher than among males who had experienced developmental arrest. In addition, this study showed that males with high levels of testosterone maintained these levels whereas males who had delayed maturation continued to have lower levels of testosterone even after development. Thompson et al.
(2012) suggest that these findings could be trait-level characteristics that tie in with a
36 particular males’ life history strategy. More research is needed to fully understand male orangutan bimaturism.
Recognizing the factors responsible for the variation observed between male orangutans is an important factor to understanding their size, development, and growth patterns that could potentially influence their responses in captive settings and potentially have implications with respect to susceptibility to certain ailments.
Male Reproductive Tactics
Forced Copulations, Copulatory Behavior, and Reproductive Success
Both flanged and unflanged males in Borneo are known to force copulations with females, however in Sumatra flanged males virtually never use forced copulation as a tactic (Delgado & van Schaik, 2000; Goossens et al., 2006). Both flanged and unflanged males are known to produce offspring both in Sumatra (Utami et al., 2002) and in Borneo
(Goossens et al., 2006). In one particular study, about half of the paternity was attributed to unflanged males indicating that flanged males do not necessarily have full control over mating opportunities (Utami et al., 2002). However, if females do not necessarily display mate choice and prefer dominant flanged males, it is difficult to explain the reproductive benefit for flanged males to maintain their costly secondary sexual characteristics (Utami et al., 2002). There is a hypothesis that flanged males employ a “sit and wait” strategy and that unflanged males employ a “go and search” strategy (Utami et al., 2002).
There are similarities and differences observed between the mating behavior of
Bornean and Sumatran orangutans (Pradhan et al., 2012). Sumatran female orangutans approach long calls of the dominant flanged male, which are individually recognizable, when they are fecund (Delgado, 2006; Spillmann et al., 2010). Females may spend an
37 upwards of three weeks in a consortship with the dominant flanged male and multiple fecund females may all actively pursue the same male at the same time (Pradhan et al.,
2012). Other flanged males may be nearby and these males will actively avoid the dominant male and females often ignore them (Pradhan et al., 2012). Interestingly, dominant flanged males also show preference for mating partners and tend to be selective by choosing to mate with parous females over nulliparous females likely due to adolescent sterility (Schurmann, 1981, 1982; Knott & Kahlenberg, 2007, as cited in
Pradhan et al., 2012). Until these females are more likely to conceive, they tend to mate voluntarily or are subject to forced copulations by unflanged males (Pradhan et al., 2012).
Other non-dominant flanged males are shown to be largely unsuccessful in mating opportunities in that they do not force copulations and they are unable to access the females because these males still long call, giving away their location and direction of travel (van Schaik, 2004, as cited in Pradhan et al., 2012) which gives females the ability to avoid them (Pradhan et al., 2012).
In Borneo, females consort with flanged males for a shorter duration of time than in Sumatra and consortships may not even happen (Pradhan et al., 2012). Male Bornean orangutans also participate in aggressive encounters with one another, inflicting bodily harm to one another and these conflicts sometimes even result in death (Knott &
Kahlenberg, 2007, as cited in Pradhan et al., 2012). Observation of this type of male conflict in Sumatra are non-existent (van Schaik unpublished, as cited in Pradhan et al.,
2012). Multiple flanged males, dominant or not, in a particular area are observed to mate and sometimes do so forcibly (Knott et al., 2010). Female orangutans in Borneo appear to be more vulnerable to flanged males who they do not choose to mate with which could
38 explain both why non-dominant flanged males have high rates of encounters and matings with these females and why these males tend to mate forcibly (Pradhan et al., 2012).
Utami et al. (2002) suggest that possibly only certain unflanged males had successful matings with females, and observations from this study appear to show that these were resident males and not roaming males, or “floating” males, that were common in the area. Utami et al. (2002) further suggest that this finding lends support to the theory that individual pair bonds may exist (van Schaik & van Hooff, 1996). A recent longitudinal paternity study indicates that a long-time dominant flanged male had greater reproductive success than other males within his home range, more than both the unflanged males in this area and other subordinate flanged males during his period of dominance (Banes et al., 2015). Banes et al., (2015) also report paternities by other males but mainly during times of rank instability, namely at the beginning and the end of this male’s dominance. These authors conclude that in contrast to Utami et al., (2002) whereby both flanged and unflanged males had equal successes reproductively, their research indicates that an evolutionarily stable strategy exists whereby dominant flanged males enjoy greater reproductive success and unflanged males wait for mating opportunities during times of rank instability (Banes et al., 2015).
Male orangutan reproductive tactics vary depending on their developmental and dominance status. Understanding why different tactics are employed by male orangutans is important in understanding their responses to certain environmental factors. These could have implications to their environmental responses in captive settings.
39
Male Dispersal and Vocalizations
Dispersal and Ranging Patterns
Strong male dispersal has recently been evidenced through genetic studies (Nater et al., 2011; Nietlisbach et al., 2012; van Noordwijk et al., 2012). At maturity, males tend to disappear from their natal ranges and the majority of new individuals moving through or entering areas are males (Delgado & van Schaik, 2000). Home ranges of flanged males are considerably larger than that of females, around 2,000 to 3,000 hectares, with very high overlap (Delgado & van Schaik, 2000; Utami Atmoko et al., 2009). Ranging patterns in males vary likely in response to fruit availability, fecund females, and other males nearby (Delgado & van Schaik, 2000). It has been difficult to properly assess male home ranges because these areas are often larger than the actual study area (Utami
Atmoko et al., 2009). There is also difficulty is determining whether there is a variance in flanged versus unflanged male ranges (Utami Atmoko et al., 2009). However, it is still fairly clear that male ranges are indeed larger than female ranges and that male ranging patterns show no definable territories or exclusive ranges (Utami Atmoko at al., 2009). It appears that male ranges are likely around three to five times larger than female ranges in the same area (Utami Atmoko et al., 2009).
Vocalizations
Only flanged males long call, and these calls can travel up to one kilometer though the forest (Spillmann et al., 2010; van Schaik & van Hooff, 1996). These long calls might be designed to display strength and the ability of that male to be a good protector or could also possibly create a safe area free of other male orangutans who typically avoid long calls of dominant males (Delgado & van Schaik, 2000). Females
40 have been observed to quickly travel towards a long calling male when being harassed by an unflanged male (Delgado & van Schaik, 2000). Studies have shown that reproductive female orangutans are attracted to male long calls and non-reproductive females avoid long calls (Spillmann et al., 2010). Other studies have proven that long calls can be individually recognized which can be beneficial for females who could use this information to their advantage (Delgado, 2006). In Sumatra, long calls are also thought to assist in female choice and in infanticide avoidance and to allow females to remain within earshot of the dominant flanged male (Mitra Setia & van Schaik, 2007). Females have also been shown to respond to familiar long calling males (Mitra Setia & van
Schaik, 2007). Flanged males will also indicate the direction of their travel the following day by long calling in that direction the night before and this information is in fact used by other orangutans who adjust their own travel plans for that day (van Schaik et al.,
2013).
Because Bornean male orangutans are suggested to flange more often than
Sumatran male orangutans, and if these secondary sexual characteristics including a more developed throat sac play a role in developing respiratory disease, then we might expect
Bornean male orangutans to have a higher predilection to developing respiratory disease than Sumatran or Hybrid orangutans in captive environments. Unless, perhaps, male orangutans develop secondary sexual characteristics more equally in captive environments. If the risk of being affected by respiratory disease is influence by larger size, then we could expect that male orangutans would have a higher propensity for respiratory disease than female orangutans, given the extreme sexual dimorphism observed in these species.
41
CHAPTER 5
ORANGUTAN ECOLOGY
Introduction to Orangutan Ecology
Because the orangutan is not part of the human main family line they have not been as studied as the African apes, in addition to being very difficult to find and easy to slip away due to their elusive nature (van Schaik, 2004). There is significant geographic variation within the populations of orangutans and these variations are observed in patterns of association, reproductive behaviors, life history patterns, morphology, tool use, vocalizations, and various other elements of orangutan life. Male orangutans are unique among primates, with two distinct morphs, each displaying different reproductive strategies and significant morphological differentiation (Utami Atmoko et al., 2009).
These adult and fully viable males come in two forms, flanged and unflanged, and vary in their development of secondary sexual characteristics with some possibly never fully developing (Utami Atmoko et al., 2009). Orangutans have the longest life history than any other primate or mammal, with females only giving birth every 6-9 years (van
Noordwijk et al., 2009). Young orangutans are very dependent on their mother for an extended period (van Noordwijk et al., 2009). Orangutans are the only great ape other than chimpanzees that are described as having cultural traditions, where these behaviors are unique to specific populations and the behaviors are learned socially (Gruber,
Singleton, & van Schaik, 2012; Krützen, Willems, & van Schaik, 2011; van Schaik et al.,
42
2003). Variation is also observed in morphology between orangutans in different populations and reflect variations in food abundance which also influences behavior, and sociality (Taylor, 2009). Orangutans are considered semi-solitary, and there is significant variation in the gregariousness of various populations, however much of their sociality remains elusive (Delgado & van Schaik, 2000).
Influence of Environment on Orangutan Behavior and Sociality
It has been argued that the orangutan social structure and their reproductive strategies derived from a gorilla-like social structure, based off of various characteristics found among orangutans today (Harrison & Chivers, 2007). Harrison and Chivers (2007) argue that due to fluctuations in weather patterns, food availability became scarce and female orangutans needed to disperse in order to acquire their nutritional needs. Because of the dispersal of these females, males could no longer monopolize and guard the females within their group, as is seen in present day gorilla groups (Harrison & Chivers
2007). Because these dominant flanged males no longer could prevent other males from breeding attempts, a niche opened for the nonflanged male (Harrison & Chivers 2007).
Harrison and Chivers (2007) go on to speculate that for these reasons, the ancestral hominoid prior to extant ape and human divergence, was more similar to the gorilla in sociality and reproductive strategies that any other extant ape. They state that some implications from their evidence suggests that mating systems of all the extant apes, including humans, are derived.
Harrison and Chivers (2007) regard orangutan and gorilla social structures to have similarities in that flanged male orangutans actively work to prevent other flanged males from mating opportunities by use of long calls and aggressive chasing. They go on to
43 state that unlike gorillas, the black back male gorillas do not have reproductive success unlike the unflanged male. It is suggested that this is due to the inability of orangutan males to prevent other males from being in his home range and to the large size and low detection rates in this type of environment, in addition to having a dispersed social system (Harrison & Chivers 2007). In terms of the orangutan mating system, they also suggest that at some point they were forced to develop into their present day dispersed- harem polygyny system from a similar form of the gorilla harem-polygyny system. The flanged male orangutan and his behavior is more similar to a silverback gorilla than to any other extant apes (Harrison & Chivers 2007).
The orangutan social structure is considered dispersed or as an individual based fission-fusion system (Malone, Fuentes, & White, 2012; van Schaik, 1999). There is significant variation within the populations of orangutans today, mainly due to habitat variation. Sumatran orangutans are more gregarious than Bornean orangutans and this is believed to be due to the higher productivity of Sumatran forests. Orangutans do have the ability to be more social when fruit abundance is high (Malone et al., 2012), suggesting a sociality exists that is just not always observable. Orangutans do form three types of social aggregations (Utami, Wich, Sterck, & van Hooff, 1997). Travel bands and temporary aggregations are related to food abundance and then there are consorts that are mating associations (Utami et al., 1997). The flexibility of orangutan sociality is dramatic, in the sense that they can drastically change their behavioral responses in direct relation to fruit densities and alter their rates of affiliation (Malone et al., 2012).
Strong overlap among female orangutan home ranges and preferential associations between these females, in Borneo and Sumatra, is also highly suggestive of
44 an existing social system that is more complicated than believed. These associations, and the need for young orangutans to socialize are significant in the process of transmitting local traditions that have been described among orangutan populations (Gruber et al.,
2012; Krützen et al., 2011; van Schaik et al., 2003). The opportunity for social learning and the behavior of adult female orangutans to encourage their young to interact imply that the significance of these encounters are great and are necessary for the successful development of young orangutans.
Geographic Variations between Populations
Species and Sub-Species
There is significant variation observed between the species and subspecies of the genus Pongo. Within the orangutan population, there are three distinct species, the
Bornean orangutan (Pongo pygmaeus), the Sumatran orangutan (Pongo abelii) that is restricted to the northern portion of this island (Groves, 2001), and the Batang Toru population (Pongo tapanuliensis) (Nater et al., 2017). There are three recognized subspecies of the Bornean orangutan; P. p. pygmaeus in western Borneo, P. p. wurmbii in southern Borneo, and P. p. morio in eastern Borneo (Groves, 2001). Currently, researchers are working to understand the differences in behavior between populations and sites.
Variation in Environment and Food Availability
Sumatran forests are known to be more productive, by producing higher quality foods and more available high-quality foods, than forests in Borneo (Marshall et al.,
2009). Diets are similar in amounts of fruit between the islands, however, Bornean orangutans have a higher variation of fruit in their diet, eat more inner bark, and have
45 more variation within their population (Wich, Utami Atmoko, Mitra Setia,
Djojosudharmo, & Geurts, 2006). For Sumatran orangutans, that means more insects and figs, but for Bornean orangutans that means a heavy dependence on fibrous foods such as inner bark (Taylor, 2009). For P. p. morio and for P. p. wurmbii, they suffer more from severe shortages in high quality foods than other orangutans (Taylor, 2009).
In north east Borneo and in south west Borneo, orangutans tend to rely heavier on fall back foods such as leaves, wood foods, and other types of vegetation which has been shown to provide less energy than fruits (Taylor, 2009).
Variation in Morphology
Morphological variation is observed among the orangutan as well, with a gradient from west to east (van Schaik et al., 2009). Quantifiable differences are found between the eastern most populations and western most populations in the Bornean orangutan, with eastern orangutans displaying more thickness in the enamel of their teeth and robustness of their jaws, reflecting a more challenging diet (van Schaik et al., 2009). The subspecies P. p. morio has a thicker jaw and higher amounts of tooth enamel, indicative of reliance on fall back foods (Taylor, 2009). Female range size also decreases from west to east, likely in response to forest quality, and these eastern orangutans have shorter day journeys than their counterparts (van Schaik et al., 2009). Folivores, because of the abundance and availability of their food source, tend to have smaller ranges than frugivores, who need more space to acquire their food (Clutton-Brock & Harvey, 1977, as cited in van Schaik et al., 2009). Cranial capacities, and therefore brain size, also decrease along this gradient also likely reflecting evolutionary responses to a less
46 frugivorous diet (van Schaik et al., 2009). When fruit in scarce, other fall back strategies are used by great apes to acquire needed calories (Taylor, 2009).
Variation in Life-Histories
In addition to morphological variation, differences are seen in many aspects of life history between the Sumatran and Bornean orangutans as well as between the
Bornean subspecies. Much of this has to do with the availability of foods. Orangutans have the slowest life history of other apes and there are various possible explanations for this, such as, lower mortality rates (Wich et al., 2009). Inter-birth intervals are also shortened in the subspecies P. p. morio, at 6.1 years whereas the Sumatran orangutan is between 7.6 and 8.75 years (Wich et al., 2004; van Noordwijk & van Schaik 2005, as cited in Taylor, 2009). In terms of life history patterns of orangutans, P. p. morio has the shortest and the Sumatran orangutan P. abelii has the longest, as well as a higher energy diet and a less robust jaw (Taylor, 2009). In orangutans, brain size and inter birth intervals significantly correspond to one another (Taylor, 2009). Interestingly, there appears to be a relationship between the degree of frugivory and life histories among hominoids (Taylor, 2009). For African great apes, a similar pattern is found in the relationships of behavioral ecology, morphological variation, life histories, and brain size that possibly can be extrapolated into predictions about lesser known species (Taylor,
2009).
Variation in Sociality
Orangutans are not consistently gregarious due to the variability of fruit abundance (Delgado & van Schaik, 2000). In all, there is agreement that orangutans are semi-solitary, but variation exists among different field sites, and within the same field
47 site over time (Delgado & van Schaik, 2000). Orangutans in Sumatra are more gregarious than Bornean orangutans (Delgado & van Schaik, 2000). Habitat productivity is higher in Sumatra than Borneo, hence Sumatran orangutans are found at higher population densities (Delgado & van Schaik, 2000). Reproductive tactics, vocalizations, encounter rates, association costs, and other behavior of orangutans is likely linked to both forest productivity and population density (Delgado & van Schaik, 2000).
The variations that exist between populations of orangutans could have implications for variations between these populations in captive environments. It is therefore important to understand these differences observed in wild orangutans in order to infer potential differences observed in captive settings and responses to various environmental factors.
Culture and Social Learning
Orangutan Culture
The existence of culture in animals is controversial because it is argued that the behavioral variation observed between populations could be genetic responses to particular environments and not derived from social learning between individuals (Gruber et al., 2012). For uses of comparison, the definition of culture as a system of socially transmitted behaviors is helpful (van Schaik et al., 2003). Van Schaik et al. (2003) concluded that geographic variation found in great ape behavior supports culture and that similarities exist between these behaviors and human cultures. They suggest that four distinct cultural elements exist and that only humans display all four. Chimpanzees and orangutans are special among nonhuman primates and display three of these elements because they are capable of innovation and higher forms of socially based learning (van
48
Schaik et al., 2003). Because of the ability of orangutans to display humanlike skills in culture, culture itself can be dated back to the divergence of orangutans and African apes, to approximately 14 million years ago, rather than to the divergence of chimpanzees and humans (van Schaik et al., 2003).
Even though there is enough genetic variation among orangutan populations that could explain the behavioral variation observed, it is more likely explained through local adaptations and developmental plasticity (Krützen et al., 2011). Krützen et al. (2011) show that developmental plasticity is in large part responsible for geographic variation seen in orangutan behavior. They also showed that genetic variation accounted for only
7% of observed behavioral variation whereas environmental variation accounted for 25% of this variation in behavioral ecology and in sociality, which lends support to developmental plasticity playing a big role (Krützen et al., 2011). In Krützen et al.
(2011), the social organization at specific sites studied was significant in understanding the cultural behaviors observed in these areas, which supports that sociality at certain sites predicts the numbers and variations of cultural behaviors. Though this study found correlations between environmental differences and social organization and behavioral ecology, it neglected to find a correlation between the environment and cultural traits, strongly suggestive of local innovations that have been socially distributed, maintained, and learned socially (Krützen et al., 2011).
Social Learning
Social learning is difficult to prove from wild studies of animals but is needed to help provide support for culture within certain species (Jaeggi et al., 2010). Differences observed in feeding behavior and diet between populations of orangutans could be the
49 result of social learning and could be the basis of the development of culture observed in orangutans (Jaeggi et al., 2010). Jaeggi et al. (2010), support the claim that orangutans have food traditions and skill cultures and that these behaviors develop when social learning is aided by associations with others. They showed that young orangutans had diets very similar to their mother, and these orangutans observed their mother during specific foraging behaviors and not during other types of behavior, showing that observational learning is important in acquiring complex skills.
Ecological or genetic variation can be used to explain geographic variation in particular skilled behaviors, however, in orangutans there are studies showing that these are not likely explanations and that social learning is likely at play (van Schaik & Knott,
2001). Van Schaik and Knott (2001) show that orangutans in certain populations use tools to get into Neesia fruits, and that this behavior is transmitted socially. They propose that certain conditions need to exist within a population for the transmission of a geographically distributed tool using skill to exist, such the high orangutan population densities (van Schaik & Knott, 2001). The particular conditions that promote transmission of these types of behaviors are likely also a major factor in not only the geographic distribution of tool using skills in orangutans, but also in chimpanzees as well
(van Schaik & Knott, 2001).
Females observed by van Schaik (1999) who had newborns often with weaned adolescent offspring were found to form parties among themselves and showed significant tolerance among one another, feeding near one another and sometimes sharing food. Benefits for these associations are not clear, however, the adolescents observed played often with one another and infants would spend time observing interactions, thus
50 this could provide benefits to social development. These females with both weaned and new infants are said to form “nursery groups” where their offspring are provided the opportunity to socialize (van Schaik, 1999). It appears overall that benefits from groupings of orangutans are mainly social (van Schaik, 1999). In addition, benefits provided by these interactions are socialization, mating, and protection against harassment (van Schaik, 1999).
It is important to recognize the significance of geographic variation not only in morphological differences between populations and their responses to their environment, but also the geographic variation that exists in behavior between these populations.
These factors have implications in the captive care and management of these species and responses to captive environments. The social lives of orangutans could also have implications for the development of healthy immune systems at an early age, as females with young offspring are found to form social groupings, possibly allowing not only for social development, for exposures that could potential assist in the development of healthy immune responses.
Vocalizations and Communication
Gestures
Intentional communication has been documented among young free-ranging orangutans (Bard, 1992). Bard (1992) showed that the intent of communicative gestures displayed by immature orangutans was not a product of human proximity, but rather a natural occurring behavior. In addition, she concluded that the ability of great apes to intentionally communicate suggests there is an evolutionary explanation for this type of competence (Bard, 1992).
51
Orangutan Vocalizations
Though communication has not been well studied in any of the great apes (Hardus et al., 2009), in particular the orangutan, available data is also suggestive of a complex social system among orangutans. For other great apes, published data reflects 38 call types for bonobos (Pan paniscus), 29 for chimpanzees (Pan troglodytes), and 16 for gorillas (Gorilla gorilla) (Fossey, 1972; Goodall, 1986; Bermejo & Omedes, 1999, as cited in Hardus et al., 2009). In total, 32 call types were discovered during the study conducted by Hardus et al. 2009 which was mostly based off of data from one particular site in Borneo. Given the fact that the number of call types for orangutans is higher than that of the gregarious and socially complex chimpanzee and just under the number of call types for bonobos, there appears to be inferences that can be made regarding the complexities of orangutan social life. Additionally, long calls that are given by flanged male orangutans also provide insight into the potential coordination of movement among certain populations of orangutans. These male orangutans give information regarding their travel plans for the next day by the direction in which they call and their conspecifics use this information to coordinate movements (van Schaik et al., 2013).
This behavior is truly fascinating and provides insight into the possible structure and existence of orangutan communities.
There is a paucity of data on vocalization and sounds made by great apes, with the possible exception of the pant hoot made by chimpanzees (Hardus et al., 2009). Most studies on orangutan vocalizations have focused on the male long call and on presence or absence of particular vocalizations between sites (Hardus et al., 2009). It is possible that the presence or absence of vocalizations among orangutan populations is yet another
52 indication of geographic variation, or cultural variation, in that vocalizations are socially learned (Hardus et al., 2009). Hardus et al. (2009) characterized orangutan calls as short- distance, middle-distance, and long-distance and interestingly found more short-distance calls than calls from the other categories. They also found that immature orangutans made 10 call types, nulliparous females made 12 call types, females with an immature made 14 call types, adult females made 4 unique call types, unflanged male made 17 call types (but no unique types), and flanged males made 15 call types with one unique type
(fast long call). Hardus et al. (2009) suggest that geographic variation in the sounds and vocalizations made by orangutans possibly lend support to an interpretation that orangutan calling is cultural.
Long Calls
Only flanged male orangutans long call (Spillmann et al., 2010). This vocalization can travel a distance of one kilometer through the forest (Spillmann et al.,
2010). Unflanged males have opportunities to gain access to females and do not make long calls hence do not give away their whereabouts to others in the area (Mitani, 1985).
A male long call may reflect his strength and his ability to be a good protector in the various properties the call itself has, such as length and duration (Delgado & van Schaik,
2000). This long call may indicate an area that is safe by creating a space that is kept clear of other flanged or unflanged males who are subordinate and typically avoid the long call of the dominant male (Delgado & van Schaik, 2000). Interestingly, it has been reported that females who are being harassed by unflanged males will quickly respond to and move towards long-calling males (Delgado & van Schaik, 2000).
53
Long calls also help in how males space themselves in relation to one another, but most likely play a large role in coordinating movements within an area with females and in female attraction (Utami Atmoko et al., 2009). Orangutans emit long calls under certain circumstances, due to disturbances in their environment, in response to another long call, during displays of strength, and sometimes for no obvious reason to the observer (Spillmann et al., 2010). Spillmann et al. (2010) were able to show that female orangutans respond accordingly to the specific context of a long call, whereby reproductive females were attracted to long calls and non-reproductive females avoided these calls, if the long call was spontaneous and meant to give that males location.
However, females avoided or ignored long calls when these calls were made in response to some type of disturbance. This study shows that females are able to discern the context of long calls given by males (Spillmann et al., 2010).
Delgado (2006) conducted a study using long calls from four distinct populations of orangutans and was able to quantitatively describe distinct variations in long calls that could be used to assign calls not only to that specific population, but also to specific individuals. This finding provides evidence that individual recognition through long calls is at play, and this would prove beneficial to females who could use this information to their advantage (Delgado, 2006). In Sumatra, long calls are also thought to assist in female choice and in infanticide avoidance and to allow females to remain in earshot of the dominant flanged male (Mitra Setia & van Schaik, 2007). Mitra Setia & van Schaik
(2007) suggest that females respond to familiar long calling males, providing evidence that orangutans, at least in one Sumatran site, have a loose social structure and are not as solitary as once believed.
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Long calls have also been shown to have planning properties, whereby males use their calls to announce their travel plans for the following day (van Schaik et al., 2013).
Van Schaik et al. (2013) showed that flanged males orangutans give a long call shortly before they nest for the night and that the direction of this call indicates the direction in which they will travel the following morning. In addition, a new call often reflects a change in direction (van Schaik et al., 2013). This study also showed that other orangutans did in fact use this information to adjust their own travel plans for the following day (van Schaik et al., 2013).
Communication among orangutans is an important component to understanding their social system, and also in understanding the evolution and development of their air sacs. Given the fact that orangutans live in more dispersed communities, this may have necessitated a more complicated and developed air sac in the genus as a whole.
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CHAPTER 6
ORANGUTAN CONSERVATION
Conservation Overview
The Bornean orangutan has recently been listed as Critically Endangered from the previous assessment of Endangered in 2008 (IUCN Red List, 2016). The status of the
Bornean orangutan population and the inclusion of this species in the category of
Critically Endangered has been influenced by significant habitat loss, degradation, and illegal hunting, with a projected loss in the population of 86% between the years of 1973-
2025 (IUCN Red List, 2016). Previous estimates for the population size of Bornean orangutans have shown 54,000 individuals remain (Wich et al., 2008). Recently, however, the use of more recent field data from Borneo displaying a larger range of their current distribution and applying this to modeling techniques, the population estimate now stands at 104,700 (IUCN Red List, 2016). Though this higher population number is encouraging, Bornean orangutans have still suffered a loss to their population of approximately 288,500 since 1973 and are expected to have a population of 47,000 by
2025 (IUCN Red List, 2016). The Sumatran orangutan population estimate has also recently been modified, though they continue to be listed as Critically Endangered as they have been since 2000 (IUCN Red List, 2016). The previous population estimate showed only approximately 6,600 individuals remaining (Wich et al., 2008). The population estimate for the Sumatran orangutan now stands at 14,613, however by excluding
56 populations that are not considered to be viable into the future, this number is reduced to
13,835 individuals (Wich et al., 2016). Threats to this population are similar for those of the Bornean species, with habitat loss and fragmentation alongside illegal hunting, contributing to significant losses (IUCN Red List, 2016). It is predicted that 4,500
Sumatran orangutans will be lost by the year 2030 based on land-use projections (Wich et al., 2016). All orangutan populations are facing major threats, mostly due to anthropogenic factors.
Approximately 75% of orangutans, both in Sumatra and Borneo, live outside of protected areas (Meijaard & Wich, 2007). There are a multitude of issues that make orangutans vulnerable to extinction which include habitat conversion, habitat fragmentation and destruction, and hunting—in addition to species characteristics such as long interbirth intervals, low population densities, and large home ranges (Wich et al.,
2008). Because orangutan habitat is being lost and populations are becoming more fragmented, the potential of using only pristine forest for the conservation management of these species is likely not a viable strategy (Marshall et al., 2006). There is, however, the potential of using lightly to moderately disturbed habitat in the conservation management of these species to greatly improve the potential of the viable populations needed for the survivability of these species (Marshall et al., 2006). This would only be possible if it is shown that orangutans can survive and reproduce in these types of forests
(Marshall et al., 2006). More information is crucial in order to better understand how orangutan populations can survive in degraded forests and what impact different types of degradation have on orangutans (Marshall et al., 2006).
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Influences on Conservation
Orangutans and Geographic Variation
It appears that the Bornean orangutans cope better with logging than do their
Sumatran counterparts (Husson et al., 2009; Meijaard & Wich, 2007) and more research in needed to determine if any logging can work in conjunction with conservation efforts
(Wich et al., 2008). However, because Bornean orangutans are understood to rely more on fallback foods than Sumatran orangutans, and fallback foods are shown to be disrupted more than other foods due to logging activities, it would seem logical that
Bornean orangutans instead would be the more susceptible species to logging.
Regardless, it is likely that orangutan responses to logging differ between species and even subspecies as is observed between other great ape species such as gorillas and chimpanzees, with chimpanzees displaying less resilience to selective logging (Hardus,
Lameira, Menken, & Wich, 2012). It is therefore important to understand the geographical variation of orangutan populations to logging activities by studying individual responses to the types of disturbances.
Logging and Orangutans
Multiple studies have been conducted on the effects of logging on orangutan populations, but have yet to lead to a clear picture of these influences (Marshall et al.,
2006). Under various logging conditions, the effect appears to differ with findings of decreases in densities (Felton, Engstrom, Felton, & Knott, 2003; Johnson, Knott,
Pamungkas, Pasaribu, & Marshall, 2005), increases in density (Russon, Erman, &
Dennis, 2001), and no effect (Knop, Ward, & Wich, 2004). Understanding these data is also influenced by variation in a multitude of other factors such as habitat type, habitat
58 quality, population density prior to logging, how often the forest had been logged, and how long ago it had been logged, in addition to variation between species and subspecies
(Marshall et al., 2006). Previous studies on orangutans and logging have focused mostly on Bornean orangutans, and more specifically on the subspecies P. p. morio of East
Kalimantan and Sabah and less on the other subspecies P. p. pygmaeus and P. p. wurmbii
(Hardus et al., 2012). Though that may be the case, virtually all studies conducted have focused mostly on orangutan densities following logging activities, with a few studies on the impact of logging on food resources (Hardus et al., 2012). Prior to the research conducted by Hardus et al. (2012), there had been no systematic research conducted on the influence of logging on orangutan daily behavior after logging, and therefore there is little understanding of the impact of logging on individual orangutans as previous data reflects the influence on populations as a whole (Hardus et al., 2012).
Logging has been shown to affect orangutans negatively, though there are significant variations between studies (Marshall et al., 2006). Important foods such as lianas and figs that live on large trees are destroyed by logging activities (Leighton &
Leighton, 1983, as cited in Marshall et al., 2006). Strangling figs are an important part of the orangutan diet due to their availability when other fruits are scarce, but they tend to prefer large trees that are also preferred by loggers (Felton et al., 2003). Logging activities causes the loss of large strangling figs that are highly productive and also causes the loss of large fruit trees; this in addition to canopy disruptions, should result in a habitat that provides lower energetic returns (Felton et al., 2003). In Borneo, when fruits are limited, orangutans will feed most commonly on cambium and leaves, but when fruits are more available, they will feed almost entirely on these fruits (Knott, 1998).
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Cambium has been shown to provide fewer calories than fruits (Knott, 1998). Logging activities breaks up the forest canopy and increases locomotor costs (Rao & van Schaik,
1997, as cited in Marshall et al., 2006). Orangutan densities decline in logged forests because of the loss of large trees and therefore the loss of available fruit (Husson et al.,
2009). The fragmentation of forest canopies due to logging that leads to higher energetic costs for orangutans is also blamed for the decline in populations of orangutans (Husson et al., 2009). Orangutans are known to adjust time spent feeding, dietary composition, and food selectivity due to fluctuations in fruit availability (Galdikas, 1988; Leighton,
1993; MacKinnon, 1974; Mitani, 1989; Rodman, 1997, as cited in Knott, 1998).
The majority of studies on logging activities and the impact on orangutans show that orangutan densities are lower in moderately and heavily logged forests as opposed to unlogged forests of similar quality (Husson et al., 2009). There are various reasons leading to the degree of population decline of orangutans under logging conditions
(Husson et al., 2009). How well orangutans can survive in logged forest, the type and intensity of logging, increased accessibility to forests by hunters, and elapsed time since logging activities, all contribute to how populations respond to logging (Husson et al.,
2009). Logging also impacts surrounding areas, as orangutans have been shown to move away and take refuge from disturbance due to logging and overcrowded nearby areas, putting pressure on the carrying capacity of that forest (Husson et al., 2009). One such study shows that a population of orangutans was reduced by one-sixth due to logging activities but a nearby forest of less quality doubled during the same time period (Husson et al., 2009). Overcrowding due to logging activities appears to be an issue primarily
60 faced by Bornean orangutans, as similar activities have not produced the same results in studies in Sumatra (Husson et al., 2009).
Illegal Hunting
For the past 80 years, it has been illegal under Indonesian law to kill orangutans but this law is not enforced nor do those who hunt orangutans illegally get prosecuted
(Wich et al., 2012). Logging concessions have opened up opportunities for hunting in previously less accessible forests (Husson et al., 2009). Hunting for the pet trade and for meat for cultural reasons has been occurring throughout the mid to late twentieth century
(Husson et al., 2009). In areas that once supported naturally occurring small populations of orangutans these populations have now likely been hunted to extinction (Husson et al.,
2009). Ecological and topographic factors influence populations of orangutans however anthropogenic threats such as hunting and logging are the major forces behind the decline of orangutan density and distribution (Wich et al., 2012). Conflict- motivated killings of orangutans also occur (Davis et al., 2013). Orangutans cause conflicts in both Sumatra and Borneo with farmers and oil palm plantations (Davis et al., 2013). In a survey conducted by Meijaard et al. (2011) in Kalimantan Borneo, killing rates of orangutans were found at higher rates than previously thought and are believed to pose a serious threat their continued existence throughout this region (Meijaard et al., 2011). The continued survival of orangutans in human dominated areas is not likely if hunting of orangutans persists (Wich et al., 2012) and results from studies of orangutan hunting and killing in Kalimantan Borneo reveal that habitat protection alone is not sufficient in protecting certain orangutan populations into the future (Davis et al., 2013).
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Palm Oil and Oil-Palm Plantations
In Malaysia and Indonesia significant revenue is generated through international trade of timber, oil, tobacco, and agricultural products such as palm oil (Husson et al.,
2009). Significant portions of forests in Sumatra have been converted to oil-palm plantations, in Borneo many lowland areas have also seen establishments of large oil- palm plantations, and oil-palm is grown in much of the coastal regions of Sabah and
Sarawak (Husson et al., 2009).
For conservation strategies, understanding the overlap between orangutan habitat and land-use categories such as protected areas, plantations, and logging concessions is necessary (Wich et al., 2012; Wich et al., 2016). In Borneo, an orangutan distribution map was modeled that covers 21% of the island’s entire land mass (Wich et al., 2012).
The overlap between land-use categories and the orangutan distribution range show that
22% of the orangutan population in Borneo is found in protected areas but 29% is found within forest concessions, 19% in undeveloped oil-palm plantations, 6% in plantation concessions, and 24% of the distribution of orangutans is found outside of both protected areas and outside of concessions (Wich et al., 2012). It is estimated that if all forest areas outside of both concessions and protected areas are destroyed, a further loss of 24% of the orangutan population would occur (Wich et al., 2012). In Sumatra, understanding the issues surrounding land-use practices and this population is also of significant concern
(Wich et al., 2016). The Sumatran species is seriously threatened due to forest loss and poaching, and predictions of forest loss into the future results in a loss of 4,500 individuals by 2030 (Wich et al., 2016). For both species on orangutan, future decimation of orangutan habitat needs to be avoided and land-use practices must be
62 carefully planned and managed in order for these species to survive into the future (Wich et al., 2012; Wich et al., 2016).
Vulnerability of Female Orangutans
Female orangutans are believed to be more vulnerable to habitat disturbance than males (Felton et al., 2003; Knott, 1998). Even when a female home range has been lost to deforestation, resident females refuse to leave (Knott et al., 2008; Singleton et al.,
2009). Bornean female orangutans are more severely impacted by periods of low fruit abundance than males (Knott, 1998). This is likely due to the high costs of reproduction in terms of lactation, infant carrying, and decreased foraging efficiency (Knott, 1998).
Explanations for why females are more significantly impacted by logging activities than males are: 1) Females have been found to be less able than males to efficiently travel through logged forest (Rao & van Schaik, 1997, as cited by Felton et al., 2003); 2)
Females and their offspring are more at risk of predation on the ground than males and will therefore avoid forests where they must go to the ground to travel (Galdikas, 1988, as cited by Felton et al., 2003); and 3) Costs of reproduction would lend support that selectively logged forests are less ideal for adult females (Felton et al., 2003).
Conservation Efforts
In Borneo, orangutans live in areas that are legal timber concessions, over 75% in
Kalimantan and over 60% in Sabah (Wich et al., 2008). Hence there is a need for forest management practices that enable orangutans to continue to live in these areas that have less of an impact on populations (Wich et al., 2008). There is an opportunity for biodiversity conservation in forests that are being maintained for timber production
(Meijaard et al., 2005). For chimpanzees, gorillas, and orangutans, improvements are
63 needed with the current conservation methods being employed, and one such improvement being explored is the possible balance between logging activities and conservation (Wich et al., 2008).
With orangutan populations dwindling, and conservation efforts working to find other avenues for success, understanding how orangutans cope with disturbed and degraded habitat is exceptionally important for their continued survival. In Borneo,
Indonesia, the loss of forest, forest degradation, and hunting are all having increasing negative effects on wildlife with many species now threatened (Meijaard et al., 2005).
All species are facing major threats, mostly due to anthropogenic factors. It has been suggested that the Sumatran orangutan could be the first great ape to go extinct (Wich et al., 2008). However, it is possible that the Bornean population is the more at risk
(Russon et al., 2001). Though the population numbers would suggest that Sumatran orangutans are at higher risk of extinction, the Bornean orangutan populations are extremely fragmented, isolating populations from one another (Russon et al., 2001), and exposing them to more risk of population decline than would be expected using numbers alone.
Due to the many threats orangutans face in their natural habitat, the significant loss of viable forest, significant declines in populations, and hence the number of orangutans now being cared for and coming into rescue and rehabilitation centers, the need to better understand issues these species face in captive settings is becoming even more critical.
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CHAPTER 7
ORANGUTANS IN CAPTIVE ENVIRONMENTS IN-SITU AND EX-SITU
Rehabilitant Orangutans/Numbers
Continued anthropogenic threats to wildlife and their natural habitats have led to increases in wildlife conflict and displacement of wild animals (Trayford & Farmer,
2013). This has also contributed to the commercial trade in animals and to poaching activities, both which are directly associated with increases in the number of displaced animals needing placement in sanctuaries and rehabilitation centers (Trayford & Farmer,
2013). A survey of native primate sanctuaries and represented species within these facilities revealed that there are 70 facilities worldwide caring for an excess of 6,000 primates (Trayford & Farmer, 2013). Reintroduction for animals housed within these sanctuaries is often the ultimate goal (Banes, Galdikas, & Vigilant, 2016). However, animals designated as suitable for release represent less than half of the sanctuary population (Trayford & Farmer, 2013).
A total of 1516 orangutans of both species currently reside in sanctuaries throughout Indonesia and Malaysia (Trayford & Farmer, 2013). Other great ape species residing in sanctuaries in-situ include: chimpanzees (Pan troglodytes) 963; bonobos (Pan paniscus) 72; and gorillas (Gorilla gorilla) 106 (Banes et al., 2016; Trayford & Farmer,
2013). Orangutan rehabilitation efforts have been in operation for more than 40 years, and during this time twelve projects have been started with eight of these continuing
65 today (Russon, 2009). Most orangutans arriving to these centers are victims of habitat loss or hunting (Russon, 2009). Lifelong care is also necessary for individual orangutans who are not suitable for reintroduction, and the numbers of these individuals have increased in rehabilitation centers (Rosen & Byers, 2002).
More sanctuaries and populations within existing sanctuaries are expected to increase given the number of anthropogenic threats many species face (Trayford &
Farmer, 2013). These sanctuaries are a common strategy in use to provide for the number of primates needing care and offer potential release opportunities or long-term care, or a combination of the two (Trayford & Farmer, 2013). Opportunities need to be found that allow for the best outcomes for each individual with respect to welfare
(Trayford & Farmer, 2013). There is a need to support in-situ sanctuaries and their progress in standards to successfully reach welfare and conservation goals (Trayford &
Farmer, 2013). There are two new populations of Sumatran orangutans being established in Sumatra though reintroduction efforts, with over 260 individuals having been reintroduced, with the goal of establishing wild and self-sustaining populations to safe- guard against the loss of other wild Sumatran populations (Singleton et al., 2016).
The Association of Zoos and Aquariums (AZA)
The Association of Zoos and Aquariums (AZA) is a 501(c)3 non-profit organization that works towards advancing zoos and aquariums with respect to conservation, education, science, and recreation (AZA website). The AZA is a professional organization that represents accredited aquariums and zoological parks and other certified related facilities (AZA website/Sustainability Partner Policy and
Application). The AZA is an independent accrediting organization for high quality zoos
66 in the United States and the world, holding them to high standards of care (AZA website). Working towards the best practices in animal population management, the
AZA works to elevate professional standards that support the continued development of high quality zoos and aquariums (AZA website/Sustainability Partner Policy and
Application). Acting as centers of excellence in wildlife conservation and public education, AZA accredited facilities work towards enhancing the public’s connection with animals and nature (AZA website/Sustainability Partner Policy and Application).
The AZA recognizes the importance of the health of ecosystems, takes responsibility for the survival of species, contributes to research, and promotes a high standard of animal welfare and care while managing small wildlife populations (AZA website/Sustainability
Partner Policy and Application).
Currently, the AZA represents over 230 facilities in the United States and abroad and are held to the highest standards in animal care (AZA website). The trained professionals working in AZA accredited facilities care for over 800,000 animals and are considered experts in animal care and welfare (AZA website). AZA accredited facilities have over 183 million visitors each year and are effective in teaching the public about science and connecting them to nature (AZA website). These institutions also contribute millions of dollars that go towards conservation, scientific research, and educational programs (AZA website). AZA accredited institutions make conservation a priority and every year $160 million is dedicated to field conservation efforts that support 2,600 projects throughout 130 countries worldwide (AZA website). In addition, $7 million support over 375 projects globally supported by the AZA Conservation Grants Fund
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(AZA website). AZA accredited institutions work towards protection of threatened and endangered species (AZA website).
The Orangutan Species Survival Plan (SSP)
The AZA Species Survival Plan (SSP) is an animal management, breeding, and conservation program that entails the cooperation of accredited institutions working towards self-sustaining and genetically diverse animal populations and currently represents over 500 species (AZA website). These SSP programs focus on threatened or endangered species working to cooperatively manage these small populations (AZA website/Sustainability Partner Policy and Application). Conservation and cooperative animal management is named one of the main goals of the AZA (AZA/Policy for Full
Participation in the Species Survival Plan Program). The AZA Board of Directors recognizes that the survival of zoological parks and aquariums and their animal collections rely on cooperative animal management practices and that AZA facilities need to be committed to SSP partnerships, animal management, conservation, and public education (AZA/Policy for Full Participation in the Species Survival Plan Program).
The Orangutan SSP began in 1988 and is composed of a group of dedicated professionals that work together to meet common goals (Orangutan SSP website). The
Orangutan SSP work towards maintaining and preserving the demographic and genetic health of the captive population, making advancements in their care, supporting research activities that promote knowledge in understanding orangutans and their care, and working together with other organizations towards the improvement in the lives of both captive and wild orangutans (Orangutan SSP website). The SSP works closely with respected field professionals and provides guidance to zoos housing orangutans to work
68 cooperatively in providing the best environments possible for these orangutans
(Orangutan SSP website). The main goal of an SSP is ensure the long-term survival of species in captive environments by working in cooperation with other institutions and treating the entire population as one gene pool or as a single reproductive unit to maintain genetic diversity (Orangutan SSP website).
The Orangutan SSP also partners with a number of other programs: AZA which is the governing body; AZA Orangutan SSP Conservation Education website, which works to help raise awareness of the plight of the orangutan; Ape TAG, is the Taxon Advisory
Group for the apes in AZA zoos; Chimpanzee SSP; Bonobo SSP; Gorilla SSP; and the
Gibbon SSP (Orangutan SSP website).
Captive Orangutans and Management
Globally, orangutans in captive environments have been managed as two distinct species, genetically separate breeding populations, representing both the Bornean and
Sumatran orangutan (Orangutan SSP website). A third population is also represented in the captive population, hybrid orangutans, which are the cross between the two species
(Orangutan SSP website). It is unclear at this point how the newly classified orangutan species, P. tapanuliensis, is represented in these populations. It was not until late in the
1980s that a better understanding of species distinctions were made among the genus
Pongo leading to a number of orangutans being born of hybrid status (Orangutan SSP website). A policy was put in place in 1985 by the Orangutan SSP to no longer breed
Bornean and Sumatran orangutans together, as other captive management programs in
Europe, Australia, New Zealand, Southeast Asia, and Japan adopted similar policies at this time (Orangutan SSP website). These hybrid orangutans represent a non-breeding
69 population and have been recommended for sterilization to prevent continued hybridization (Orangutan SSP website). This hybrid population is managed and housed in exactly the same way that the Bornean and Sumatran population are managed and are considered an important part of the overall captive orangutan population as they continue to hold significance as social partners to other orangutans (Orangutan SSP website) and are valued as individuals among their respective institutions.
Orangutan husbandry refers to how the physiological, biological, psychological, and their social needs are meet and addressed and their welfare is the results of how these needs are met (Orangutan SSP website). The physical health and psychological well- being of orangutans require that appropriate nutrition, exercise, social groupings, veterinary care, and environmental conditions are provided and that motivational needs, with control and choice, environments designed for their adaptations, and cognitive opportunities are addressed (Orangutan SSP website).
To meet high levels of welfare the AZA’s Animal Welfare Committee outlines six programs that work toward this outcome: Enrichment; Habitat; Nutrition; Research;
Health; and Training (Orangutan SSP website). The employment of these programs describe animal husbandry, by making use of the knowledge of natural history and individual history to offer high quality care (Orangutan SSP website). Additionally,
Animal Care Manuals have been created through collaborative efforts with Taxon
Advisory Groups (TAGs), SSPs, The Animal Welfare Committee, and members of AZA, that reflect years of animal care expertise and scientific information that can be used as guidelines to help identify physical and biological needs of animals (Orangutan SSP website).
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The North American Orangutan Species Survival Plan (SSP) and zoological institutions that house these species also work to educate the public regarding threats these species face and support various conservation and research projects that are working to promote these species survival into the future. Unfortunately, there are a number of health challenges that face the captive orangutan population, and hence, influence the achievement of a self-sustaining population (Lung, Smith, & Perkins,
2012). In 2011, the Orangutan SSP conducted a mortality and population review of
North American captive orangutans and found that cardiac, respiratory, renal, and reproductive disease negatively affect this population (Lung et al., 2012). This has led to reduced numbers of healthy orangutans within the breeding population and is therefore negatively influencing the viability of this population (Lung et al., 2012).
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CHAPTER 8
ORANGUTANS AND RESPIRATORY DISEASE
Orangutans and Air Sacculitis
The Orangutan SSP 2012 Health Survey conducted on the North American population asked zoological institutions to identify the most serious health problems facing captive orangutans, and respiratory infections were ranked number one. Air sacculitis is a common form of respiratory disease in captive orangutans (Herrin,
Spelman, & Wack, 2002; Orangutan SSP Health Survey, 2012; Zimmermann et al.,
2011). Air sacculitis is associated with significant levels of morbidity and mortality among captive orangutans (McManamon et al., 1994; Zimmerman et al., 2011).
Treatments for these infections can more complicated in great apes due to the structure of their air sacs that extend into the axillary region, and among male orangutans can also extend around the mandible towards the ears and cheeks (Lowenstine & Osborn, 2012).
Air sacs are most developed in great apes but are a common anatomic feature in many other primate species (Cambre et al., 1980). Air sacculitis has been observed in a number of primate species in the wild, in captive environments, and in rehabilitation centers. Air sacculitis has been described in wild mountain gorillas (Gorilla gorilla beringei); a silverback (Hastings, 1991) and an adult female who had recently given birth (Palacios et al., 2011). Both of these cases were reported during respiratory outbreaks among their associated groups. Air sacculitis has also been described in captive chimpanzees (Pan
72 troglodytes) (Kumar, Fox, Owston, Hubbard, & Dick, 2012; Strobert & Swenson, 1979) and bonobos (Pan paniscus) (Herrin et al., 2002). Other primate species that have been reported to have air sacculitis are baboons (Papio spp.) (Gross, 1978; Kumar et al.,
2012), owl monkeys (Aotus trivirgatus) (Giles, Hildebrandt, & Tate, 1974), pig-tailed macaques (Macaca nemenstrina) (Brown & Swenson, 1995), and a silver leaf monkey
(Trachypithecus cristatus ssp ultima) (Luz, Oh, Martelli, Oh, & Furley, 2005). Air sacculitis has also been reported in juvenile rehabilitant orangutans, all having once been kept illegally as pets then confiscated and transferred to a quarantine and rehabilitation facility (Lawson, et al. 2006). At this particular quarantine and rehabilitation center, air sacculitis is reported to be an important issue facing juvenile orangutans and requires frequent surgical intervention (Lawson et al., 2006).
Captive orangutans appear particularly susceptible to air sacculitis (Cummins,
1985). Over 40% of responding North American zoological institutions reported having diagnosed throat sac infections in orangutans within the past 10 years (Orangutan SSP
Health Survey, 2012). Over 30% of these responding institutions also reported diagnosing pneumonia and sinusitis, and over 20% reported diagnosing bronchiectasis/chronic bronchitis within the past 10 years (Orangutan SSP Health Survey,
2012). The pathogenesis and etiology of air sacculitis and sinusitis among orangutans are not well understood (Zimmerman et al., 2011). It has been suggested that possible fecal contamination in the captive environment is a predisposing factor of air sacculitis because reports of air sacculitis in wild orangutans are absent from the literature (Cambre et al.,
1980; Lawson et al., 2006). It has also been suggested that at least in one case of air
73 sacculitis, obesity and stress of pregnancy could have played a role in the onset of illness
(Cambre et al., 1980).
Project Significance, Objectives, and Preliminary Research
Significance of Project
Given the high incidence of respiratory disease in the captive orangutan population, both in North America and abroad, gaining a better understanding of the predisposing factors that influence these diseases is crucial. This information will be used by animal care providers, managers, and zoological institutions to identify high risk individuals who can then be monitored more closely and be treated earlier if necessary.
Air sacculitis is not easily detectable in the early stages, making early diagnoses challenging (Cambre et al., 1980). Successful treatment of this life-threatening infection depends heavily on early recognition (Cambre et al., 1980). Clinical signs of this disease are generally subtle and when more obvious signs appear serious infection could already be present (Cummins, 1985). Early detection of disease is a challenge and careful observations by zoo staff for the early warning signs of disease are crucial (Cambre et al.,
1980). This study will help elucidate potential risk factors that will assist in the early detection of respiratory disease.
Project Objectives
The research conducted by Zimmermann et al. (2011) has provided valuable insight into the understanding of the risk factors involved in the development of respiratory disease in orangutans. Through a similar study of the North American orangutan population, it will be possible to determine if there are similar patterns between these populations. If similarities are found, this will enhance our knowledge on the
74 factors that influence respiratory disease in orangutans and will provide valuable information to zoological institutions that will assist in the management and care of these species. The proposed project is designed to uncover these potential patterns and to elucidate other potential factors related to these diseases.
This project investigates if there is a difference in the prevalence of respiratory disease in the North American orangutan population between the two species of orangutan, between the sexes, between age brackets, and if developmental status plays a role. Another potential risk factor is obesity, and this project investigates if this plays a role in the onset of respiratory disease. The project also addresses if there are geographical regions within the North American orangutan population that show a higher preponderance for the incidence of respiratory disease. The prevalence of different forms of respiratory disease is investigated. Housing conditions and basic husbandry practices are also investigated for a potential link to respiratory illness. In addition, stress events, family history, and rearing history are also explored.
Preliminary Research
With approval by recommendation of the Orangutan SSP Steering Committee, I designed and sent out a survey to North American zoological institutions housing orangutans in 2008. Responses from various institutions were helpful in understanding what questions should be asked, and which questions could be removed from the survey.
Having participated in the 2012 Orangutan SSP Health Workshop, additional information was acquired and the need for the survey was again made apparent. Using the original respiratory survey as a pilot study, having worked on other drafts in the past with the assistance of the Orangutan SSP and SSP veterinary advisors, this study addresses some
75 of main issues surrounding the prevalence of respiratory disease in the North American zoological population of orangutans. This project also serves as a starting point to where future projects can focus by providing information that will guide these future projects.
Factors that Influence Respiratory Disease
Predisposing Factors for Respiratory Disease
In a study conducted by Zimmermann et al. (2011), predisposing factors for, and the prevalence of upper respiratory disease in zoos throughout Europe were investigated.
Of the 20 zoos that were visited by the authors, respiratory disease occurred in 15. The authors used two categories for the presence of respiratory disease; chronic respiratory signs and air sacculitis. Results from this study found that Bornean orangutans showed a higher propensity for chronic respiratory signs (13.8%; n = 11) than Sumatran orangutans
(3.6%; n = 4), though no difference was found between the species for the presence of air sacculitis. Male orangutans (15.8%; n = 12) showed these respiratory signs more often than did females (3.9%; n = 3) with no difference found between the sexes for air sacculitis. Air sacculitis was more prevalent among hand-reared orangutans (21%; n =
21) than mother-reared orangutans (5%; n = 5), but no difference was found between these categories with chronic respiratory signs. Orangutans with respiratory disease were more often related to other orangutans with respiratory disease (93%; n = 14) than healthy orangutans (54%; n = 42). Environmental conditions were also studied, however these showed no significant influence on the presence or absence of disease. Signs of chronic respiratory disease appeared at an earlier age than did air sacculitis, suggesting that chronic respiratory signs might be a precursor to air sacculitis (Zimmermann et al.,
2011). In the study conducted by Lawson et al. (2006), ages of the juvenile orangutans
76 were undetermined due to the fact that they had been illegally held, and they reported air sacculitis in both females (n = 9) and males (n = 5). There have been other reports of sex differences in the prevalence of air sacculitis in other species. Kumar et al. (2012) found that among the 37 cases of air sacculitis among baboons in their study, 36 were male and only one was female. In addition, of the 7 cases of air sacculitis among the chimpanzees in their study, 6 were male and one was female.
Other Risk Factors/Obesity
One possible risk factor for respiratory disease in captive orangutans is obesity.
Orangutans have a propensity for obesity in captive environments. It has been suggested that obesity in primates could be a risk factor for respiratory disease because it promotes sedentary behavior and hence precludes the ability for fluid to properly flow from the air sac (Cambre et al.,1980; Gross, 1978; Zimmermann et al., 2011). The observation has also been made that Bornean orangutans are more obese than Sumatran orangutans in the captive environment (Courtenay, Groves, & Andrews, 1988; Zimmermann et al., 2011).
Male Bornean orangutans have been shown to have a higher propensity for respiratory disease in captivity (Zimmermann et al., 2011). The higher potential incidence for
Bornean orangutan obesity as compared to Sumatran orangutans in captive environments could be due to the ecological conditions they have evolved to cope with. Sumatran forests are known to be more productive, by producing higher quality foods and more available high-quality foods, than forests in Borneo (Wich et al., 2009). Diets are similar in amounts of fruit between the islands, however, Bornean orangutans have a higher variation of fruit in their diet, eat more inner bark, and have more variation within their population (Wich et al., 2009). For Sumatran orangutans, that means more insects and
77 figs, but for Bornean orangutans that means a heavy dependence on fibrous foods such as inner bark (Taylor, 2009). For P. p. morio and for P. p. wurmbii, they suffer more from severe shortages in high quality foods than other orangutans (Taylor, 2009). In north east
Borneo and in south west Borneo, orangutans tend to rely more heavily on fall back foods such as leaves, wood foods, and other types of vegetation which has been shown to provide less energy than fruits (Taylor, 2009). Because orangutans in captive environments receive similar nutrition between the species, it is possible that Bornean orangutans hold on to food stores more effectively than Sumatran orangutans, hence making them more prone to storing fat, falling in line with the thrifty genotype hypothesis (Neel 1962).
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CHAPTER 9
METHODS
Institutional Animal Care and Use Committee (IACUC) Process/Approval
An application was submitted through the California State University Fullerton
Institutional Animal Care and Use Committee (“CSUF IACUC”) for the current research project titled “Respiratory Disease in the North American Captive Orangutan
Population”. The application and protocol for this study were reviewed by the CSUF
IACUC and approved on June 24, 2016. The approval for this project was valid for one full year, expiring June 24, 2017. One month prior to the expiration of this approval, the project and protocol can be extended for one full additional year with the submission and approval of a continuation form. Therefore, an extension application was submitted in
May of 2017. This extension application was waived as current CSUF IACUC policy no longer requires approval for research of this nature.
The type of research in the protocol was described in the application as a behavioral study, and “other”, listed as a survey. Other information provided on the application included the species to be used, potential number of subjects, ages of individuals, sex, and the conservation status of the species. Questions were also answered within the application regarding the scientific significance of the project, the objectives, and why the species used are appropriate for this study. Other questions addressed in the application were the educational significance of the project, the
79 educational objectives, and the appropriateness of the species being studied. Within the application, the source of the study population was outlined as well as the nature of the data collection methods. A literature review was also outlined in the application to justify the use of this species for this particular study and to identify various search methods used for background research on the subject matter. Information was also provided within the application describing some similar research on a different population of orangutans, and why this study could provide valuable comparable research. Documents were attached to the application to provide information on the nature of the questions included in the survey. In addition, the approval letter from the
Association of Zoos and Aquariums (AZA) Orangutan Species Survival Plan (SSP) was also included for reference.
It is mandated by federal regulations that the university animal care and use committee must review every research project that will use vertebrate animals in their research. It is advised, once a protocol is approved, that the research guidelines described are closely followed. The current research project is completely non-invasive and asks
AZA accredited institutions in North America that currently house orangutans to provide information on both living and deceased orangutans. In addition, the North American
Studbook data are also used to provide historical information.
Orangutan Species Survival Plan (SSP) Approval and Endorsement
A research proposal for this project was submitted to the Orangutan Species
Survival Plan (SSP) for approval prior to any research conducted and prior to the IACUC application submission and subsequent approval. The Orangutan SSP Steering
Committee members reviewed the research proposal for this project and voted to endorse
80 the proposal. After approval, the proposal was distributed to Institutional Representatives
(IRs) through one of the Orangutan SSP list-serves to encourage member institutions to participate in this project. Contact information was also provided to allow for individual institutions to be contacted if needed. In addition, a synopsis of this project was provided to the Orangutan SSP Social Media Coordinator so the project description could be included on the Orangutan SSP website under “Currently Supported Projects.” The SSP approval and endorsement for any species is often a prerequisite for institutional support of any given project through each individual institutional research review process.
Though SSP endorsement does not require that zoos participate, this support lends necessary significance and importance to given projects. One individual institution requested an additional AZA research request application be submitted. This form was completed and submitted and was approved by the requesting institution.
Development and Dissemination of Survey
The survey was developed through the survey site Survey Monkey and was designed to be completed by appropriate zoo staff. The aim of the survey was to identify factors that influence the presence of respiratory disease in the North American captive orangutan population. Questions asked included individual orangutan and background information, including developmental questions. Also included were questions regarding family history and basic husbandry practices. Body condition information and activity level questions were included. Some of these questions were subjective yet important to gaining some insight into the relevance of this potential factors. Those who completed this survey for an individual orangutan who has had respiratory problems were also asked questions regarding respiratory health history
81 and questions regarding symptoms of respiratory disease. These sets of questions were automatically be skipped for those who completed a survey for an orangutan who has not had problems with respiratory disease. Those who completed the survey needed access to this information and corresponding data on age and dates.
Additionally, current weights and the five most recent previous weights were requested. Understanding that there are likely multiple weights on individual orangutans, it was requested that actual weight documents in lieu of filling out this portion of the survey be uploaded to the survey. To compare data, it was necessary to have data on healthy orangutans with no history of respiratory disease. The survey was significantly reduced in length for those providing data on individuals without respiratory disease, and these data are also of great comparative value. Those institutions with orangutans with no history of respiratory disease were highly encouraged to complete the survey. It was estimated that approximately 15-20 minutes were needed to complete the full survey but it was also stated that it would likely depend on access to some of the information described above. For those completing the survey for orangutans without respiratory disease, the survey was estimated to take about 10 minutes to complete. The survey was designed to be completed for each individual orangutan.
The main study group for this research project is the North American captive orangutan population housed in facilities accredited by the Association of Zoos and
Aquariums (AZA). Both species of orangutan are represented in this project, as well as hybrid orangutans. Data on both living and deceased individuals are incorporated into this study. The survey was sent out to all North American AZA accredited facilities
82 housing orangutans through professional list serves. The survey was made available for completion for approximately 6 months, allowing ample time for maximum results.
Data Management
Individual surveys needed to be sorted through to ensure that there were no duplicates, or any surveys that were incomplete or otherwise void. On the first pass, surveys were sorted through looking for incompletes. Surveys were deleted if they were partial responses, likely those curious to review the survey prior to full completion. The second pass through the individual surveys began by finding surveys that omitted names of individual orangutans, as this would likely be completed for any survey justifying inclusion into analysis. Five surveys were deleted at this time, though two surveys needed further investigation. The third pass was made to follow up on previous questionable surveys. Surveys were deleted at this time for various reasons; for example, some were duplicates for individuals, and others were incompletes. The fourth pass was completed to look through the remaining incomplete surveys to determine if they contained enough data for analysis. Survey Monkey will not denote a survey complete unless the survey taker presses the done button at the end of the survey. It will also not denote the survey as complete if the survey taker does not answer the logic question asking whether the individual orangutan has or has had respiratory disease. Again, duplicate surveys and incompletes were deleted where appropriate and surveys were deemed complete for others that contained enough data for analysis in this project. On the fifth pass, all surveys were assessed again to ensure no duplicates were incorporated into the data set. This was done by using each individual orangutan’s International
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Studbook Number (ISB) and sorting data in ascending order to ensure there were no duplicate surveys. Four more duplicate surveys were found at this time.
Data were exported from Survey Monkey into SPSS at this time. New variables were created for coding throughout the spreadsheet. Each AZA accredited zoo currently housing orangutans was numbered alphabetically. Additional zoos were coded as were other locations that were referenced in historical data and in transfer data which were then added to this list. Referenced cities were numbered alphabetically at this time.
These numbers were used to code for both the cities and the zoos referenced within these data. The variable names were changed within SPSS in accordance to the data they referenced. Using the International Orangutan Studbook, I included Studbook numbers for individual orangutans that had this information missing. Using day of birth, current location, species, and sex, these orangutans and their associated ISB numbers were cross- checked. A dozen other ISB numbers were double checked to ensure accuracy. Also by using the ISB, some missing data were collected. Two dates of birth, one place of birth, and one current location. Though the survey requested that dates be filled out in a specific format, not all completed their dates in this framework. Therefore, dates not properly formatted were reformatted. For number of moves to other facilities, the ISB was utilized again to verify number of moves in addition to sex, species, date of birth, and ISB number for all surveys and individual orangutans represented in these data.
Studbook and Historical Data/Keyword Searches
The International Studbook Keeper ran a number of keyword searches through the
ISB dataset with respect to respiratory disease. A number of keywords were searched referencing respiratory disease, such as; respiratory disease, air sacculitis, pneumonia,
84 throat sac infections, etc., however, due to the lack of specific institutional approval these data are not used in this data set.
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CHAPTER 10
RESULTS
Current North American Orangutan Population and Research Population
Currently, there are 53 zoological institutions that house orangutans throughout the United States, Canada, and Mexico that are accredited by the Association of Zoos and
Aquariums (AZA) and are therefore participants in the North American Orangutan SSP
(Orangutan SSP website). Within this orangutan population, there are a total of 223 individual orangutans including 129 (57.85%) females and 94 males (42.15%). Bornean orangutans are represented by a total of 96 individuals (43.05%) with 54 females and 42 males; Sumatran orangutans are represented by a total of 87 individuals (39.01%) with 53 females and 34 males; and hybrid orangutans are represented by a total of 40 individuals
(17.94%) with 22 females and 18 males (M. Elder, personal communication, March 8,
2017) (see Table 1).
Data collected through Survey Monkey for this research reflect a study population of 154 individual orangutans comprising 81 females and 74 males; Bornean orangutans are represented by 35 females and 28 males, Sumatran orangutans are represented by 32 females and 31 males, and hybrid orangutans are represented by 14 females and 14 males
(see Table 2). Of the 154 (missing = 1) orangutans in the current study population, 128 are currently living and 25 are deceased (see Table 4). Of the 53 AZA accredited institutions currently housing orangutans, a total of 41 (77.36%) institutions completed
86 one or more surveys for this study (see Appendix A), with 12 (22.64%) institutions not contributing to these survey data (see Table 3).
Table 1. Demographics of the Current North American Orangutan Species Survival Plan Population
Female/% Male/% Total Percent Bornean 54 (24.22%) 42 (18.83%) 96 43.05% Sumatran 53 (23.77%) 34 (15.25%) 87 39.01% Hybrid 22 (9.87%) 18 (8.07%) 40 17.94% Total 129 94 223 100% Percent 57.85% 42.15% 100% Note: Data provided by Megan Elder, International Studbook Keeper March 8, 2017
Table 2. Demographics of the Current Research Population
Female/% Male/% Total Percent Bornean 35 (22.72%) 28 (18.18%) 63 40.91% Sumatran 32 (20.78%) 31 (20.13%) 63 40.91% Hybrid 14 (9.09%) 14 (9.09%) 28 18.18% Total 81 74 154 100% Percent 52.60% 47.40% 100%
Figure 3. Current North American Figure 4. Current research Orangutan SSP population by sex population by sex.
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Figure 5. Current North American Figure 6. Current research Orangutan SSP population by species. population by species.
Table 3. Number of AZA Institutions Completing Surveys
Institutions Completing One or Institutions Not Total Number of AZA Institutions More Surveys Included with Orangutans Number 41 12 53 Percent 77.36% 22.64% 100%
Table 4. Orangutan Living or Deceased According to Species
Living Deceased Total Bornean 54 9 63 Sumatran 48 14 62 Hybrid 26 2 28 Total 128 25 153 Percent 83.66% 16.34% 100%
Table 5. Orangutan Living or Deceased According to Sex
Living Deceased Total Female 71 10 81 Male 57 15 72 Total 128 25 153 Percent 83.66% 16.34% 100%
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Figure 7. Percent of current research population living or deceased.
Research Question, Hypotheses, and Predictions with Results
The focus of this research is to determine if there are certain risk factors that predispose orangutans to respiratory disease. Because orangutans appear to have a higher prevalence of respiratory disease than other primates in captive environments, determining what makes them more susceptible to these diseases is of significant value.
Results from these data reflect 32 individual orangutans having or previously had respiratory disease (see Table 6) representing 20.78% of the study population (see Figure
8).
The question, “does or did this orangutan have respiratory disease?” acted as a logic question within the survey, whereby if the responder answered yes, the survey continued with additional questions regarding respiratory disease. A total of 32 responses of yes were collected (see Table 6). If the responder answered no or unknown, the survey ended at this point excluding any additional responses. For survey responders answering yes to the above question, the following series of questions were under the heading “Respiratory Disease Health History” and “Diagnoses”. The question regarding the presence of disease was asked for under the heading “Diagnoses”; respiratory disease, air sacculitis, rhinitis, pneumonia, bronchitis, sinusitis, and other (see Table 7). A question regarding the frequency of occurrence was asked for corresponding answers (see
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Table 8). Frequency of occurrence definitions are as follows: acute is defined by “short duration/sudden/severe”; subacute is defined by “moderate/between chronic and acute”; and chronic is defined by “persistent/long-lasting”.
For diagnoses of respiratory disease, only 25 of the 32 original respondents who answered yes to the original question “does or did this orangutan have respiratory disease?” continued on through this portion of the survey. Of these 25 responses, 84% answered yes (n = 21). The most common form of respiratory disease is reported as air sacculitis with 78.3% (n = 18), with rhinitis being reported at 55% (n = 11), pneumonia reported at 50% (n = 9), sinusitis reported at 38.9% (n = 7), bronchitis reported at 27.8%
(n = 5), and other reported at 57.1% (n = 4) of the total responses per each diagnosis (see
Table 7). Figures 9 through 22 show the presence or absence of the types of respiratory disease and frequency of occurrence.
A logic question was incorporated into the current survey to allow for respondents reporting on individuals without respiratory disease to complete the survey prior to more specific questions regarding the presence of respiratory disease. At this point, only 25 of the original 32 respondents answering yes to the question “does or did this orangutan have respiratory disease?” continued to the following questions. This could reflect that some respondents were unsure of actual diagnostics performed on the individual orangutan they were reporting on, and therefore did not respond as to specific diagnoses.
Of these 25, 21 (84%) answered yes to the diagnosis of respiratory disease, 4 (16%) answered no, again likely reflecting a lack of official diagnosis. The most common type of respiratory disease diagnosis reported was air sacculitis, with 18 (78.3%) respondents answering yes to this diagnosis and 5 (21.7%) answering no, out of a total of 23
90 responses. Rhinitis, pneumonia, sinusitis, bronchitis, and “Other” followed in that order in terms of the number of diagnoses. Respiratory disease was reported as chronic 47.1%
(n = 8) out of 17 responses, more than subacute 29.4% (n = 5), or acute 23.5% (n = 4).
Air sacculitis was reported more often (n = 16) and more often as chronic 56.3% (n = 9) than other forms or diagnoses of respiratory disease. These data reflect air sacculitis is the most common form and diagnoses of respiratory disease in the study population and is more often reported as a chronic issue than acute or subacute.
Table 6. Presence or Absence of Respiratory Disease in the North American Captive Orangutan Population
Present Absent Unknown Total Respiratory Disease 32 116 6 154 Percent 20.78% 75.32% 3.90% 100%
Figure 8. Presence or absence of respiratory disease.
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Table 7. Diagnoses of Respiratory Disease and Types in the North American Captive Orangutan Population
Diagnoses Yes Percent No Percent Unknown Percent Total Responses Respiratory Disease 21 84% 4 16% 0 0% 25 Air Sacculitis 18 78.3% 5 21.7% 0 0% 23 Rhinitis 11 55% 4 20% 5 25% 20 Pneumonia 9 50% 8 44.4% 1 5.6% 18 Sinusitis 7 38.9% 7 38.9% 4 22.2% 18 Bronchitis 5 27.8% 9 50% 4 22.2% 18 Other 4 57.1% 1 14.3% 2 28.6% 7 Note: These numbers represent responses to the follow-up question regarding diagnosis of respiratory disease, only 25 responded to this question from the original 32 that responded “yes” to the presence of respiratory disease in the original presence or absence question.
Table 8. Frequency of Occurrence of Diagnosed Respiratory Disease and Types
Frequency of Total Occurrence Acute Percent Subacute Percent Chronic Percent NA Percent Responses Respiratory 4 23.5% 5 29.4% 8 47.1% 0 0% 17 Disease Air 3 18.8% 4 25% 9 56.3% 0 0% 16 Sacculitis Rhinitis 4 36.4% 2 18.2% 3 27.3% 2 18.2% 11 Pneumonia 5 45.5% 3 27.3% 1 9.1% 2 18.2% 11 Bronchitis 1 14.3% 2 28.6% 1 14.3% 3 42.9% 7 Sinusitis 0 0% 1 11.1% 5 55.6% 3 33.3% 9 Other 2 40% 2 40% 0 0% 1 20% 5
Figure 9. Presence of respiratory disease. Figure 10. Frequency of respiratory disease.
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Figure 11. Presence of air sacculitis. Figure 12. Frequency of air sacculitis.
Figure 13. Presence of rhinitis. Figure 14. Frequency of rhinitis.
Figure 15: Presence of pneumonia. Figure 16: Frequency of pneumonia.
Figure 17: Presence of bronchitis. Figure 18: Frequency of bronchitis.
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Figure 19: Presence of sinusitis. Figure 20: Frequency of sinusitis.
Figure 21: Presence of other. Figure 22: Frequency of other.
Demographics and Body Size
Factors such as body condition, obesity, and body size may influence the susceptibility of respiratory disease. Bornean orangutans are adapted for ecological conditions that make them reliant on fall back foods, whereas Sumatran forests are more productive, therefore Bornean orangutans would be expected to have a higher preponderance for obesity in captive environments and hence are expected to show a higher incidence of respiratory disease. Orangutan males often become significantly larger than females. So, if body size influences the onset of respiratory disease we would expect to see male orangutans and older mature orangutans with a higher incidence of disease. Because activity levels influence weight and body condition, then orangutans with lower activity levels will also be at a higher risk for respiratory disease.
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Hypothesis 1
If Bornean orangutans are better able to store fat, then we would expect captive
Bornean orangutans to be heavier and to have a higher risk of respiratory disease than
Sumatran or Hybrid orangutans.
Prediction 1
Bornean orangutans will be heavier and have higher risk of diagnosis than
Sumatran or Hybrids.
Hypothesis 1 is based on the differences in food distribution and abundance across space and time between species and the thrifty genotype hypothesis (Neel 1962).
Weight data were collected, and by using current weight in kilograms (KG = 2.2 lbs.) and age at measurement, species differences can be observed using loess smooth regressions for growth curves (see Figure 23). Bornean orangutans are found higher above the curve and more often than Sumatran or Hybrid orangutans, and Sumatran orangutans fall below the curve more often than Bornean or Hybrid orangutans. This chart reflects that Bornean orangutans in this study population weigh more than Sumatran or Hybrid orangutans.
Using loess smooth regressions for growth curves for male orangutans according to species, male Bornean orangutans are higher above the curve more often than
Sumatran or Hybrid male orangutans and Sumatran male orangutans fall below the curve more often than their male Sumatran and Hybrid counterparts (see Figure 24). More strikingly, female Bornean orangutans are also observed higher above the curve than
Sumatran female orangutans and Hybrid females are observed above the curve more often than Sumatran females (see Figure 25). Sumatran female orangutans are found
95 lower below the curve more than both Bornean and Hybrid female orangutans. These data reflect that Bornean male and female orangutans are heavier than both their
Sumatran and Hybrid orangutan counterparts, and that Hybrid male and female orangutans fall between Bornean and Sumatran orangutans in this study population.
Using presence or absence of respiratory disease data from the entire study population, we see that a total of 154 orangutans are represented in these data (see Table
9). Of these 154 orangutans, more Sumatran orangutans are represented with the presence of respiratory disease (n = 15) than Bornean orangutans (n = 12) or Hybrid orangutans (n = 5) (see Table 10). Though it is observed that Bornean orangutans have larger body sizes in this study population, these data do not reflect that this influences the presence or absence of respiratory disease in this study population among these species.
Figure 30 displays the number of orangutans with respiratory disease compared to those without respiratory disease by species. We can see that there is little variation between these species with respect to respiratory disease. Figure 26 displays the differences observed between species and the presence and absence of respiratory disease.
Using Kaplan-Meier curves for survival and hazard functions for male orangutans
(n = 60) by species (see Table 11) no significance is found (Wilcoxon df = 2; p = .472)
(see Table 12). Using Kaplan-Meier curves for survival and hazard functions for female orangutans (n = 76) by species (see Table 13) no significance is found (Wilcoxon df = 2; p = .981) (see Table 14). Using the age at first diagnosis for orangutans with respiratory disease and the age in years for orangutans without respiratory disease as the censored data, no statistical significance was found using Kaplan-Meier curves for survival and hazard functions for captive male orangutans (n = 60) by species. The survival and
96 hazard functions represent time to first diagnosis as the end point, not death. However, looking at the graphs for male orangutans, we do see Bornean male orangutans with a lower cumulative survival curve than for the Sumatran and Hybrid orangutans and a higher curve for cumulative hazard than for Sumatran and Hybrid orangutans (Figures 27 and 28). There were only 13 number of events, or age at diagnosis, for male orangutans in this analysis. These data reflect that there are no additional risks or hazards in developing respiratory disease for male orangutans of certain species in this study population.
Using the age at first diagnosis for orangutans with respiratory disease and the age in years for orangutans without respiratory disease as the censored data, no statistical significance was found using Kaplan-Meier curves for survival and hazard functions for captive female orangutans (n = 76) by species. The survival and hazard functions represent time to first diagnosis as the end point, not death. Looking at the graphs for female orangutans, the cumulative survival curves appear fairly even for Bornean,
Sumatran, and Hybrid orangutans (Figure 29). In the hazard function graph for females, the curve for Bornean females is higher than the curves for both Hybrid and Sumatran orangutans (Figure 30). There were only 9 number of events, or age at diagnosis, for female orangutans in this analysis. These data reflect that there are no additional risks or hazards in developing respiratory disease for female orangutans of certain species in this study population. It should be noted here that the study population includes many younger orangutans, which could potentially have resulted in the lack of statistical significance found in the Kaplan-Meier analyses.
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Figure 23. Cross sectional loess smooth of male and female orangutan body size for age by species, using current age in years and current weight in KG. Note: KG = 2.2lbs.; Bornean = black circles, Sumatran = squares, Hybrids = x.
Figure 24. Cross sectional loess smooth of male orangutan body size for age by species, using current age in years and current weight in KG. Note: KG = 2.2lbs.; Bornean = black circles, Sumatran = squares, Hybrids = x
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Figure 25. Cross sectional loess smooth of female orangutan body size for age by species, using current age in years and current weight in KG. Note: KG = 2.2lbs.; Bornean = black circles, Sumatran = squares, Hybrids = x.
Table 9. Presence or Absence of Respiratory Disease in Captive Orangutans by Species in the Study Population
Presence Absence Unknown Total Bornean 12 (7.79%) 50 (32.47%) 1 (0.65%) 63 (40.91%) Sumatran 15 (9.74%) 44 (28.57%) 4 (2.6%) 63 (40.91%) Hybrid 5 (3.25%) 22 (14.29%) 1 (0.65% 28 (18.18%) Total 32 (20.78%) 116 (75.32%) 6 (3.9%) 154 (100%)
Table 10. Respiratory Disease in Captive Orangutans by Species among the Affected Population
Presence Percent Bornean 12 37.50% Sumatran 15 46.88% Hybrid 5 15.63% Total 32 100%
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Figure 26. Number of captive orangutans with or without respiratory disease by species.
Table 11. Kaplan-Meier Case Processing Summary for Males
Censored Species Total Number Number of Events Number Percent Bornean 26 6 20 76.9% Sumatran 22 5 17 77.3% Hybrid 12 2 10 83.3% Overall 60 13 47 78.3%
Table 12. Kaplan-Meier Overall Comparisons for Males
Chi-Square Df Sig. Log Rank (Mantel-Cox) 1.272 2 .530 Breslow (Generalized Wilcoxon) 1.501 2 .472 Tarone-Ware 1.411 2 .494 p significant < .05
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Figure 27. Kaplan-Meier curves for survival functions of males by species, using age at first diagnosis and age in years for censored data.
Figure 28. Kaplan-Meier curves for hazard functions of males by species, using age at first diagnosis and age in years for censored data.
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Table 13. Kaplan-Meier Case Processing Summary for Females
Censored Species Total Number Number of Events Number Percent Bornean 33 4 29 87.9% Sumatran 30 3 27 90.0% Hybrid 13 2 11 84.6% Overall 76 9 67 88.2%
Table 14. Kaplan-Meier Overall Comparisons for Females
Chi-Square Df Sig. Log Rank (Mantel-Cox) .018 2 .991 Breslow (Generalized Wilcoxon) .038 2 .981 Tarone-Ware .004 2 .998 p significant < .05
Figure 29. Kaplan-Meier curves for survival functions of females by species, using age at first diagnosis and age in years for censored data.
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Figure 30. Kaplan-Meier curves for hazard functions of females by species, using age at first diagnosis and age in years for censored data.
Hypothesis 2
If activity levels affect the risk of respiratory disease, then we would expect to see orangutans with poor activity level scores at higher risk.
Prediction 1
Orangutans who have poorer body condition scores and are considered obese will be at higher risk for respiratory disease. Because activity level likely influences body condition then we would also expect to find that orangutans with lower activity levels having a higher incidence for respiratory disease.
Because orangutans vary significantly in size and shape, it has not been possible to determine systematic body scoring techniques with these species. Investigating the potential of respiratory disease being influenced by obesity, poor body condition, and low
103 activity levels, respondents to the survey were asked to rate or score orangutans as to their current body condition and their current activity level. This question was asked for both the overall current study population, and for those responding for orangutans with or having had respiratory disease and what these scores were when symptoms of disease first appeared.
Definitions of body condition classes are as follows: Too thin is defined as
“unhealthily underweight”; Thin is defined as “could use some additional weight but not unhealthy”; Ideal is defined as “ideal for age and sex class”; Overweight is defined as
“could lose some additional weight but not considered unhealthy”; Obese is defined as
“unhealthily overweight”.
Definitions of activity levels are as follows: Lowest is defined as “minimal movement with little to no climbing”; Low is defined as “some movement and some climbing”; Medium is defined as “good amount of movement and climbing regularly”;
High is defined as “high level of movement and climbing frequently”; and Highest is defined as “extremely active and high energy with climbing throughout much of the day.”
Using Crosstabs in SPSS, body condition scores and activity levels when symptoms first appeared are investigated (see Table 15). Out of a total of 23 respondents, the majority rated the orangutan as being at an ideal weight (n = 14) and 10 reported that when symptoms first appeared, the individual orangutan was at an ideal weight and their activity level was at rated as medium. Only 5 of the 23 respondents rated the orangutan as being overweight and no orangutans were rated as obese when symptoms first appeared.
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Crosstabs were also used to investigate the overall ratings of the study population in relation to current body condition and current activity levels (see Table 16). The majority of the 134 respondents rated the individual orangutan as being at an ideal weight
(n = 77). Overweight ratings were given to 42 orangutans, 11 orangutans were rated as thin, 3 orangutans were rated as obese, and 1 orangutan was rated as too thin.
Additionally, crosstabs were used to investigate current body condition scores and activity levels by species (see Table 17). Out of 61 respondents for Bornean orangutans,
36 were rated as ideal, 21 as overweight, 2 as thin, and 2 as obese. For Sumatran orangutans, out of 52 respondents, 32 reported orangutans as being at an ideal weight, 6 as overweight, 10 as thin, 1 as too thin, and 3 as obese. Hybrid orangutans, out of 28 respondents, 12 were rated as ideal and 16 as overweight, no Hybrid orangutans were rated as obese. More Bornean orangutans are rated as overweight then Sumatran orangutans, and Hybrid orangutans are rated as overweight more often than Sumatrans.
Activity levels appear more consistent between Bornean and Sumatran orangutans (see
Table 18), though Sumatran orangutans are rated as having low activity levels (n = 14) more often than Bornean orangutans (n = 4).
These results to not support prediction that orangutans who are considered obese and have poorer body condition scores will be at higher risk for respiratory disease.
Results also do not support the prediction that because activity level likely influences body condition then we would also expect to find that orangutans with lower activity levels having a higher incidence for respiratory disease. However, body condition scores by species do reflect that Bornean orangutans are considered overweight more often in general than Sumatran orangutans, with Hybrid orangutans overweight scores falling
105 between Bornean and Sumatran orangutans in this study. Also, activity level scores, given that Sumatran orangutans are more frequently scored as being less active, would suggest we should see Sumatran orangutans overweight scores higher than Bornean orangutan overweight scores, which is not the case in this study population.
Table 15. Crosstabs Body Condition and Activity Level when Symptoms First Appeared
Activity Level Body Condition Lowest Low Medium High Highest Total Too Thin 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) Thin 0 (0%) 3 (13.04%) 1 (4.35%) 0 (0%) 0 (0%) 4 (17.39%) Ideal 0 (0%) 1 (4.35%) 10 (43.48%) 3 (13.04%) 0 (0%) 14 (60.87%) Overweight 0 (0%) 2 (8.7%) 3 (13.04%) 0 (0%) 0 (0%) 5 (21.74%) Obese 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) Total 0 (0%) 6 (26.09%) 14 (60.87%) 3 (13.04%) 0 (0%) 23 (100%)
Table 16. Crosstabs Current Study Population, Current Body Condition, and Activity Level
Activity Level Body Condition Lowest Low Medium High Highest Total Too Thin 1 (0.75%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 1 (0.75%) Thin 4 (2.99%) 4 (2.99%) 1 (0.75%) 2 (1.49%) 0 (0%) 11 (8.21%) Ideal 1 (0.75% 13 (9.7%) 33 (24.63%) 16 (11.94%) 14 (10.45%) 77 (57.46%) Overweight 4 (2.99%) 8 (5.97%) 28 (20.9%) 2 (1.49%) 0 (0%) 42 (31.34%) Obese 0 (0%) 1 (2.99%) 2 (1.49%) 0 (0%) 0 (0%) 3 (2.24%) Total 10 (7.46%) 26 (19.4%) 64 (47.76%) 20 (14.93%) 14 (10.45%) 134 (100%)
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Table 17. Crosstabs Current Body Condition and Species
Species Body Condition Bornean Sumatran Hybrid Total Too Thin 0 (0%) 1 (0.71%) 0 (0%) 1 (0.71%) Thin 2 (1.42%) 10 (7.09%) 0 (0%) 12 (8.51%) Ideal 36 (25.53%) 32 (22.7%) 12 (8.51%) 80 (56.74%) Overweight 21 (14.89%) 6 (4.26%) 16 (11.35%) 43 (30.5%) Obese 2 (1.42%) 3 (2.13%) 0 (0%) 5 (3.55%) Total 61 (43.26%) 52 (36.88%) 28 (19.86%) 141 (100%)
Table 18. Crosstabs Current Activity Level and Species
Species Activity Level Bornean Sumatran Hybrid Total Lowest 3 (2.24%) 4 (2.99%) 3 (2.24%) 10 (7.46%) Low 4 (2.99%) 14 (10.45%) 8 (5.97% 26 (19.4%) Medium 35 (26.12%) 16 (11.94%) 13 (9.7%) 64 (47.76%) High 9 (6.72%) 10 (7.46%) 1 (0.75%) 20 (14.93%) Highest 8 (5.97%) 5 (3.73%) 1 (0.75%) 14 (10.45%) Total 59 (44.03%) 49 (36.57%) 26 (19.4%) 134 (100%)
Hypothesis 3
If respiratory disease is influenced by an increase in body size, then as body size increases the risk of being affected by respiratory disease also increases.
Prediction 1
Male orangutans will be more at risk for respiratory disease than female orangutans.
In Figure 31 we see the loess smooth curves for male and female orangutan weight represented by their current age in years and their current weight in kilograms.
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This figure helps display the significant weight difference between males and females of this species, and extreme sexual dimorphism.
Presence of respiratory disease is reported in 20 male orangutans within the study population and in 12 of the female orangutans, with the total study population representing 154 individual orangutans (see Table 19). The percentage of female versus male orangutans of the affected population is shown in Table 20. Using logistic regression for the presence or absence of respiratory disease and species and sex as covariates, we do not see significance at the species level; Bornean (p = .642), Sumatran
(p = .432), and Hybrid (p = .891) (see Table 21). However, significance is observed in sex (p = .036) with males being 2.4 times more likely than females of having respiratory disease (see Table 21).
Kaplan-Meier curves for survival and hazard functions for female (n = 76) and male (n = 60) captive orangutans using age at first diagnosis and current age in years (see
Table 22) no significance is found (Wilcoxon df = 1; p = .176) (see Table 23). Kaplan-
Meier curves for survival and hazard functions by sex, female (n = 76) and male (n = 60), show no statistical significance. The survival and hazard functions represent time to first diagnosis as the end point, not death. The graph displaying survival functions by sex do show that the female curve above the male curve. For the graph displaying hazard functions by sex, the curve for male orangutans is far above the curve for females, and appears particularly dramatic for males in their twenties (Figure 32 and 33). The dramatic curve for male orangutans being diagnosed with respiratory disease in their twenties could possibly be representative of the time when these males began to develop
108 their secondary sexual characteristics, with their throat sac becoming more pronounced and developed.
Figure 31: Cross sectional loess smooth curves for male and female captive orangutans, using current age in years and current weight in KG. Note: KG = 2.2lbs.
Table 19. Presence or Absence of Respiratory Disease in Captive Orangutans by Sex in the Current Study Population
Presence Absence Unknown Total Female 12 (7.79%) 68 (44.16%) 1 (0.65%) 81 (52.6%) Male 20 (12.99%) 48 (31.17%) 5 (3.25%) 73 (47.4%) Total 32 (20.78%) 116 (75.32%) 6 (3.9% 154 (100%)
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Table 20. Presence or Absence of Respiratory Disease in Captive Orangutans by Sex in the Affected Population
Presence Percent Female 12 37.50% Male 20 62.50% Total 32 100%
Table 21. Logistic Regression for Presence or Absence of Respiratory Disease by Species and Sex
B S.E. Wald Df Sig. Exp(B) Bornean .887 2 .642 Sumatran .357 .446 .641 1 .423 1.429 Hybrid -.082 .599 .019 1 .891 .921 Sex .867 .412 4.416 1 .036 2.379 Constant -2.742 .730 14.115 1 .000 .064 p significant < .05
Table 22. Kaplan-Meier Case Processing Summary by Sex
Censored Sex Total Number Number of Events Number Percent Female 76 9 67 88.2% Male 60 13 47 78.3% Overall 136 22 114 83.8%
Table 23. Kaplan-Meier Overall Comparisons by Sex
Chi-Square Df Sig. Log Rank (Mantel-Cox) 2.777 1 .096 Breslow (Generalized Wilcoxon) 1.828 1 .176 Tarone-Ware 2.374 1 .123 p significant < .05
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Figure 32. Kaplan-Meier curves for survival functions for male and female captive orangutans, using age at first diagnosis and age in years for censored data.
Figure 33. Kaplan-Meier curves for hazard functions for male and female captive orangutans, using age at first diagnosis and age in years for censored data.
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Environment
Certain environmental factors, such as stress events, rearing history, climate, indoor and outdoor access, and time kept indoors while cleaning duties are performed may influence the presence and susceptibility of respiratory disease in orangutans.
Hypothesis 4
If stress or stress events influence the susceptibility to respiratory disease then orangutans who have experienced these events will be at higher risk.
Prediction 1
The number of times an orangutan moves to another facility will influence their chance of having respiratory disease.
Prediction 2
Hand-raised orangutans will show a higher incidence of respiratory disease.
The logistic regression for the presence or absence of respiratory disease and the number of moves and rearing history of individual captive orangutans show that rearing history a not significant risk factor for respiratory disease in this study (p = .178) (see
Table 24). The number of times an orangutan is moved to another institution is significant however (p = .017), showing that orangutans are 1.5 times more likely to have respiratory disease with each move to another facility (see Table 24). Figure 34 shows the number of orangutans with and without respiratory disease and the number of times they have moved facilities. We see that he majority of orangutans without respiratory disease have never moved facilities.
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Table 24. Logistic Regression for Presence or Absence of Respiratory Disease, Number of Moves, and Rearing History
B S.E. Wald Df Sig. Exp(B) Number of Moves .391 .163 5.736 1 .017 1.478 Rearing History -.273 .202 1.816 1 .178 .761 Constant -.1.399 .433 10.461 1 .001 .247 p significant < .05
Figure 34. Bar chart for orangutans with or without respiratory disease and number of moves.
Hypothesis 5
If environmental factors affect the presence and susceptibility of respiratory disease then orangutans in certain conditions will be more at risk.
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Prediction 1
Orangutans born at certain institutions will have a higher risk of respiratory disease.
Prediction 2
Orangutans with limited outdoor access will be at higher risk of respiratory disease. Months spent indoors will put orangutans at higher risk. Orangutans who are not shifted out of their enclosures regularly before cleaning and hosing duties are performed will be at higher risk of respiratory disease.
The logistic regression for the presence or absence of respiratory disease and place of birth shows that there is statistical significance (p = .014) with having respiratory disease and where the orangutan was born (see Table 25). No significance is observed when looking at the logistic regression for the presence or absence of respiratory disease and the possible risk factors of months spent indoors (p = .538), whether the orangutan has indoor and outdoor access (p = .814), or whether the orangutan is shifted out before cleaning (p = .514) (see Table 26 and Table 27).
Figure 35 shows the number of orangutans with and without respiratory disease and months spent indoors. The percentage of orangutans with respiratory disease and indoor/outdoor access (84.4%) and orangutans without respiratory disease and indoor/outdoor access (86.8%) are very similar (see Table 28). The percentage of orangutans with respiratory disease with no indoor/outdoor access (15.6%) and those without respiratory disease and no indoor/outdoor access (13.2%) were also very similar
(see Table 28). Figure 36 shows the number of orangutans with and without respiratory disease and if they have indoor and outdoor access. The percentage of orangutans with
114 respiratory disease that are shifted for cleaning all or most of the time (80.6%) is similar to the percentage of orangutans without respiratory disease in this same category (75%)
(see Table 29). The percentage of orangutans that are not shifted or are only shifted sometimes who have respiratory disease (19.4%) is fairly close to the percentage of orangutans without respiratory disease in this same category (25%) (see Table 29).
Figure 37 shows the number of orangutans with and without respiratory disease and if they are shifted for cleaning. When looking at months spent indoors, the percentage of orangutans with respiratory disease and those without do not deviate significantly (see
Table 30).
Table 25. Logistic Regression for Presence or Absence of Respiratory Disease and Place of Birth
B S.E. Wald Df Sig. Exp(B) Place of Birth .024 .010 6.085 1 .014 1.024 Constant -2.220 .454 23.944 1 .000 .109 p significant < .05
Table 26. Logistic Regression for Presence of Respiratory Disease, Indoor and Outdoor Access, and Shifted Before Cleaning
B S.E. Wald Df Sig. Exp(B) Indoor Outdoor Access? -.133 .565 .055 1 .814 .876 Shifted Before Cleaning .331 .508 .426 1 .514 1.393 Constant -1.384 .681 4.134 1 .042 .251 p significant < .05
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Table 27. Logistic Regression for Presence of Respiratory Disease and how Many Months a Year the Individual is Kept Indoors
B S.E. Wald Df Sig. Exp(B) Months Indoors -.132 .215 .378 1 .538 .876 Constant -1.013 .456 4.931 1 .026 .363 p significant < .05
Figure 35. Bar chart for orangutans with or without respiratory disease and months kept indoors.
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Table 28. Crosstabs Respiratory Disease and Indoor/Outdoor Access
Indoor/Outdoor Access Respiratory Disease Yes No Total 99 15 114 No 86.8% 13.2% 100.0% 27 5 32 Yes 84.4% 15.6% 100.0% 126 20 146 Total 86.3% 13.7% 100.0%
Figure 36. Bar chart for orangutans with or without respiratory disease and indoor/outdoor access.
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Table 29. Crosstabs Respiratory Disease and Shifted for Cleaning
Shifted for Cleaning Yes/Most of the Time No/Sometimes Total Respiratory Disease No 81 27 108 75.0% 25.0% 100.0% Yes 25 6 31 80.6% 19.4% 100.0% Total 106 33 139 76.3% 23.7% 100.0%
Figure 37. Bar chart for orangutans with or without respiratory disease and shifted for cleaning.
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Table 30. Crosstabs Respiratory Disease and Months Indoors
Months Indoors Respiratory 1-3 4-6 7-9 10-12 Disease None Months Months Months Months Overnight Unknown Total 1 23 22 6 7 6 2 67 No 1.5% 34.3% 32.8% 9.0% 10.4% 9.0% 3.0% 100.0% 0 2 10 2 3 3 0 20 Yes 0.0% 10.0% 50.0% 10.0% 15.0% 15.0% 0.0% 100.0% 1 25 32 8 10 9 2 87 Total 1.1% 28.7% 36.8% 9.2% 11.5% 10.3% 2.3% 100.0%
Genetics
Orangutans who are related to other orangutans who have respiratory disease may be at higher risk than those not related to other orangutans with respiratory disease.
Orangutans in the same family line will have a higher propensity for respiratory disease.
Hypothesis 6
If there is a genetic factor in influencing the predisposition to respiratory disease then we will see higher incidence of respiratory disease with orangutans who are related to other orangutans with respiratory disease.
Prediction 1
Orangutans with respiratory disease will more often be related to other orangutans with respiratory disease than orangutans without respiratory disease.
No significance is observed in the logistic regression looking at the presence or absence of respiratory disease and a family history of respiratory disease (p = .997) (see
Table 31). For the entire current study population (n = 153, n = 1 missing) a family history of respiratory disease is reported in 15% (n = 23) of the population, no history of respiratory disease is reported in 26.1% (n = 40) of the population, but the majority of
119 respondents reported that a family history of respiratory disease is unknown 58.8%
(n = 90) (see Table 32). When looking at crosstabs between the answers to questions regarding the presence or absence of respiratory disease and a family history of respiratory disease, of the reported orangutans who have or have had respiratory disease all 7 (100%) also report a family history (see Table 34), 0 report no history, and 24 report an unknown family history (see Table 33). For orangutans who are not reported to have or have had respiratory disease, 14 report a family history of respiratory disease, 39 report no history, and 63 report an unknown family history (see Table 34), while 6 report an unknown status of respiratory disease with 2 of these individuals having a family history, 1 with no family history, and 3 with unknown family history. Figure 38 shows the number of orangutans with or without respiratory disease and if there is a family history with respiratory disease.
For family relationships within the study population, we see that for relationship
1, a total of 13 (59.1%) respondents report a father with respiratory disease and only 4
(18.2%) report a relationship with a mother (see Table 35). For family relationships among orangutans with diagnosed respiratory disease, only 3 report a relationship with a father with respiratory disease, only 1 with a relationship to a mother, 3 with a relationship to a sister or half-sister, 2 with a brother or half-brother, and 1 to a grandfather (see Table 36).
Table 31. Logistic Regression for Presence or Absence of Respiratory Disease and Family History of Respiratory Disease
B S.E. Wald Df Sig. Exp(B) Family History? 20.510 6436.027 .000 1 .997 807737443.700 Constant -21.203 6436.027 .000 1 .997 .000 p significant < .05
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Table 32. Family History of Respiratory Disease in the Current Study Population
Family History Frequency Percent Yes 23 15% No 40 26.1% Unknown 90 58.8% Total Responses 153 100%
Table 33. Family History of Respiratory Disease and Presence or Absence of Respiratory Disease in Orangutans
Family History Respiratory Disease Yes No Unknown Total Presence 7 0 24 31 Absence 14 39 63 116 Unknown 2 1 3 6 Total 23 40 90 153
Table 34. Crosstabs Family History of Respiratory Disease
Family History Respiratory Disease Yes No Total No 14 (26.4%) 39 (73.6%) 53 (100%) Yes 7 (100%) 0 (0%) 7 (100%) Total 21 (35.0%) 39 (65.0%) 60 (100%
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Figure 38. Bar chart for orangutans with or without respiratory disease and family history of respiratory disease.
Table 35. Family Relationships and Respiratory Disease in the Current Study Population
R1 R1 R2 R2 R3 R3 Relationship 1-3 Frequency Percent Frequency Percent Frequency Percent Mother 4 18.2% 2 25% 0 0% Father 13 59.1% 1 12.5% 0 0% Sister or Half-Sister 3 13.6% 0 0% 1 33.3% Brother or Half-Brother 0 0% 2 25% 0 0% Aunt 0 0% 1 12.5% 1 33.3% Uncle 0 0% 1 12.5% 1 33.3% Grandmother 0 0% 0 0% 0 0% Grandfather 0 0% 1 12.5% 0 0% Mate 2 9.1% 0 0% 0 0% Total 22 100% 8 100% 3 100% Note: R1 = Relationship 1, R2 = Relationship 2, R3 = Relationship 3
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Table 36. Family Relationships and Presence or Absence of Respiratory Disease in Orangutans
Respiratory Disease R1 R1 R2 R2 R3 R3 Relationship 1-3 Present Absent Present Absent Present Absent Mother 0 4 1 1 0 0 Father 3 9 0 1 0 0 Sister or Half-Sister 3 0 0 0 0 1 Brother or Half- 0 0 2 0 0 0 Brother Aunt 0 0 0 1 0 1 Uncle 0 0 0 1 0 1 Grandmother 0 0 0 0 0 0 Grandfather 0 0 1 0 0 0 Mate 0 1 0 0 0 0 Total 6 14 4 4 0 3
Physical and Behavioral Symptoms
Table 37 displays the most commonly experienced types of symptoms experienced by captive orangutans with diagnosed respiratory disease. Table 38 displays the frequency of these particular symptoms, and Table 39 displays the severity of these symptoms as described by respondents to the survey.
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Table 37. Presence or Absence of Physical and Behavioral Symptoms
Physical Symptoms Yes Percent No Percent Total Responses Coughing 19 82.6% 4 17.4% 23 Nasal Discharge 16 72.7% 6 27.3% 22 Sneezing 16 69.6% 7 30.4% 23 Lethargy 13 56.5% 10 43.5% 23 Decreased Appetite 11 52.4% 10 47.6% 21 Dyspnea 9 52.9% 8 47.1% 17 Change in Palpation of Throat Sac 6 33.3% 12 66.7% 18 Halitosis 6 35.3% 11 64.7% 17 Increase or Change in Drainage of Fistula 5 38.5% 8 61.5% 13 Diarrhea 5 27.8% 13 72.2% 18 Change in Body Odor 4 22.2% 14 77.8% 18 Increase in Size of Throat Sac 4 22.2% 14 77.8% 18 Weight Loss 4 23.5% 13 76.5% 17 Skin Problems 4 22.2% 14 77.8% 18 Tachypnea 2 18.2% 9 81.8% 11 Decreased Vocalization 2 11.1% 16 88.9% 18 Voice Change 1 5.6% 17 94.4% 18 Fever 1 9.1% 10 90.9% 11 Increased Appetite 0 0% 17 100% 17 Behavioral Symptoms Decreased Activity Level 14 66.7% 7 33.3% 21 Change in Eating Habits 11 55% 9 45% 20 Change in Behavior Towards Caregivers 7 35% 13 65% 20 Change in Behavior Towards Conspecifics 6 30% 14 70% 20 Increased Agitation 6 35.3% 11 64.7% 17 Increased Aggression 3 17.6% 14 82.4%17 17 Weakness 2 12.5% 14 87.5% 16 Change in Other Habits 1 7.1% 13 92.9% 14
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Table 38. Frequency of Physical and Behavioral Symptoms.
Total Physical Symptoms CH % IM % EA % UC % Responses Nasal Discharge 6 37.5% 5 31.3% 3 18.8% 2 12.5% 16 Coughing 2 10.5% 7 36.8% 6 31.6% 4 21.1% 19 Halitosis 2 25% 2 25% 2 25% 2 25% 8 Increase in Size of 2 40% 0 0% 2 40% 1 20% 5 Throat Sac Skin Problems 2 50% 2 50% 0 0% 0 0% 4 Sneezing 1 6.3% 5 31.3% 3 18.8% 7 43.8% 16 Lethargy 1 8.3 1 8.3% 7 58.3% 3 25% 12 Decreased Appetite 1 10% 2 20% 5 50% 2 20% 10 Increase or Change in 1 20% 1 20% 2 40% 1 20% 5 Drainage of Fistula Dyspnea 1 12.5% 4 50% 2 25% 1 12.5% 8 Weight Loss 1 33.3% 1 33.3% 1 33.3 0 0% 3 Tachypnea 0 0% 0 0% 1 50% 1 50% 2 Voice Change 0 0% 0 0% 0 0% 1 100% 1 Diarrhea 0 0% 1 25% 2 50% 1 25% 4 Fever 0 0% 0 0% 0 0% 1 100% 1 Decreased Vocalization 0 0% 0 0% 1 50% 1 50% 2 Increased Appetite 0 0% 0 0% 0 0% 0 0% 0 Behavioral Symptoms Change in Eating 1 10% 0 0% 5 50% 4 40% 10 Habits Increased Agitation 1 16.7% 1 16.7% 3 50% 1 16.7% 6 Decreased Activity 0 0% 2 15.4% 8 61.5% 3 23.1% 13 Level Change in Behavior 0 0% 2 33.3% 3 50% 1 16.7% 6 Towards Conspecifics Weakness 0 0% 0 0% 1 50% 1 50% 2 Change in Behavior 0 0% 2 40% 2 40% 1 20% 5 Towards Caregivers Increased Aggression 0 0% 1 33.3% 1 33.3% 1 33.3% 3 Change in Other Habits 0 0% 0 0% 1 100% 0 0% 1 UC = Uncommon IM = Intermittent EA = Episode Affiliated CH = Chronic
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Table 39. Severity of Physical and Behavioral Symptoms
Total Physical Symptoms HT % H % M % L % LT % Responses Increase or Change in Drainage of 1 20% 1 20% 2 40% 1 20% 0 0% 5 Fistula Nasal Discharge 0 0% 5 31.3% 9 56.3% 2 12.5% 0 0% 16 Increase in Size of 0 0% 4 80% 0 0% 0 0% 1 20% 5 Throat Sac Lethargy 0 0% 4 36.4% 2 18.2% 4 36.4% 1 9.1% 11 Halitosis 0 0% 3 42.9% 2 28.6% 0 0% 2 28.6% 7 Decreased 0 0% 3 30% 3 30% 3 30% 1 10% 10 Appetite Change in Palpation of 0 0% 3 50% 3 50% 0 0% 0 0% 6 Throat Sac Dyspnea 0 0% 1 14.3% 2 28.6% 4 57.1% 0 0% 7 Coughing 0 0% 1 5.9% 9 52.9% 5 29.4% 2 11.8% 17 Sneezing 0 0% 0 0% 6 40% 5 33.3% 4 26.6% 15 Diarrhea 0 0% 0 0% 1 33.3% 0 0% 2 66.7% 3 Skin Problems 0 0% 0 0% 0 0% 1 33.3% 2 66.7% 3 Change in Body 0 0% 0 0% 0 0% 3 75% 1 25% 4 Odor Weight Loss 0 0% 0 0% 1 33.3% 1 33.3% 1 33.3% 3 Fever 0 0% 0 0% 0 0% 0 0% 1 100% 1 Increased Appetite 0 0% 0 0% 0 0% 0 0% 0 0% 0 Tachypnea 0 0% 0 0% 2 100% 0 0% 0 0% 2 Voice Change 0 0% 0 0% 0 0% 1 100% 0 0% 1 Decreased 0 0% 0 0% 0 0% 1 100% 0 0% 1 Vocalization Behavioral Symptoms Change in Eating 0 0% 2 22.2% 2 22.2% 3 33.3% 2 22.2% 9 Habits Weakness 0 0% 1 50% 0 0% 0 0% 1 50% Decreased Activity 0 0% 1 8.3% 5 41.7% 5 41.7% 1 8.3% 12 Level Change in Behavior 0 0% 0 0% 3 75% 0 0% 1 25% 4 Towards Caregivers Change in Behavior 0 0% 0 0% 3 60% 1 20% 1 20% 4 Towards Conspecifics Increased 0 0% 0 0% 3 60% 1 20% 1 20% 5 Agitation Change in Other 0 0% 0 0% 1 100% 0 0% 0 0% 1 Habits Increased 0 0% 0 0% 2 100% 0 0% 0 0% 2 Aggression Lowest = LT Low = L Mild = M High = H Highest = HT
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Additional Information from Survey Results
Additional information obtained from survey results are reported here. Reported age at maturity, age of flange for males, and age of first menses for females are described. We see the mean age for sexual maturity at 9.4 years of age, mean age for flange at 13.7 years of age, and the mean age for first menses at 8.2 years of age (see
Table 41). The mean ages for respiratory disease diagnoses ranges from 15.2 years old to
18.8 years old (see Table 40). Figure 39 shows the ages at first diagnosis. Overall, the mean age of diagnoses is higher than for the age parameters for maturity, suggesting that more mature orangutans have a higher likelihood of being diagnosed with respiratory disease. However, when looking at the ages at first diagnoses (n = 19) the ages are well distributed and clustering is not observed. Table 42 displays family relatedness for orangutans with air sacculitis, 4 respondents that report air sacculitis here also report a family history, and 13 report that this information is unknown.
The logistic regression for the presence or absence of respiratory disease and stress events prior to the onset of illness (see Table 43) is not significant. The majority of respondents (n = 18) reported that there was no stress prior to the onset of illness (see
Table 44). Only 4 respondents offered answers to the type of stress experienced prior to illness, with 1 answering a move to another facility, 1 having lost a companion, 1 stating other medical issues, and 1 answered unknown (see Table 45).
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Table 40. Age at Respiratory Diagnoses
Number Minimum Maximum Mean Std. Deviation Age at First Diagnoses 19 6.00 45.00 18.84 10.63 Age at Second Diagnoses 8 7.50 45.00 17.69 12.50 Age at Third Diagnoses 8 7.00 39.00 18.15 10.42 Age at Fourth Diagnoses 6 8.00 23.00 15.12 6.18 Valid N (listwise) 6
Figure 39. Bar chart for age of orangutans at first diagnosis of respiratory disease.
Table 41. Age of Sexual Maturity, Flange, and First Menses
Number Minimum Maximum Mean Std. Deviation Age of Sexual Maturity 34 5.00 15.00 9.44 2.44 Age of Flange 21 8.00 19.00 13.71 2.70 Age of First Menses 9 6.00 11.00 8.22 1.99 Valid N (listwise) 0
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Table 42. Family History of Respiratory Disease and Orangutans that Have or Had Air Sacculitis
Family History Yes No Unknown Total Air Sacculitis Yes 4 0 13 17 No 2 0 3 5 Unknown 0 0 0 0 Total 6 0 16 22
Table 43. Logistic Regression for Presence or Absence of Respiratory Disease and Stress before Illness
B S.E. Wald df Sig. Exp(B) Did this Individual Experience Stress 19.593 20096.485 .000 1 .999 323094968.600 Events Prior to Ilness? Constant 1.609 .632 6.476 1 .011 5.000 p significant < .05
Table 44. Was there Stress before Illness?
Stress Before Illness Frequency Yes 4 (18.18%) No 18 (81.82%) Total 22 (100%)
Table 45. Did this Individual Experience Stress before Illness? What Type of Stress?
Stress Before Illness Yes No Unknown NA Total Type of Stress Moved Facilities 1 0 0 0 1 Loss of Companion 1 0 0 0 1 Other Medical Issues 1 0 1 0 2 Unknown 1 1 9 0 11 Not Applicable 0 12 1 100 113 Other 0 0 3 0 3 Total 4 13 14 100 131
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CHAPTER 11
DISCUSSION
Significance of the Prevalence of Respiratory Disease in Multiple Populations of Captive Orangutans
The orangutan, which in Malay means Person of the Forest, is the only extant great ape found outside of Africa. The Bornean orangutan (P. pygmaeus) and the
Sumatran orangutan (P. abelli) are currently listed as critically endangered by the IUCN
(2016), and a newly classified species (P. tapanuliensis) has a population of fewer than
800 individuals (Nater et al., 2017). Therefore, of significant concern and interest, are the problems that these species face both in their natural habitat and in captive environments. As such, understanding critical aspects of their health and well-being in captive environments is necessary to facilitate the continued success of captive management, both in-situ and ex-situ. Respiratory disease is a leading cause of mortality and morbidity in zoo-housed orangutans. Respiratory disease in orangutans is found in many zoological institutions both in North America (2012 Orangutan SSP Health Survey) and in Europe (Zimmerman et al., 2011). Rehabilitation centers for orangutans, that offer permanent sanctuary for some and possible release back into their natural habitat for others, have also been experiencing issues relating to respiratory disease (Lawson et al.,
2006). It has become abundantly clear that respiratory disease in orangutans is a serious threat to the zoological captive orangutan population and possibly for orangutans residing in rehabilitation centers. A previous study looking at respiratory disease in the North
130
American orangutan population (2012 Orangutans SSP Health Survey) focused on prevalence of disease at an institutional level. This research aimed to identify potential factors influencing the prevalence of respiratory disease in captive orangutans at an individual level.
Similarities in the Prevalence of Respiratory Disease between the North American and European Captive Orangutan Population
The current study population is very closely representative demographically to the current North American SSP orangutan population, which allows for more accurate analyses with respect to respiratory disease and the prevalence of disease within certain demographic classes. The primary focus of this research was to identify potential risk factors that predispose orangutans to respiratory disease and to understand the prevalence of respiratory disease in the North American orangutan population. Though definitions of specific types of respiratory disease varied across the current study and Zimmermann et al. (2011), both studies investigated overall prevalence of respiratory disease in their respective populations.
Results from this study reflect a total of 32 individual orangutans that currently have or have had respiratory disease, representing a total of 20.78% of the study population (n = 154). Of significant interest, research conducted by Zimmermann et al.,
(2011) produced a very similar percentage of respiratory disease among zoo housed orangutans within the European population, with 20.40% of their study population (n =
201) being reported as having either “chronic respiratory signs only” or “air sacculitis.”
The authors suggest this number could be even larger due to the unknown respiratory status of 79 individual orangutans. Zimmermann et al. (2011) also report that of the 20 zoos visited for this research, respiratory disease occurred in a total of 15. One-fifth of
131 the captive population of orangutans is directly affected by respiratory disease, at least in these two populations.
Previous Medical Assessment of the North American Orangutan Population
Utilizing medical records from the North American captive orangutan population, an overall medical assessment of this population was previously evaluated (Wells,
Sargent, Andrews, & Anderson, 1990). Using respiratory bouts as a category to assess this population, they found that a total of 41.8% of this population suffered at least one bout with respiratory illness (Wells et al., 1990).
Prevalence in Rehabilitation Centers
A publication has described respiratory disease, in the form of air sacculitis, at a rehabilitation center in Borneo, Central Kalimantan (Lawson et al., 2006). Air sacculitis is reported as being an important medical condition among the juvenile orangutans being housed at this facility, the Orangutan Care Center and Quarantine (OCC&Q) in Central
Kalimantan (Lawson et al., 2006). There is currently an assessment underway at another rehabilitation center in Borneo to understand the prevalence of respiratory disease among orangutans (F. Sulitsyo, personal communication). Understanding the significance of respiratory at rehabilitation centers is critical given the substantial numbers of orangutans currently being housed in these centers waiting for potential release back into livable forests. Large numbers of orangutans also continue to come into these centers (Russon,
2009), and knowing what possible factors are influencing the onset of disease is needed.
Some of these individuals will be permanent residents in sanctuaries, because they are not eligible for release (Russon, 2009), in which case will need long-term care.
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Prevalence of Types of Respiratory Disease
Air sacculitis is the commonly reported form of respiratory disease in this population (78.3%), with the majority of responses reporting chronic cases (56.3%). Air sacculitis is followed in diagnoses by rhinitis, pneumonia, sinusitis, bronchitis, and other.
Further data collection and analysis could provide insight into possible progression of less serious forms of respiratory disease and if these are predictors for more serious forms of respiratory disease in the future. In addition, it would be valuable to understand if there are variations between the species, and or sex, in the prevalence of certain types of diseases. More data are needed for continued investigation into these potential differences and in the possibility of disease progression.
Interpreting Results Regarding Demographics and Body Size
Species, Ecology, Obesity, Respiratory Disease, and the Thrifty Genotype Hypothesis
It has been suggested that obesity could play a role in prevalence of respiratory disease in the captive orangutan population (Cambre et al. 1980). It has also been suggested that sedentary behavior is reinforced by obesity and that mechanisms for the removal of fluid from the air sac could become compromised due to this decreased activity (Gross, 1978). In turn, it could be argued instead that a more sedentary way of life reinforces weight gain and obesity. A study has reported the daily energy expenditure (DEE) of captive orangutans, described as having similar activity levels as wild orangutans, as using less energy relative to body mass than almost any other eutherian mammal that has been measured (Pontzer, Raichlen, Shumaker, Ocobock, &
Wich, 2010). This low rate of energy use is consistent with the low reproduction and growth rates of orangutans and is suggestive of an evolutionary response to the ecological
133 conditions with extreme food shortages, such as what is found in orangutan native habitats (Pontzer et al., 2010). Pontzer et al. (2010) suggest that orangutans have become low-energy specialists to offset the risks of starvation when quality food is scarce. It is likely that captive orangutans are prone to obesity and being overfed due to their low energy needs (Pontzer et al., 2010). This suggestion is in line with the thrifty gene hypothesis (Neel, 1962), and with hypotheses and predictions from the present study. In humans, obesity has become a significant public and individual health problem over the past few decades (Piper, 2012). When respiratory issues already exist in humans, excess weight can have an even more significant impact on the respiratory system (Piper, 2012).
In humans, the influence of excess weight on both poor responses to therapy and on respiratory symptoms is underestimated (Piper, 2012).
The potential relationship between body condition, obesity, and body size with the susceptibility of respiratory disease in orangutans was investigated. Data from studies of wild orangutans suggest that they are during times of food abundance, orangutans are highly efficient at storing fat, then allowing them to use these stores when high energy foods become less available (Knott, 1998). Because Bornean orangutans are adapted for ecological conditions that make them reliant on fall back foods, whereas
Sumatran forests are more productive (Marshall et al., 2009; Taylor, 2009; Wich et al.,
2006), Bornean orangutans would be expected to have a higher preponderance for obesity in captive environments, in accordance with the thrifty genotype hypothesis (van Schaik et al., 2009). Hence, they would be expected to show a higher incidence of respiratory disease. It has been noted by several authors that Bornean orangutans in captive environments are more prone to obesity than Sumatran orangutans, who seldom become
134 overweight (Courtenay et al., 1988; Zimmermann, et al., 2011). Therefore, this study looked at whether Bornean orangutans would be rated more often as overweight or obese, rated as less active, and have heavier body weights than Hybrid and Sumatran orangutans in captive environments. Though body condition and activity level ratings data are highly subjective, as mentioned above, a standard body condition scoring system does not exist for these species.
Additionally, it should be mentioned again that measured weights could also be somewhat misleading due to the variability in shapes and sizes in individual orangutans.
The loess smooth curves appear to show that captive Bornean orangutans are indeed heavier than Hybrid and Sumatran orangutans, and they are rated more often as overweight than Sumatran and Hybrid orangutans. Interestingly, the Hybrid orangutans fall in between both Bornean and Hybrid orangutans in the loess smooth growth curves, as would be predicted and expected under the thrifty genotype hypothesis. Body condition and activity level scores did not reflect any influence on risk for respiratory disease, with the majority of respondents (43.48%) answering that the individual had a medium activity level and ideal weight when symptoms first appeared. In terms of the entire study population, again the majority of respondents (24.63%) reported that the individual has a medium activity level and ideal weight. However, 31.34% of the respondents report that the individual orangutan is overweight, nearly one-third of the study population. At the species level, 14.89% of the study population are Bornean orangutans that are scored as overweight, as compared to 4.26% of Sumatran orangutans who are scored as overweight, and 11.35% of the population are Hybrid orangutans who are scored as overweight. This would be expected, Bornean orangutans being ranked
135 overweight more often, Sumatran orangutans ranked overweight less often, and Hybrid orangutans falling in the middle. Of interest, Sumatran orangutans are ranked as having low activity levels more often (10.45%) than Bornean orangutans (2.99%). Within their respective populations, Bornean orangutans are rated as overweight or obese 37.7%,
Sumatrans 17.31%, and Hybrids 57.15%. It should be noted here, that because AZA accredited zoos no longer breed Hybrid orangutans, the majority of Hybrid orangutans in this population are older individuals.
Wild Orangutan Weights
Given the fluctuations of food availability for orangutans, it would be expected that average wild weights would correspond to these fluctuations. However, for purposes of comparison, reported wild weights are still of use. Eckhardt (1975) report that female orangutans weigh nearly the same between Sumatran and Bornean orangutans, but that
Bornean males appear slightly heavier than Sumatran, yet these differences did not yield statistical significance. Summaries of various published wild orangutan weight data were collated by Markham and Groves (1990) and are as follows: Bornean males (n = 4) 86.3
(80-91) kg and Bornean females (n = 5) 38.7 (33-45)kg; Sumatran males (n = 1) 86.3kg and Sumatran females (n = 5) 38.3 (34-43)kg. Other published weight data on wild
Bornean orangutans (P. p. morio) report: flanged males (n = 12) 74 +/- 9.78kg and adult females (n = 7) 35.29 +/- 7.32kg (Rayadin & Spehar, 2015). It should again be mentioned that weights on wild orangutans likely fluctuate significantly depending on forest quality and fruit availability, and possibly individual variations. Larger sample sizes, taking into account current forest quality and food abundance, are needed for a better understanding of wild orangutan weights and variations across populations.
136
Captive Orangutan Studies on Life-History Variations
Captive studies on variations in life-history parameters between species of orangutans have not yielded any suggestions of major differences between the Bornean and Sumatran orangutans, though it was reported that Bornean orangutans had longer inter-birth intervals than Sumatran orangutans (Anderson, Thompson, Knott, & Perkins,
2008). However, the difference observed is possibly related to captive breeding and management practices (Wich et al., 2009). In another study on captive orangutan mortality and fertility patterns, Hybrid orangutans had lower survival rates and higher infant rejection rates than Bornean or Sumatran orangutans, and infertility was 3 times higher in Bornean orangutans than observed in Sumatran or Hybrid orangutans (Cocks,
2007). Wich et.al. (2009) also report that no differences were found between species, with respect to inter-birth intervals or survival curves in captive orangutans.
Prevalence of Respiratory Disease by Species between Studies
In an overall medical assessment of the North American orangutan population, no statistical significance was observed in the prevalence of respiratory illness between species in the study population (n = 104); Bornean orangutans 33.7% (n = 35), Sumatran orangutans 46.2% (n = 48), and Hybrid orangutans 20.2% (n = 21) (Wells et al., 1990).
Zimmermann et al. (2011) did observe species differences among their study population.
Using two categories for respiratory disease, “chronic respiratory signs” and “air sacculitis,” they report statistical significance with Bornean orangutans having chronic respiratory signs more often (13.8%; n = 11) than Sumatran orangutans (3.6%; n = 4).
No significance was found when comparing these two species in regard to air sacculitis, though Sumatran orangutans were found to have air sacculitis more often (n = 16) than
137
Bornean orangutans (n = 8), reflecting that air sacculitis occurs in 10% of the Bornean population and in 14.3% of the Sumatran population in their study. 154 orangutans are represented in these data. Of these 154 orangutans, more Sumatran orangutans are reported to have respiratory disease (9.74%; n = 15) than Bornean orangutans
(7.79%; n = 12) or Hybrid orangutans (3.25%; n = 5), in the overall population. The percentage of orangutans by species in those with respiratory disease (n = 32) show
Sumatran orangutans being affected 46.88%, Bornean orangutans being affected 37.5%, and Hybrids affected 15.63%. Though it is observed that Bornean orangutans have larger body sizes, these data do not reflect that this is a risk factor for respiratory disease in these species. Zimmermann et al. (2011) suggest that facial morphological variation between the species could be a factor in the development of chronic respiratory signs among Bornean orangutans, due to anatomic variations within the intra and paranasal cavities when compared to Sumatran orangutans.
Sex, Extreme Sexual Dimorphism, Respiratory Disease, and the Thrifty Phenotype Hypothesis
Orangutans are highly sexually dimorphic with males often becoming twice the size of females. If larger body size is a risk factor for the onset of respiratory disease, then it would be expected that male orangutans would have higher rates of respiratory disease than female orangutans. The development of secondary sexual characteristics of male orangutans produce a large throat sac, much larger than females, unflanged males, or immature orangutans, which could possibly have an effect on the development of respiratory disease. If males flange more often in captive environments, and if body size does influence the susceptibility of respiratory disease, then possibly the prevalence in captive male orangutans is in response to this. Lawson et al. (2006) suggest that the
138 absence of air sacculitis in infants and young juveniles with a body weight <13.6kg should be equated to the lack of development of the laryngeal air sac at this early age.
The loess smooth growth curves for male and female orangutans in this study, using current weight in kilograms and age in years, demonstrate quite dramatically the differences in weight, and hence size, of captive male orangutans compared with captive female orangutans.
The presence of respiratory disease is reported in 20 (12.99%) male orangutans within the study population and in 12 (7.79%) of the female orangutans, with the total study population representing 154 individual orangutans. Among the affected population
(n = 32) we see male orangutans representing 62.50% of this population and females representing 37.50%. Using logistic regression for the presence or absence of respiratory disease and species and sex as covariates, significance is not found at the species level, however, significance is observed in sex with males being 2.4 times more likely than females of having respiratory disease.
In the medical assessment of the North American orangutan population conducted by Wells et al. (1990), a total of 58 females (55.8%) were identified as having respiratory illness and 46 males (44.2%), though this was not statistically significant. Zimmermann et al. (2011) found statistical significance between the sexes in their category of chronic respiratory signs, with males (15.8%) showing these signs more often than females
(3.9%). Zimmermann et al. (2011) suggest that the variation in maxillary sinus between males and females could possibly be a factor in developing chronic respiratory signs. In terms of air sacculitis, no statistical significance was found between the sexes in the study by Zimmermann et al. (2011). In Lawson et al. (2006) they also found air sacculitis in
139 both males (n = 5) and females (n = 9), however it should be noted that these individuals were juveniles.
Sex differences in other primate species have also been reported. In the study by
Kumar et al. (2012) they found that of the 37 cases of air sacculitis that they identified,
36 were male and only one was female. Kumar et al. (2012) also identified seven cases of air sacculitis in chimpanzees, six of these individuals were male and only one was female. The proportion of male baboons identified as having air sacculitis in this population suggests a male predisposition, though it is not clear why this is (Kumar et al.,
2012). Baboons are also considered highly sexually dimorphic, so possibly the preponderance of males affected in this study is reflective of differences in body size between males and females.
Interpreting Results Regarding Environment
A Captive Environment
It has been suggested that fecal contamination in captive environments could be a risk factor in the development of air sacculitis in orangutans (Cambre et al., 1980).
Though it could be argued that if fecal contamination was indeed a factor involved in the onset of respiratory disease in orangutans, than the same would hold true for other primate species. The fact that respiratory disease appears particularly prevalent in orangutans, more so than other potentially vulnerable species, would suggest other risk factors being involved. Environmental factors that could possibly contribute to the development of respiratory disease in captive orangutans were also explored by
Zimmermann et al. (2011). They documented enclosure size, group size at the time of infection, cleaning practices, and enclosure substrate, none of these were found to be
140 statistically significant. Zimmermann et al. (2011) also report that the number of individuals with respiratory disease within a group was small, typically with only one group member being affected at one time. Zimmermann et al. (2011) argue here that this should support the significance of individual factors relating to the development of respiratory disease as opposed to environmental factors, as one would expect to see a greater number of individuals within a group affected if environmental factors played a greater role.
It should be noted here as well, that when survey respondents in this study were asked if they had evidence that suggested the transmission of respiratory disease among orangutans, the vast majority answered no. It would be expected in this case as well, if environmental factors were involved, that more respondents would have answered yes, as more individuals within their groups would likely be affected leading to a possible explanation of disease transmission. Regardless of the potential that environmental factors do not contribute to the development of respiratory disease in orangutans, several environmental risk factors were explored in the present study. Environmental factors that could potentially be risk factors for the development of respiratory disease investigated here are different than what was studied by Zimmermann et al., (2011) and include variables such as stress events, rearing history, indoor and outdoor access, and time kept indoors while cleaning duties are performed.
Environmental Factors as Possible Risk Factors for Respiratory Disease in the Current Study
The logistic regression for the presence or absence of respiratory disease and the number of moves and rearing history show that rearing history is not significant in this study population. However, rearing history was statistically significant in European
141 study population (Zimmermann et al., 2011). The possibility that young orangutans are more susceptible to various ailments due to the lack of protection from mother’s milk and corresponding immune deficiencies could potentially be a risk factor. The lack of protection from breast milk could also factor in to the prevalence of respiratory disease in rehabilitation centers, possibly coupled with exposure to more conspecifics. The number of times an orangutan is moved to another institution is significant however, showing that orangutans are 1.5 times more likely to have respiratory disease with each move to another facility. Because male orangutans in this study are more often affected by respiratory disease, and the possibility exists that male orangutans just simply move to other facilities more frequently, the number of times males moved and females moved was calculated. Males in this study did in fact move more often than females, but not by much, (males n = 57; females n = 52). However, individually, males moved more frequently. It is possible that orangutans who are moved are exposed to different pathogens or are otherwise more susceptible to elements in their environment due to a suppressed or naïve immune system.
The majority of respondents (n = 18) reported that there was no stress prior to the onset of illness. Only 3 respondents offered answers to the type of stress experienced prior to illness, with 1 answering a move to another facility, 1 having lost a companion, 1 stating other medical issues, and 1 answering unknown.
The logistic regression for the presence or absence of respiratory disease and place of birth shows that there is significance with having respiratory disease and where the orangutan was born. It is possible however that these institutions having more orangutans with respiratory disease, simply house larger numbers of orangutans and
142 therefore have higher incidence of respiratory disease at their given facility. Given the percentage of orangutans with respiratory disease, this would certainly be a reasonable explanation.
No significance is observed when looking at the logistic regression for the presence or absence of respiratory disease and the possible risk factors of months spent indoors, whether the orangutan has indoor and outdoor access, or whether the orangutan is shifted out before cleaning. The percentage of orangutans with respiratory disease and indoor/outdoor access (84.4%) and orangutans without respiratory disease and indoor/outdoor access (86.8%) are very similar. The percentage of orangutans with respiratory disease with no indoor/outdoor access (15.6%) and those without respiratory disease and no indoor/outdoor access (13.2%) were also very similar. The percentage of orangutans with respiratory disease that are shifted for cleaning all or most of the time
(80.6%) is similar to the percentage of orangutans without respiratory disease in this same category (75%). The percentage of orangutans that are not shifted or are only shifted sometimes who have respiratory disease (19.4%) is fairly close to the percentage of orangutans without respiratory disease in this same category (25%). When looking at months spent indoors, the percentage of orangutans with respiratory disease and those without do not deviate significantly.
In addition, it should also be noted here that because orangutans move to other facilities, sometimes multiple times within their lifetime, discovering what environmental conditions were present at each of these facilities prior to the onset of disease is a daunting task making these assessments even more challenging. Where disease originated may not be possible to determine in some cases where orangutans have moved
143 facilities multiple times. Another complicating factor to understanding potential environmental risk factor is the fact that many facilities update, renovate, or completely design new habitats and holding areas for their orangutans. Cleaning protocols and other management protocols (e.g. bedding and substrate type) may also change over time.
Therefore, for orangutans who move to other facilities, and for those who do not, certain risk factors that contribute to the onset of respiratory disease are very challenging to identify.
Interpreting Results Regarding Family History
Orangutans who are related to other orangutans who have respiratory disease have been shown to be at higher risk than those not related to other orangutans with respiratory disease (Zimmermann et al., 2011). Zimmermann et al. (2011) suggest that inheriting genetic predisposing factors that increase the susceptibility of orangutans to respiratory disease should be considered. Zimmermann et al. (2011) found that nearly all of the orangutans in their study with respiratory disease also had at least one parent with respiratory disease (93%), as opposed to healthy animals having at least one parent with respiratory disease (54%). It is not clear if this is in part due to being housed in the same conditions, but given this study did not show environmental signs as being significant in acquiring disease, this is considered unlikely (Zimmermann et al., 2011).
No significance is observed in the logistic regression looking at the presence or absence of respiratory disease and a family history of respiratory disease. For the entire current study population (n = 153, n = 1 missing) a family history of respiratory disease is reported in 15% (n = 23) of the population, no history of respiratory disease is reported in
26.1% (n = 40) of the population, but the majority of respondents reported that a family
144 history of respiratory disease is unknown 58.8% (n = 90). Given that nearly 60% of the entire study population has an unknown family history, it demonstrated the need for this information to be obtained and documented. The potential of having a data base, where all these data and family relationships are entered, will prove to be a useful tool in the future to understand the true potential of this risk factor as it relates to the disposition of certain individuals to be predisposed to respiratory disease.
It is important to point out here that for all 7 individual orangutans reported to have respiratory disease it is also reported that they have a family history of respiratory disease. Given that the majority of the population have unknown family histories, the fact that that for all of these responses affirming respiratory disease and family history, this possibly reflects investigation into these individuals histories by their respective institutions due to their disease. Another point to be made here is that the high percentage of individuals related to a father with respiratory disease is possibly indicative of the fact that in general, more male orangutans in this study population are affected by respiratory disease than females, and hence will be represented more. Additionally, the fact that female orangutans reproduce as slowly as they do, and males can reproduce more frequently than females as they may have access to multiple females, this could also lead to a bias when looking into family relatedness. Work on genetics within the captive orangutan population of North America is currently being conducted (G.L. Banes, unpublished data). In addition, research looking specifically at potential genetic predispositions in the North American captive orangutan population as it relates to respiratory disease is also currently underway. Results from these studies will elucidate
145 what role genetics and family relationships play in respiratory disease among the captive population in North America.
Most Commonly Reported Symptoms of Respiratory Disease
Signs of respiratory disease, such as air sacculitis, in orangutans are often considered subtle, making early diagnosis challenging (Cambre et al., 1980). Detecting these signs early is considered essential for successfully treating the potentially life- threatening disease of air sacculitis (Cambre et al., 1980; Lawson et al., 2006). Two forms of respiratory disease are described, acute/subacute form and a chronic form
(Spelman & McManamon, 2003). Clinical signs based on visual exams and histories for the acute/subacute forms include; lethargy, anorexia, moist cough, swelling of air sac, signs of fever, and occasional nasal discharge (Spelman & McManamon, 2003). Clinical signs for chronic disease are described based on visual exams and histories and include; history of recurring nasal discharge, congestion, intermittent cough, halitosis, dermatitis, and intermittent diarrhea (Spelman & McManamon, 2003). There are a number of different clinical signs associated with air sacculitis (Lawson, et al. 2006). Lawson et al.
(2006) report halitosis and cough being the most commonly combined signs in their study with nasal discharge being observed less often. In Wells et al. (1990) they found that nasal discharge or congestion was the most common symptom (61.9%) in their study population, followed by coughing (32.6%), change in behavior and activity levels
(16.7%), and sneezing (15.5%).
The 5 most common physical symptoms found in this study were; coughing
(82.6%; n = 19), nasal discharge (72.7%; n = 16), sneezing (69.6%; n = 16), lethargy
(56.5%; n = 13), and decreased appetite (52.4%; n = 11). The 5 most common behavioral
146 symptoms were; decreased activity level (66.7%; n = 14), change in eating habits
(55%; n = 11), change in behavior towards caregivers (35%; n = 7), change in behavior towards conspecifics (30%; n = 6), and increased agitation (35.3%; n = 6). What would appear to be mild cold-like or allergy signs could potentially reflect much more serious disease in these species. This underscores the importance of recognizing such innocuous seeming signs as something potentially much more serious. For orangutan caregivers and managers, hyper-vigilance for potential warning signs of serious disease is warranted.
Concluding Remarks
In conclusion, given the presence of respiratory disease among rehabilitant orangutans, particularly among juveniles, there would appear to be other risk factors contributing to the onset of respiratory disease, rather than long-term captive care in zoo environments, age, and body size or condition. Though currently there does not appear any discernable difference in prevalence of disease between species, at least not observable or statistically significant at this point, there does appear to be a pattern with male orangutans having a higher propensity for respiratory disease. The underlying cause for this bias is yet to be determined, though speculation could lead one to believe that overall body size and throat sac size could have some bearing. However, severity of disease, progression of disease, and age/maturity of orangutans at different stages of disease should be explored to investigate this as a decisive risk factor. Overall, recognizing that approximately 20% of captive orangutans, at least in the European population study and the current study, are directly affected by respiratory disease should be cause for continued study and research. Also of importance are the orangutans these
147 diseases affect in a more indirect way, which should also be recognized as an issue facing our captive orangutan population.
A genetic component could also exist, but again is not likely the only contributing factor to the predisposition for respiratory disease among orangutans. Again, given the presence of respiratory disease in rehabilitation centers among wild born orangutans who are not likely related to each other, at least not in the capacity as we see in captive breeding programs within zoological institutions, respiratory disease is not likely strictly genetic. However, there is a possibility that there are related individuals in these centers given dominant flanged males reproductive success within a given area, and the potential for multiple orangutans to enter these centers originating from such areas (G. L. Banes, personal communication).
To the authors knowledge, respiratory disease has not been reported in wild orangutans, though has been reported in wild mountain gorillas (Hastings, 1991; Palacios et al., 2011). The death of a wild mountain gorilla caused by a human respiratory virus has also been reported (Palacios, et al., 2011). Infectious disease, mainly respiratory related, are responsible for 20% of the sudden deaths of mountain gorillas, second only to trauma (Mudakikwa et al., 2001; as cited in Palacios et al., 2011). Respiratory disease outbreaks among wild populations of wild mountain gorillas are believed to have been caused by human-gorilla transmission (Palacios et al., 2011). Respiratory disease outbreaks have also observed among wild chimpanzees, and some thought to have been caused by human-related viruses (Kaur et al., 2008). The diagnosis of air sac infections among wild mountain gorillas is challenging due to the air sac not being obviously distended, air sacs are visible on occasion in healthy gorillas, and therefore a visibly
148 distended air sac is not always indicative of infection (Hastings, 1991). It is possible that laryngeal air sac infections are common in mountain gorillas (Hastings, 1991).
It is possible that respiratory disease just simply has not been identified by orangutan field researchers, given the often-subtle signs of disease and the distance that field researchers give the animals they are observing. Particularly with wild orangutans, those who have not previously been in rehabilitation centers or are being provisioned, respiratory disease from human contact seems unlikely given their arboreal lifestyles. It is also possible, that if wild orangutans do in fact suffer from severe respiratory disease, and succumb to their ailments, are not discovered. It is also not feasible to necropsy orangutans who are found deceased in their natural habitat to determine cause of death due to the decay rates found in the Southeast Asian rainforest, in addition to the logistics needed for these types of procedures. It would seem unlikely that respiratory disease, at the percentage that it is found in the captive population, would be an evolutionarily stable condition in wild populations of orangutans. Unless, affected orangutans are able to reproduce successfully. With the male prevalence of respiratory disease, their ability to reproduce more often than females, and their lessened life-span as compared to females, perhaps the risks of developing disease are not as severe as they would be for females in wild environments.
Future Work
Regardless of the presence of respiratory disease in wild orangutans, the high prevalence of these diseases in zoo-housed orangutans is disconcerting and is in need of further investigation. Affected orangutans who become seriously ill often need invasive and expensive medical procedures to be effectively and properly cared for. In addition,
149 the strain it can have on the psychological well-being of these individuals can also be challenging for the individual and for their social partners, often times needing to be separated from conspecifics for long periods of time during recoveries. The prevalence of respiratory disease in rehabilitation centers is now being recognized, posing new and serious issues for the facilities caring for these individuals. More work to understand the prevalence of respiratory disease among rehabilitant orangutans is needed.
The thrifty genotype hypothesis was designed to help explain the population genotype and how long-term selection influences this, and the thrifty phenotype hypothesis works to explain how plasticity in early development influences all members of a species (Wells, 2007). It is also possible that early life experiences have some influence on the susceptibility of disease. How the environment and nutritional intake during development in orangutans could possibly influence later outcomes is of interest.
Investigating species differences in weight, body size, and growth patterns using additional longitudinal weight data is also of interest. These data could be used as additional support for the thrifty genotype hypothesis in orangutans at the species level, as possibly between the sexes. These data could be used when investigating possible disease risk at various stages of development and if there are higher risks at these different stages. This would also help to elucidate if there is any type of disease progression with respect to respiratory disorders. Using these data from this study, and extrapolating from here to find ages and weights at various diagnoses would expand our understanding of how respiratory disease interacts with these variables.
Zoos worldwide have reported airsacculitis in captive primates (Cambre et al.,
1980). Respiratory disease is an important problem in the captive non-human primate
150 populations and there is a need for more information relating to air sacculitis among the captive non-human primate population (Kumar et al., 2012). Surveys to determine the prevalence of respiratory disease among all captive species of primates would provide valuable insights into the pervasiveness of disease and the threats these disease pose to these populations as a whole, both in zoos and in the large number of rescue and rehabilitation centers for primates across the globe. These data would also provide important information to investigate the preponderance of respiratory disease as it relates to morphological variations and sex differences between certain species. With more data soon to come from the field and continued data collection from zoological institutions, a better understanding of the impact respiratory disease has the orangutan population will be elucidated.
151
APPENDIX A
LIST OF CONTRIBUTING INSTITUTIONS
ABQ BioPark, Albuquerque, NM Birmingham Zoo, Birmingham, AL Brookfield Zoo, Chicago, IL Cameron Park Zoo, Waco, TX Cheyenne Mountain Zoo, Colorado Springs, CO Cincinnati Zoo & Botanical Garden, Cincinnati, OH Columbus Zoo and Aquarium, Columbus, OH Como Park Zoo & Conservatory, Saint Paul, MN Denver Zoo, Denver, CO El Paso Zoo, El Paso, TX Erie Zoological Society, Erie, PA Fort Wayne Children's Zoo, Fort Wayne, IA Fresno Chaffee Zoo, Fresno, CA Gladys Porter Zoo, Brownsville, TX Greenville Zoo, Greenville, SC Henry Vilas Zoo, Madison, WI Honolulu Zoo, Honolulu, HI Houston Zoo, Houston, TX Kansas City Zoo, Kansas City, MO Little Rock Zoological Gardens, Little Rock, AR Los Angeles Zoo and Botanical Gardens, Los Angeles, CA Milwaukee County Zoo, Milwaukee, WI Oklahoma City Zoo and Botanical Gardens, Oklahoma City, OK Omaha's Henry Doorly Zoo and Aquarium, Omaha, NE Philadelphia Zoo, Philadelphia, PA Phoenix Zoo, Phoenix, AZ Racine Zoo, Racine, WI Sacramento Zoo, Sacramento, CA Saint Louis Zoo, Saint Louis, MO San Diego Zoo, San Diego, CA Seneca Park Zoo, Rochester, NY Smithsonian's National Zoo, Washington, DC Tampa's Lowry Park Zoo, Tampa, FL The Louisville Zoo, Louisville, KY Toledo Zoo, Toledo, OH Topeka Zoo & Conservation Center, KS
152
Toronto Zoo, Toronto Virginia Zoo, Norfolk, VA Woodland Park Zoo, Seattle, WA Zoo Atlanta, Atlanta, GA Zoo Miami, Miami, FL
153
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