Relationships Among Captive Orangutan Diets, Undesirable Behaviors, and Activity: Implications for Health and Welfare

Home , Karen (orangutan)

RELATIONSHIPS AMONG CAPTIVE ORANGUTAN DIETS, UNDESIRABLE BEHAVIORS, AND ACTIVITY: IMPLICATIONS FOR HEALTH AND WELFARE

Christine M. Cassella

Submitted in partial fulfillment of the requirements

for the degree of Master of Science

Department of Biology

CASE WESTERN RESERVE UNIVERSITY

May 2012 CASE WESTERN RESERVE UNIVERSITY

SCHOOL OF GRADUATE STUDIES

We hereby approve the thesis/dissertation of

______Christine M. Cassella______

candidate for the ____Master of Science______degree*.

(signed) ____Kristen E. Lukas, PhD______(chair of the committee)

_____Patricia Dennis, PhD, DVM______

_____Mark Willis, PhD______

(date) _1/20/2012______

*We also certify that written approval has been obtained for any proprietary material contained therein.

Table of Contents

List of Tables………………………………………………………………………………………………………………….5

List of Figures……………………………………………………………………………….………………………………..6

Acknowledgements………………………………………………………………………………………………………..7

Abstract………………………………………………………………………………………………………………………….8

General Introduction…………………………………………………………………………………………………..…9

Wild vs. Captive Feeding and Activity……………………………………………………………….11

The Current Project……………………………………………………………………………………..……16

Prevalence of Regurgitation and Reingestion (R/R) in Orangutans Housed in North American Zoos and an Examination of Factors Influencing its Occurrence in One Group of Bornean Orangutans………………………………………………………………………………………………..17

Method…………………………………………………………………………………………………………….22

Prevalence of R/R in the SSP Population……………………………………………….22

Rates of R/R in a Group of Orangutans………………………………………………….23

Results……………………………………………………………………………………………………………..27

Prevalence of R/R in the SSP Population……………………………………………….27

Rates of R/R in a Group of Orangutans……………………………………………….…29

Discussion…………………………………………………………………………………………………….…..32

A Reduction of Biscuits Leads to Increased Activity and Elevated Space Use in Zoo- Housed Orangutans……………………………………………………………………………………………………..36

Method………………………………………………………………………………………………………….…39

Subjects………………………………………………………………………………………………..39

Diet Change…………………………………………………………………………………………..40

Data Collection………………………………………………………………………………….....41

Data Analysis…………………………………………………………………………………………43

Results……………………………………………………………………………………………………………..43

Behavior………………………………………………………………………………………………..43

Space-Use……………………………………………………………………………………………..45

Discussion………………………………………………………………………………………………………..47

Conclusion……………………………………………………………………………………………………………………52

Appendix ……………………………………………………………………………………………………………...... 56

A. Letter to Orangutan Institutional Representatives…………………..…………………56 B. Notice of Copyrighted Material…………………………………………………………………..57

References……………………………………………………………………………………………………………………58

List of Tables

Table 1. Individual orangutan sex, age, and weight before and after diet manipulation at

Cleveland Metroparks Zoo………………………………………………………………………….…...…….……40

Table 2. Institutional guidelines for daily orangutan diet (per animal) at Cleveland

Metroparks Zoo………………………………………………………………………………..…………………….……41

Table 3. Ethogram of selected orangutan behaviors at Cleveland Metroparks

Zoo……………………………………………………………………………………………………………………………....42

Table 4. Activity budget of orangutans at Cleveland Metroparks Zoo before and after

dietary manipulation……………………………………………………….………………………………………..…44

Table 5. Individual variation in selected behaviors of orangutans at Cleveland

Metroparks Zoo before and after dietary manipulation………………………………………..….….45

Table 6. Individual orangutan variation in time spent in the tree, on the elevated rock, or

on the ground of the exhibit at Cleveland Metroparks Zoo……...……………………..….……...47

List of Figures

Figure 1. Percent of male and female orangutans in a sample of the AZA population that

engage in R/R behavior with differences among Bornean, Sumatran, and hybrid orangutans highlighted……………………………………………………………………………………..…………28

Figure 2. Mean percent of time orangutans at Cleveland Metroparks Zoo spent feeding and engaging in R/R during each hour on exhibit…….…...……………………………………………..30

Figure 3. Cleveland Metroparks Zoo orangutans’ rate of R/R and percent of time spent feeding at 1000h and 1100h (data combined) with and without the availability of browse. Browse (n=27); No Browse (n=13). ……………………………………………………………….31

Figure 4. Individual rates of R/R of three orangutans at Cleveland Metroparks Zoo in

conditions with and without the availability of fruit. Two orangutans, Tiram and Kera,

had significantly different (p< 0.05) rates of R/R when sweet foods were not available.

Fruit (n =12); No Fruit (n = 28)……………………………………………….………………………………..…..32

Figure 5. Photograph of the orangutan exhibit at Cleveland Metroparks Zoo with

different areas of elevation highlighted……………………………………………….……………………...42

Figure 6. Percent of scans orangutans at Cleveland Metroparks Zoo spent occupying the

artificial tree in their exhibit before and after the diet manipulation…………………………...46

Acknowledgments

First, I would like to acknowledge the orangutans at Cleveland Metroparks Zoo for being my primary study subjects and I hope that some of the research I have done will be of benefit to their lives and other apes living in zoos. These red forest people have taught me a lot and I will always cherish my time with them. My deepest appreciation goes to my adviser, Dr. Kristen Lukas, for all her enthusiasm, support, and guidance. She has helped me to grow as a professional, as a person, and has encouraged me to follow my dreams. I am so thankful to have had her as an adviser, and to know her as a friend. Thanks to the other people in the Conservation & Science department that have been my family during my time here. Many heartfelt thanks to Dr. Pam Dennis for her support, academic guidance, and positivity. It has been wonderful to work with her on projects ranging from orangutans to coyotes. Thanks to the others in C&S: Dr. Mandi Vick, Kym Gopp, Gayle Albers, Laura A, and especially to my academic siblings, Elena Less, Jason Wark, and Grace Fuller. Other people to thank at the zoo include Dr. Chris Kuhar for all of his help in organizing the studies involved in this project, for statistical advice, and for his overall support of my projects. Thanks to orangutan keepers of past and present including Karen Weisenseel, Steve Kinczel, and Mary Yoder for all of their essential support. I would also like to thank Case Western Reserve University for supporting my time in this program. I have grown tremendously as a person since I first began this course of study, and I am better prepared to reach my life’s goals. Thank you to my adviser at Case, Dr. Mark Willis, for being an overall supportive and helpful figure during my time here. Finally, I am extremely grateful to my support system of family and friends that are always there for me, and have supported me through my years as a graduate student. Thank you for accepting me at all times, and for making my life beautiful even when things have been difficult.

Relationships among Captive Orangutan Diets, Undesirable Behaviors, and Activity:

Implications for Health and Welfare

Abstract

CHRISTINE M. CASSELLA

Zoo-housed orangutans are fed diets that are quantitatively and qualitatively different from the diets of their wild counterparts and, therefore, from what orangutans have evolved to eat. This discrepancy in dietary composition could be leading to health issues such as cardiovascular disease and metabolic abnormalities, weight problems, and undesirable behaviors in captive orangutans. The current study explored zoo

orangutan diets in relation to the undesirable behavior of regurgitation and reingestion

(R/R), and also examined behavioral changes after a reduction of commercially

formulated primate food (referred to as biscuits) in the orangutans’ diet at Cleveland

Metroparks Zoo. A survey of R/R in the North American zoo population found a

prevalence of 36% with some sex and species differences. Increased access to high-fiber

food reduced rates of R/R in a group of Bornean orangutans at Cleveland Metroparks

Zoo. Additionally, these orangutans increased the amount of time spent in locomotion and occupying the highest level of their exhibit after they received less commercially formulated diet. The reduction of commercial diet also resulted in weight loss in some individuals. Implications for health and welfare are discussed.

General Introduction

In natural environments, primates spend large portions of their day engaged in physical activity, oftentimes in the pursuit of high-energy food (Oates, 1987; Strier,

2003). Natural environments are inherently variable and flexible thus affecting food

availability across seasons and under different climatic conditions. Calorie and nutrient

content change throughout the year, and animals must spend much of their time

searching for, processing, and consuming food to meet energy requirements. This

situation is drastically different from the zoo environment that is characterized by

routine feeding times with energy-dense foods that can be procured and eaten quickly,

and prescribed diets that prevent fluctuations over time in calories or nutritional

composition.

The variation in natural diets makes it difficult to accurately assess the

nutritional composition of wild primate diets and even when we can, it is difficult to

know which time of year should be mimicked in the zoo environment and which

composition is nutritionally best – not just the one that animals prefer. Because of the

dearth of information on wild primate diet composition and nutrition, most zoos follow

guidelines established by the National Research Council that are compiled into the

manual, Nutrient Requirements of Nonhuman Primates (2003). The information

contained in this manual is based on research done with nonhuman primates used as models for human nutrition research and generalizes nutritional information across many different primate species. Thus, although it is not tailored to individual primate

species, it provides some sort of guideline for feeding captive primates. Exotic animal

feeding companies have used this information to create a standardized food product

(hereafter referred to as “biscuits”) that is intended to provide essential nutrients and

calories to animals. Zoos then supplement these biscuits with commercially purchased fruits and vegetables.

These guidelines make diets fairly standardized between zoos and minimize the effort needed to formulate zoo primate diets, but these standards might not be promoting the best health for the primates in zoos. The combination of high-calorie

processed biscuits, produce that has been selected for human standards, and the fact

that these foods can be gathered, processed, and eaten with minimal amounts of

physical activity involved may be resulting in undesirable behaviors and health problems

for nonhuman primates. Like humans living in industrialized societies who have seen a

rise in obesity and subsequent health issues because of a combination of energy-dense

foods and few opportunities and/or motivation for physical activity (Cordain, 2007; Stein

& Colditz, 2004), zoo-housed primates appear to be experiencing a similar fate.

Among humans in industrialized countries, obesity, which is defined as an excessive amount of body fat (Klein, Wadden, & Sugerman, 2002), is considered an epidemic that has been linked to a number of chronic diseases (Stein & Colditz, 2004). In particular, there seems to be a relationship among obesity, inflammation, type 2 diabetes, and heart disease that contribute to increased mortality (Rana et al., 2007).

Obesity and the presence of metabolic abnormalities such as elevated triglycerides,

reduced HDL-cholesterol, elevated fasting plasma glucose, and high blood pressure are

often referred to as metabolic syndrome (Alberti et al., 2006). All of these symptoms

increase the risk for developing heart disease, type 2 diabetes, and other chronic

diseases (Howard et al., 2002).

Like humans, zoo-housed orangutans are also susceptible to chronic diseases such as heart disease (McManamon, 2009) and symptoms related to metabolic syndrome have been documented in several studies of zoo-housed orangutans (Gresl et al. 2000; Schmidt et al. 2006). Other common causes of mortality in captive orangutans such as respiratory, renal, and gastrointestinal disease (McManamon, 2009) have also been associated with obesity in humans (Hoy et al., 2006; Martins et al., 2010; Hall et al., 2002; Conway & Rene, 2004; Kopelman, 2000; Murugan & Sharma, 2008; Poulain et al., 2006; John et al., 2006). The situation of orangutans in zoos may parallel that of humans in industrialized society where an overabundance of high-energy foods combined with lower activity levels can lead to obesity and increase the risk for chronic disease. It is also likely that a cycle is created where animals become overweight and are less able to exercise and therefore become increasingly unhealthy and overweight.

Wild vs. Captive Orangutan Feeding and Activity

Wild orangutans spend a large amount of their activity budget (~50%) foraging for, handling, and consuming food, especially in seasons with high fruit availability

(Mitani, 1989; Morrogh-Bernard et al., 2009; Kanamori et al., 2010, Knott, 1998). Diets consist of a diverse selection of seasonally dependent invertebrates, bark, leaves, and

fruit, and these items are consumed in different ratios at different field sites (Morrogh-

Bernard, 2009). Despite this dietary diversity, reports compiled from nine different field

sites suggest that orangutans consume 50% of their diet as fruit with leaves as the

second most common food item (Morrogh-Bernard, 2009).

Despite the high consumption of fruit, the native fruit and other diet items are much different in composition from the domestic fruit and produce fed to orangutans in

zoos (Schmidt, 2004). One of the largest differences is likely to be in fiber content. In a

detailed study of wild orangutan foods, Knott (1998) reported that neutral detergent

fiber comprised 24 – 61% of the diet, with fiber levels being highest during the non-

fruiting period when bark and leaves were the main food items. However, fiber levels

reported during the times of mast fruiting indicate that even the fruits consumed by

wild orangutans have higher levels of fiber than what is available in domestic produce

(Schmidt, 2002). Additionally, most commercial biscuits have a relatively low fiber level

because of processing constraints (Schmidt, 2004), making the overall amount of fiber

consumed by captive orangutans much lower than what they evolved to eat in the wild.

In spite of the nutritional differences between wild and domesticated fruits,

fruits are still very energy-rich foods in the wild and when available, orangutans

consume almost 100% of their diet as fruit (Knott, 1998; Bastian et al., 2010; Morrogh-

Bernard, 2009; Kanamori et al., 2010). Because ketones (products of fat metabolism)

were found in orangutan urine during non-fruiting periods, Knott (1998) hypothesized

that orangutans stored the excess energy consumed during fruiting periods for use

during times when less high quality food items were available. Thus, there is evidence

that orangutans have adapted an ability to gorge on excessive calories during times of mast fruiting and to store fat efficiently. This is a trait that would be beneficial in the wild to survive times of famine, but could easily contribute to obesity in zoo environments when high quality food items are fed daily and there is little activity to accompany their procurement. Additionally, Pontzer (2010) reported that orangutans have extremely slow metabolisms that may make it even easier for orangutans to gain weight. Overall, evidence suggests that orangutans evolved to eat a predominantly high fiber diet of leaves, barks, and stems which is supplemented by complete shifts to fruit when available to reserve as energy for use during times of less abundance.

In zoos it is recommended that caretakers feed orangutans 86% of their diet as produce and 14% as nutritionally complete primate biscuits on an as fed basis which translates to 50% biscuits and 50% produce on a dry matter basis (Schmidt, 2004).

However, as mentioned above, the fruits and vegetables fed in zoos tend to be of poorer fiber quality with higher sugar content compared with wild foods because commercially available foods have been selected for human preferences (Schmidt,

2002). While the biscuits fed to primates in zoos are an improvement on earlier zoo diets because they allow for greater control and consistency among zoos in regard to nutritional content (Ratcliffe, 1963), they have recently been under scrutiny in ape diets

(e.g. Less, 2012). This is because the biscuits are high in starch and low in fiber in contrast to the diets of wild primates, including orangutans (Hamilton & Galdikas, 1994;

Knott, 1998).

In addition to the nutritional differences, the typical zoo orangutan diet can be

consumed very quickly. Whereas wild orangutans spend a great deal of time foraging

for, processing, and eating foods, the largest source of zoo orangutans’ calories

(biscuits) can be consumed quickly and easily. Even the whole produce offered to

orangutans in zoos cannot compare to the diversity of foods available and associated

processing skills used in the wild (e.g. see Jaeggi et al., 2010). Finally, a prescribed diet

such as those offered in the zoo does not allow for the natural ebb and flow of caloric

intake that orangutans have evolved to handle.

These differences between the diets of captive and wild orangutans may play a part in the chronic diseases seen in zoo-housed orangutans and could be contributing to weight issues and undesirable behaviors. One promising area to begin investigating how diet may be contributing to these issues is to explore differences in the fiber content of zoo- and wild-orangutan diets. In humans, dietary manipulations aimed to increase fiber have resulted in health benefits such as reduced serum cholesterol, LDL- cholesterol (Trumbo et al., 2002; Kendall et al., 2010), levels of fasting blood glucose

(Sievenpiper et al., 2009), insulin (Ludwig et al., 1999), and markers of inflammation

(Jenkins et al., 2003, 2005). High fiber diets are also associated with lower levels of obesity, potentially because of reduced insulin secretion that may prevent hormonal changes that lead to weight gain (Anderson et al., 1994; Ludwig et al., 1999; Liu et al.,

2003).

In addition to the potential health concerns, the lack of fiber in zoo-housed orangutan diets may also be contributing to undesirable behaviors seen only in captive apes, and may be reduced if fiber content of the diet is increased, energy-dense foods are minimized, and/or if opportunities for prolonged feeding are provided. In particular, a behavior seen in each of the captive great apes, regurgitation and reingestion (R/R), involves the voluntary retrograde movement of food from the stomach to the mouth, hands or floor to then be re-consumed. This behavior has been reduced in gorillas and chimpanzees by providing more fibrous feeding materials (i.e. what is commonly referred to as browse – willow, hay, palm leaves, etc.) that may better mimic the nearly continuous access to high fiber foods in the wild and that also prolong the amount of time spent feeding (Baker, 1997; Struck et al., 2007). Furthermore, drastic reductions of fruit and starch along with increased fiber in zoo-housed gorilla diets have led to the elimination of R/R behavior in some individuals (Less et al., 2010).

Dietary differences are not the only major lifestyle variation between wild and zoo-housed orangutans that could be playing a part in the chronic diseases seen in zoo orangutans – wild orangutans are also likely to be more active than their zoo-housed counterparts. Although an activity budget for zoo-housed orangutans has not been published, orangutans are known to have low levels of daytime activity in zoos (Wright,

1995). Additionally, attempts have been made to increase the arboreality of zoo- housed orangutans (Hebert & Bard, 2000) which suggests that zoo-housed orangutans often spend much of their time on the ground. In the wild, orangutans are almost exclusively arboreal and thus would be engaging in physical activities such as foraging,

15 traveling, and nest building in ways that the captive environment does not usually allow.

In humans, sedentary behaviors are linked to obesity and, subsequently, risk factors related to chronic disease (Ching et al., 1998; Fung et al., 2000; Manson et al., 2004).

Additionally, there is likely a circular relationship where decreased physical activity can lead to obesity, while obesity may also be contributing to decreased physical activity (Winsier et al., 2000). If zoo-housed orangutans are already obese, this may be leading to more sedentary behaviors and it may be difficult to encourage them to use their arboreal spaces in zoos. However, it is well accepted that physical activity contributes to improved health (Haskell et al., 2007), and that activity levels are inversely related to disease outcomes including heart disease, type 2 diabetes, and obesity in humans (Burnham, 1998). Therefore, if the observed relationships between activity, obesity, and chronic disease in humans are also true in orangutans, it is possible that chronic diseases seen in zoo-housed orangutans may also be linked to or exacerbated by low activity levels and subsequent obesity issues.

The Current Project

Much research is needed to examine the relationship among diet, activity, undesirable behaviors, obesity, and health in orangutans. To begin exploring some of these concerns, the current project studied diet in relation to the undesirable behavior of R/R, with both a survey and a quasi-experimental dietary manipulation. The survey was designed to determine both the prevalence of R/R within the zoo-housed orangutan population and to discover common dietary items associated with this

behavior. In association with this survey, the diet of orangutans at Cleveland

Metroparks Zoo was manipulated to explore if there were differences in the rate of R/R when high fiber food items (i.e. browse – palm leaves, alfalfa, willow, etc.) were provided to the animals compared to conditions when these food items were unavailable. We also explored if the effects of browse changed in the presence and absence of fruit. We expected that increased access to browse would decrease the rates of R/R observed and that the highly desirable nature of fruit might lessen the effectiveness of browse as a deterrent to R/R. The second study explored behavioral changes that occurred in relation to a diet manipulation that reduced the amount of calories (mainly through a reduction of biscuits) consumed by the orangutans. It was expected that a reduction in calories, especially if accompanied by weight loss, would increase the amount of time that the animals spent active and at elevated levels of their exhibit.

Study 1: Prevalence of Regurgitation and Reingestion (R/R) in Orangutans Housed in

North American Zoos and an Examination of Factors Influencing its Occurrence in One

Group of Bornean Orangutans

Regurgitation and reingestion (R/R) is a behavior seen in several species of zoo- housed primates including gorillas (Lukas, 1999), chimpanzees (Yerkes, 1943; Baker &

Easley, 1996), gibbons (Fox, 1971), and orangutans (Maple, 1980). This behavior, which is not known to occur in these animals in the wild, refers to an individual’s self-induced and seemingly effortless movement of food or liquid from its esophagus or stomach to

its mouth, hand, or floor. The regurgitated material is then consumed again

(Strombeck, 1979; Gould & Bres, 1986; Lukas, 1999; Struck et al., 2007). R/R differs

from vomiting because it is not a reflexive action triggered by the autonomic nervous

system (Strombeck, 1979), and it differs from rumination in herbivores with compartmentalized stomachs because the anatomy of primates does not include R/R as a part of the usual digestive process (Hill, 2009).

In gorillas and chimpanzees, this behavior has been linked with a number of

potential causes including social deficits in early development (Gould & Bres, 1986),

boredom, restricted living areas, feeding frustration, or lack of control (Ruempler, 1992;

Lukas, 1999). However, most advancements in understanding and treating R/R have

come from examining differences in the diets and feeding behaviors of wild and captive

primates. For example, reviews of both chimpanzee and gorilla R/R have discussed

potential differences between wild and captive feeding opportunities that may be

related to R/R (Baker & Easley, 1996; Lukas, 1999). Wild apes spend a great deal of their

activity budget foraging for, handling, and consuming food, while zoo-housed primates

are often given several concentrated and easily consumed meals at pre-planned times

throughout the day, sometimes in the same location. Diets provided to primates in the

zoo also consist of qualitatively different food items, and therefore most zoo primate

diets are likely to vary nutritionally from the diets consumed by wild apes.

Several experiments attempting to more closely mimic wild ape diets by

increasing access to edible fibrous plant matter throughout the day have resulted in

reductions in the rate of R/R (Gould & Bres, 1986; Baker, 1997; Hill, 2004; Struck et al.,

2007; Less, 2012). Gould & Bres (1986) found that feeding browse (i.e. edible plants such as maple, beech, willow, bamboo, kudzu, and mulberry) to gorillas decreased R/R and doubled the amount of time spent feeding. Similar results have been observed in chimpanzees with increased access to browse (Baker, 1997; Struck et al., 2007). Less

(2012) has shown that R/R may even be eliminated in gorillas with certain dietary manipulations that increase access to fibrous food and prolong feeding time. In particular, R/R was eliminated in a group of gorillas (and reduced in additional gorilla groups) by removing commercially available primate food (i.e. biscuits) while simultaneously increasing the amount of leafy greens and alfalfa in gorilla diets and decreasing portions of fruit. In addition to prolonging time feeding, Less (2012) suggested that in part, this diet may have reduced R/R by being better suited to gorilla physiology and assisting in hindgut fermentation.

Like wild gorillas and chimpanzees, wild orangutans also spend a large amount of their activity budget (~50%) foraging for, handling, and consuming food, especially in seasons with high fruit availability (Mitani, 1989; Morrogh-Bernard et al., 2009;

Kanamori et al., 2010, Knott, 1998). Despite some documentation that orangutans also

engage in R/R in captive settings (Maple, 1980), research on orangutan R/R is rare, and

there is no published information on the prevalence of this behavior in zoos.

Additionally, no one has examined the relationship between feeding schedule and R/R

in orangutans, or if treatments that prolong feeding time will reduce the occurrence of

R/R as has been found in gorillas and chimpanzees. Although Tripp (1985) explored the

19 effects of browse on orangutan activity levels, there was no report of any impact that browse had on undesirable behaviors such as R/R.

While differences in feeding-related activity budgets between zoo-housed and wild orangutans are important, we should also consider the composition of the diet. We may come to understand more about R/R if we learn what types of food animals most frequently regurgitate, and think about this in relation to what is consumed or preferred by wild animals. Ruempler (1992) saw reductions in gorilla R/R after the removal of fruit from the diet and Less et al. (2010) eliminated R/R in gorillas fed a diet high in fiber and low in fruits and starches. Similarly, Lukas et al. (1999) showed reductions in R/R when milk was removed from the diet. These diet manipulations are all similar in that they reduced access to food items that are highly concentrated in simple sugars (i.e. fruit and milk), which are highly preferred over fibrous foods in chimpanzees and gorillas (Remis,

2002). Given that orangutans can taste sweet compounds in smaller concentrations than either chimpanzees or gorillas (Simmen & Charlot, 2003), and fruits are preferred over more fibrous foods in the wild (Hamilton & Galdikas, 1994; Bastian et al., 2010;

Kanamori et al., 2010), they are also likely to prefer simple sugars to fibrous foods in zoos.

In the wild, simple sugars would be limited in availability, but preferred as a beneficial energy resource (Hladik & Simmen, 1997). In zoos, the fruits we offer are very high in simple sugars (Schmidt, 2002). The high desirability and low availability of these food items in a zoo diet, coupled with an absence of other foods or enrichment

activities, may make R/R more likely after a meal containing food items concentrated

with fructose, glucose, lactose, or sucrose as a way to simulate further consumption of these desirable food items.

It is important to study R/R in captive apes because it is a behavior that has

never been seen in wild apes and therefore may indicate that we are not properly

addressing some individuals’ needs. R/R may be considered an abnormal behavior

under the definition that abnormal behaviors differ in pattern, frequency, or context

from those that would be shown by other members of the species in conditions allowing

for a full behavioral range (Broom & Johnson, 2000). In other words, captivity may

restrict an individuals’ ability to eat and engage in activities in ways that they would in

the wild and this may be leading to the demonstration of R/R behavior.

Additionally, R/R is unsightly to the public, and there is some potential for R/R to

lead to health complications. R/R in captive apes is similar to a disease seen in humans

called Human Rumination Syndrome (HRS) (American Psychiatric Association, 1994).

Although there is not currently any evidence for health complications associated with

R/R in captive apes, humans with this disorder often suffer from dental erosion,

esophageal dysfunctions, and ulcers that may be associated with continually

regurgitating stomach acid. Hill (2009) found that regurgitant from gorillas was more acidic than the original food consumed and thus the risks involved with HRS may also be present for zoo-housed primates that R/R.

One goal of the research presented here is to begin the discussion of R/R in

orangutans by determining the prevalence of R/R in the Association of Zoos and

Aquariums Species Survival Plan® (SSP) population and to explore the possibility that specific items in the diet can be associated with the behavior. In addition, we examined general trends of R/R in one group of zoo-housed Bornean orangutans. In particular, we were interested in the relationship between R/R and feeding schedule and if the availability of browse affected the rate of R/R and percent of time spent feeding. We also looked for differences in individual rates of R/R in conditions where fruits were or were not available. We hypothesized that the behavior of R/R is related to the diet fed to the orangutans at Cleveland Metroparks Zoo. In particular, we predicted that: 1) R/R would increase at times when the orangutans had access to food; 2) R/R would decrease and time spent feeding would increased in conditions where browse was available; and

3) R/R would be higher during times when the diet included preferred food items (i.e. fruit).

Method

Prevalence of R/R in the SSP Population

Every SSP institutional representative (IR) for orangutans (n=53) was solicited to participate in a survey to determine the prevalence of R/R in the orangutan population.

Thirty-five IRs responded for a response rate of 66%. This response represented 154 orangutans (out of a population of 226). Within this group, 54 were male and 83 were female. Forty four animals were Sumatran (Pongo abelii), 60 were Bornean (Pongo

pygmaeus), and 33 were hybrids. The survey requested that the IR rate the R/R

behavior of each orangutan at his or her institution, or to pass the survey along to an

individual that could best report the information. We asked that each orangutan’s R/R

behavior was rated with a number corresponding to the following scale:

1) Frequently – the animal engages in multiple bouts of R/R per day

2) Often – the animal engages in R/R at least once per day

3) Sometimes – the animal engages in R/R several times per week or in response to

certain food items

4) Never – the animal has never been observed to R/R

5) Don’t know – there is not sufficient information to report on R/R behavior in this

animal

Respondents were also asked to indicate if there were any foods that were commonly associated with the behavior (see survey in Appendix A). Data are reported as the percent of animals that engaged in the behavior out of the entire population, and out of specific subsets (i.e. sex, species). We also used SPSS 12.0® for Windows® to run

Pearson Chi-Square tests to look for differences in the prevalence of R/R between sexes and among the species.

Rates of R/R in a Group of Orangutans

Subjects were four Bornean orangutans (Pongo pygmaeus) housed at Cleveland

Metroparks Zoo including one adult male (24 yrs), one adult female (22 yrs), and two

subadult females (11 and 9 yrs). A fifth group member was present but not analyzed

because of his age (three yrs). All subjects were housed together on-exhibit and in

adjacent holding cells when off-exhibit (the adult female and three-year old male shared

a holding cell).

Between 1000 and 1700h, the orangutans occupied an indoor, semi-naturalistic

exhibit with a large rock structure and attached climbing tree, and a waterfall. Each

evening, the orangutans transferred to their holding cells. The orangutans were fed a

morning meal at approximately 1000h and an evening meal around 1700h. An

afternoon snack was fed around 1400h. Meals varied by keeper, but generally consisted

of commercial primate biscuits (Lab Diet – 5038 Monkey Diet), vegetables, and some

fruit.

We wanted to document the pattern of R/R throughout the day, and therefore

conducted observations during all hours that the animals were on-exhibit. We classified

observations as occurring during one of seven on-exhibit time periods (1000h, 1100h,

1200h, 1300h, 1400h, 1500h, and 1600h), and we collected four observations during

each of these time periods. This resulted in a total of 140 observation sessions (4

observation sessions x 7 time periods x 5 days a week). Because the observation

sessions were 30 min long, this resulted in 70 hrs of total observation time. The day and time of observations were selected randomly. These data were collected by a total of three observers, who obtained inter-observer agreement with 90% reliability. Data

were collected from June through November of 2009.

To make this study as low-impact as possible on other zoo staff, all conditions

were implemented opportunistically. Therefore, these data represent how the orangutans behaved under the usual conditions offered by the zoo and nothing was manipulated. Instead, we created conditions opportunistically by recording whether or not browse was available to the orangutans. In this study, browse included edible

materials such as hay, alfalfa, willow, maple, or palm leaves. Out of 140 observations, browse was available during 100 observations (71%). It is important to note that browse was typically provided early in the day (before the orangutans came onto exhibit) and thus was at its highest quality (i.e., it had not gotten wet, mixed with excrement, etc.)

and quantity during the morning, even though the orangutans may still have been

classified as having browse during later observations. For this reason, the analyses

exploring the relationship between browse, feeding, and R/R were only done on data

collected during the first two hours that the orangutans were on exhibit (n=40). Browse

was available during 27 of these observations.

We also recorded whether or not fruits were available during this time of day.

Fruits were generally oranges, apples, and bananas, but a fruit flavored Popsicle was

also considered a fruit during one observation. Fruits were available during 12 of the observations. Other food items (such as commercial biscuits) were generally fed before or after the animals were on exhibit, but there were days that vegetables such as green beans, carrots, or romaine lettuce were provided. However, these food items were not included in these analyses.

We used group-scan sampling of behavior at 2-min intervals for individuals in a

focal group during 30-min observation sessions. Categories for behavior were

exhaustive and mutually exclusive. The only behavior on the scan-sampling ethogram

that is presented here is feeding behavior, which was defined as the consumption or

processing of food and/or browse. We also used all-occurrence sampling of R/R

behaviors. We recorded pre-R/R behaviors and confirmed R/R because the orangutans

often regurgitate into their mouths making it difficult to observe reingestion from a

distance (in contrast to gorillas who only regurgitate into a closed mouth 8% of the time;

Lukas et al., 1999).

However, previous observations of this orangutan group in their holding area

allowed for identification of several behaviors that have been observed to occur in relation to R/R. These behaviors include: (1) firm and repeated palpitations of the abdomen with the animal’s hands combined with (2) a lurching movement that

characteristically preceded regurgitating. These behaviors have also been observed to occur before R/R in gorillas (Lukas et al., 1999). When these behaviors were observed they were scored as R/R. We also scored R/R if we saw animals spitting up and consuming regurgitated materials without seeing the characteristic pre-R/R behaviors. If pre-R/R behaviors and R/R were observed in sequence, this was only counted as one bout. There are no published reports that quantify how often pre-R/R behaviors precede actual R/R in orangutans. As such, the results should be interpreted with this in mind – some bouts of R/R could have been counted where only pre-R/R behaviors occurred.

Scan-sampling data were summarized for each individual as the percent of total scans in which feeding occurred (plus or minus the standard error). The mean of the individual scores was used to report the group’s percent of time spent feeding. For all- occurrence data, we report the average of total R/R bouts observed per hour for the group, and also as individual averages across observations. Although the data were not normally distributed and are from a small sample size, paired t-tests were run to compare individual means between conditions with and without browse as these tests are robust to violations of distribution when comparing means (Kuhar, 2006). Cohen’s d was also calculated for each paired t-test. Cohen (1988) suggested that d values of .2 indicate a small effect size while values >.5 indicate a medium-sized effect, and >.8 indicate large effect sizes. Mann-Whitney Rank Sum tests were run to compare data for single individuals between conditions with and without fruit. For these tests, the number of observations was used as the sample size.

Results

Prevalence of R/R in the SSP Population

Of the 154 orangutans represented by this survey, there was an overall prevalence of R/R behavior of 32%. However, we observed that the youngest orangutans to R/R were five years of age. After removing animals four years of age or younger, the prevalence became 36% (n=137). Females have a significantly higher prevalence of R/R than males at 42% compared with 26% [X2(2, N = 137) = 3.76, p=0.05].

Data were also analyzed by looking at the prevalence of R/R within each species. There

was a significant difference among the species [X2(2, N = 137) = 8.79, p=0.012].

Sumatran orangutans had the lowest prevalence of R/R at 18% while Borneans and

Hybrids were at 45% and 42% respectively (see Figure 1).

Figure 1. Percent of male and female orangutans in a sample of the AZA population that engage in R/R behavior with differences among Bornean, Sumatran, and hybrid orangutans highlighted.

Of the animals that engaged in R/R, there were notable differences in how often they displayed the behavior. Animals that were described as engaging in R/R

“Frequently” made up 24% of the population, while those that “Often” R/R comprised

16%. Most animals (59%) that engage in R/R only demonstrate the behavior

“Sometimes”. Of the animals that have never been observed to R/R (64% of the population), only 3% were classified as “Don’t Know” while the others (97%) were classified as “Never” engaging in R/R.

In addition to the scale to determine the prevalence of R/R behavior, the survey

asked respondents if there were food items that the orangutans prefer to R/R. Of the

41 responses to this question, the most common response indicated that fruit and other

sweet items are thought to be associated with R/R (78% of responses). Seven percent of

respondents indicated that R/R is associated with favored food items. Additional responses that were only mentioned a single time each included: biscuits, pasta, novel items, “after every meal”, “when food is gone”, and “not sure”.

Rates of R/R in a Single Group of Orangutans

To more closely examine factors associated with R/R in orangutans, percent of

time spent feeding and rates of R/R were recorded in a single group of Bornean

orangutans at Cleveland Metroparks Zoo (see Figure 2). Feeding was the highest at

1000h (32.56% + 4.53) and remained fairly low throughout the rest of the day, although

there was a small increase in this behavior consistent with the afternoon snack at 1400h

(15.32% + 4.69). The group rate of R/R per hour appeared to be related to the feeding

schedule as there was a peak at 1000h (7.4 bouts per hour + 2.36) and again after the afternoon snack was provided at 1400h (3.4 bouts per hour + 2.42) and 1500h (5.6

bouts per hour + 2.96).

Figure 2. Mean percent of time orangutans at Cleveland Metroparks Zoo spent feeding and engaging in R/R during each hour on exhibit.

Overall, the group engaged in an average of 3.53 (+ 2.07) bouts of R/R per hour

of the day. To explore the effects of browse on the rate of R/R, data from 1000h and

1100h were combined and used for this analysis because browse, when it was available, was at its peak quality and quantity at this time. Availability of browse reduced the group’s total bouts of R/R by roughly half from 8.77 (+ 2.75) bouts per hour to 4.07 (+

2.01) bouts per hour (Figure 3). Despite the group’s reduction in R/R, the paired t-test comparing individual means of R/R rates was not statistically significant (t(3) = 1.35, P =

0.26, d = 0.57), but the power of this test was very low (0.10). Combined with a medium effect size as indicated by Cohen’s d, this test should be interpreted cautiously and with the small sample size in mind. However, there was a significant increase in time spent feeding (t(3) = -5.339, P = 0.013, d = 2.94). The power of this test was exceptionally high

(0.92), and Cohen’s d indicates that there was a large effect. Without browse available, the orangutans spent an average of 7.06% (+ 1.90) of time at the 1000h and 1100h 30

feeding. This nearly tripled to 20.99% (+ 2.29) of time when browse was available

(Figure 3).

Only three of the four subjects engaged in R/R during this time of day. In general, we observed that R/R was higher in conditions where fruit was present (see

Figure 4). The adult male’s (Tiram) average rate of R/R was 2.29 (+ 0.23) bouts per hour when fruit was not present and 7.83 (+0.77) bouts per hour when fruits were available.

This result was statistically significant [T=379.50; df = 12(fruit), 28(no fruit); P = 0.005].

There was also a significant difference in one of the adolescent females [Kera: T =

333.00; n= 12(fruit), 28(no fruit), P = 0.038]. When fruits were not available, she

engaged in R/R at a rate of 0.57 (+ 0.09) bouts per hour which increased to 2.67 (+ 0.33)

bouts per hour when fruits were in the enclosure.

Figure 4. Individual rates of R/R in three orangutans at Cleveland Metroparks Zoo in conditions with and without the availability of fruit. Two orangutans, Tiram and Kera, had significantly different (p< 0.05) rates of R/R when fruits were not available. Fruits (n =12); No Fruit (n = 28).

Discussion

The results reported here are the first to document the prevalence of R/R behavior within the SSP population of orangutans. The prevalence of R/R in orangutans that have reached an age where R/R is observed (>4) was reported as 36% which is less than the reported prevalence of R/R in the zoo-housed gorilla population of around 65%

(see Lukas, 1999 for review). However, a prevalence of 36% indicates that this behavior is happening in over 1/3 of zoo-housed orangutans and therefore it deserves further exploration. Furthermore, there are specific subsets of the population that have a higher prevalence of R/R. There was a statistically significant difference found between

32 the species and between females and males. An additional consideration is that this behavior may be more difficult to detect in orangutans than in gorillas or chimpanzees.

The orangutans observed in the second half of this study often regurgitated into their mouths and the behavior might have been missed if an observer was not aware of the behaviors that typically accompany R/R.

In addition to the survey, and despite the limitations of a small sample size, this study was the first to quantify the rate of R/R in a group of orangutans, to look at a relationship between feeding schedule and R/R, and to examine the influence of browse and fruit on this behavior. Rates of R/R were highest when the orangutans first came on exhibit at 1000h and peaked again at 1500h. These high rates of R/R coincided with the feeding schedule as the animals had either just entered an exhibit containing food, or had recently received an afternoon snack. Additionally, although not statistically significant, the group’s total rate of R/R was reduced in half when browse was provided.

This was accompanied by a significant increase in time spent feeding. Similar results demonstrating an increase in feeding and decrease in R/R with browse have been observed in gorillas and chimpanzees (Baker, 1997; Struck et al., 2007). The results reported here suggest that a similar pattern may hold true for orangutans. Traditional feeding conditions of zoos where meals are offered at pre-determined times may frustrate feeding motivation in animals that spend much of their time foraging in the wild. As such, R/R may have developed as a way to artificially prolong the amount of time spent exhibiting feeding behavior (Lukas, 1999). Zoos that work to prolong feeding

time through use of browse may help to minimize undesirable behaviors that may be

related to feeding frustration, such as R/R.

Although provisioning with browse may help to reduce R/R by prolonging time spent feeding, R/R may still be likely to occur in response to particularly desirable food items, even if browse is available. A potential reason that the reduction of R/R observed here was not statistically significant is that the presence of fruit may have lessened the effectiveness of browse as a way to decrease R/R when it was available.

That is, the animals may have preferred to R/R fruit as a way to prolong feeding behavior with a desirable food item rather than to prolong feeding in general by consuming browse.

Two of the three animals in this group that engage in R/R had significantly higher levels of R/R when fruits were present. Reports from the survey are consistent with this observation. A majority of respondents (78%) reported that fruit and other sweet items are present when animals are engaging in R/R. It appears that orangutans are more likely to choose to regurgitate desirable and sweet food items rather than to engage in this behavior just because they are bored or have learned the behavior from another animal, although these factors are likely to contribute to the onset of R/R, its frequency, and maintenance over time. That is, boredom might still play a role in whether or not an animal engages in R/R, but we now have evidence that the animals may be choosing certain foods to R/R. The combination of these variables should be explored further in future research.

The finding that fruit and sweet foods are often involved in orangutan R/R makes

sense given that wild orangutans prefer fruit over other food matter (Bastian et al.,

2010; Hamilton & Galdikas, 1994) and will consume as much as 100% of their diet as fruit if that is available (Kanamori et al., 2010; Knott, 1998). Orangutans can also detect sweet tastes at low thresholds (Simmen & Charlot, 2003), and the especially high sugar content of commercially available fruits (Schmidt, 2002) may make them particularly desirable to re-consume via R/R. A preference for energy-dense foods like fruit is adaptive to wild orangutans because the extra calories can then be stored as energy for use during periods when less high-quality food is all that is available (Knott, 1998).

However, when fruits are fed in limited amounts so that captive orangutans do not gain weight, and especially in the absence of other food or enrichment activities, R/R may be a behavior that can both prolong feeding time and act as a way to simulate eating more fruits. Interestingly, when foods that are likely to be preferred such as fruit and milk have been removed from the diets of gorillas, R/R has been reduced (Ruempler, 1992;

Lukas et al., 1999) or even eliminated (Less et al., 2010).

Orangutans use less energy relative to their body mass than most other eutherian mammals (Pontzer et al., 2010) and evolved in an environment where gorging on high energy foods when available is advantageous to survive periods of low fruit availability (Knott, 1998). The combination of these unique adaptations makes managing zoo-housed orangutans particularly difficult when trying to prevent obesity.

The findings of the current study add background on orangutan R/R to the literature and pose new avenues of study. The results presented here are not intended to influence

zoo managers to remove fruit from orangutan diets, or to provide unlimited amount of

fruits. Before diet recommendations are made, further research is needed to

understand the interplay of variables that influence R/R and how we can reduce its

occurrence.

It is likely that combined dietary and environmental manipulations resulting in a

more naturalistic diet and more behavioral options will be necessary to permanently reduce rates of R/R. Future research should systematically explore the impact of offering browse, fruit, and the combination of these foods on orangutan R/R to see if fruits truly interfere with the effectiveness of browse as a way to decrease R/R. If fruits continue to elicit higher levels of R/R, more research should explore what qualities of fruit contribute to increased R/R and how we can better manage diets and other aspects of husbandry to limit its occurrence and promote more species-typical behavior.

Study 2: A Reduction of Biscuits Leads to Increased Activity and Elevated Space Use in

Zoo-Housed Orangutans

Caretakers of zoo-housed orangutans are often interested in ways to increase activity levels and arboreality in their animals. In an attempt to address this, several studies have explored the effect of novel, varied, and manipulable enrichment options on zoo-housed orangutan activity with results indicating that these enrichment options can successfully increase time spent active (Wilson, 1982; Tripp, 1985; Perkins, 1992;

Wright, 1995). Few research studies have investigated how to increase time spent at elevated exhibit levels in zoo-housed orangutans but elevated space use has been

increased by flooding the floor of an orangutan exhibit (Hebert & Bard, 2000).

Additionally, though less arboreal in the wild than orangutans, studies have

documented that gorillas and chimpanzees both utilize elevated areas of their exhibit,

and chimpanzees are more likely to occupy elevated areas of their exhibit than would be

expected by chance (Ross & Lukas, 2006). This suggests that there may be a lack of

appropriate elevated options for zoo-housed orangutans that is necessitating an

increased use of terrestrial space in zoos. However, this has not been explored.

Another consideration in analyzing zoo-housed orangutan activity and space-use

patterns is that they often weigh more than their wild counterparts (Cocks, 1998; Leigh,

1994). Although we do not yet have a reliable way to classify whether or not orangutans are obese, obesity has been discussed as an issue by orangutan experts

(Maple, 1980; Mayo, 2009), in relation to orangutan health concerns (e.g. Murphy,

2009; Schmidt et al., 2006; Gresl, Baum, & Kenmitz, 2000), and in relation to their

unique energetic adaptations (Knott, 1998; Pontzer et al., 2010).

In addition to the health concerns that may be associated with obesity, it is

possible that excess fat mass could be contributing to lethargy and increased terrestrial

behavior. Although lack of exercise and inactivity are often associated with obesity, it is

unclear whether inactivity causes obesity and/or if obesity contributes to inactivity. In a

study of human females, Weinsier et al. (2000) reported that weight loss improved the participants’ physiologic capacity for exercise. Thus, it is possible that reducing the weight of zoo-housed orangutans could lead to increased activity because it may be

easier for orangutans to climb upwards when carrying less body mass. If orangutans

were to increase their activity in zoos this would likely benefit their health (Haskell et al.,

2007) and increased activity could also attract more zoo visitors to orangutan exhibit spaces. Zoo visitors are more interested in viewing active animals (Bitgood et al., 1988;

Mitchell et al., 1992; Fernandez et al., 2009).

The current study tested the hypothesis that a diet manipulation, especially if it resulted in weight loss, would increase activity (i.e. time spent locomoting) and the amount of time orangutans spent at elevated exhibit levels. The hypothesis was explored opportunistically in response to management decisions to alter the orangutans’ diet. Their diet was altered because of concerns for the health and weights of the adult male and female of the group in particular. Management aimed for orangutan weights to be approximately 10% higher than what has been reported for wild orangutans so that the male would weigh approximately 95 kg (instead of 125 kg) and the female 50 kg (instead of 72 kg). The reported average weight for adult Bornean males in the wild is 86.3kg (range of 80 – 91 kg) and 38.7 kg (range of 33 – 45 kg) for females (Markham & Groves, 1990). The group’s activity budgets and space-use data were compared before and after the diet change that led to weight loss in three of the four animals studied.

Method

Subjects

The subjects included one male and three female Bornean orangutans housed at

Cleveland Metroparks Zoo. At the beginning of the study, the male was 23 years old,

and females ranged from 7-22 years of age (see Table 1). A three-year old male was also

in the group, but was not included in the analysis because of his age and noticeably

different activity budget. The adult male and female are a breeding pair, and the 7-

year-old female is one of their offspring (the three-year-old male being the other). The

10-year-old female is unrelated. Pre- and post-diet weights included in Table 1 are the average of three values recorded closest to the beginning of behavioral data collection periods. The adult male lost 32.3 kg after the diet manipulation and the adult female lost 21.4 kg. Their final weights were very close to the target weights (i.e. 10% above the average reported weight for wild orangutans) of 95kg and 50kg for the male and female respectively. The other individuals were not targeted for weight loss, but the unrelated 10-year old female (Kera) lost 5kg while the female offspring (Kitra) did not lose any weight.

No other notable changes in husbandry were made.

TABLE 1. Individual orangutan sex, age, and weight before and after diet manipulation at Cleveland Metroparks Zoo

Adult Male Adult Female Adolescent Female Adolescent Female Tiram Kayla Kera Kitra Age Weight (kg) Age Weight (kg) Age Weight (kg) Age Weight (kg) Pre-Diet 23.5 125.5 22.0 72.3 10.5 49.5 7.0 41.4 Post-Diet 25.0 93.2 23.5 50.9 12.0 44.5 8.5 41.4 Weight Difference -32.3 -21.4 -5 0

Diet Change

The diet was first modified in January of 2010 when management requested

animal keepers to better follow established dietary guidelines for feeding orangutans in

their holding area (see Table 2). In particular, there was a focus on ensuring that Tiram

and Kayla, the two adult animals that were believed to be overweight were fed proper

portions of food. In particular, keepers were asked not to provide fruits and vegetables outside of the daily guidelines (i.e., extra food should not be provided as rewards for training, but should be within the diet), and to reduce the amount of biscuits (Lab Diet

5038 – Monkey Diet) by using better methods of measurement. Keepers were to provide 4 cups of biscuits to each of the animals. For this diet change, keepers were

instructed to measure the food more precisely, and not to use rounded cups. These instructions changed the amount of biscuits from ~1 lb of biscuits with heaping scoops

(pre-diet) to ~0.6 lbs of biscuits with a level scoop (post-diet), representing a reduction of ~520 calories from pre-to post-diet. Although there is not an accurate way to determine the caloric reduction achieved from following vegetable and fruit provision

40 guidelines, there was likely a reduction in calories in this regard, too. However, it was likely much less than the decrease of ~520 calories of biscuits.

No other changes were made to diet composition or presentation of food.

TABLE 2. Institutional guidelines for daily orangutan diet (per animal) at Cleveland Metroparks Zoo Orangutan Diet 4 Cups Monkey Biscuits 1/4 - 1/2 medium orange 1 - 1 1/2 medium apple 15 grapes 1/2 - 1 banana 1 - 1 1/2 medium carrot 1/2 - 1 bunch celery 1/2 - 1 bunch greens 1/4 - 3/4 large yam Browse not to exceed 10% of total diet

Data Collection

Behavioral observations were conducted between June and September of 2009

(pre-diet phase), and again between January and March of 2011 (post-diet phase).

Thirty observations were collected during each phase. Observation periods lasted for

30-minutes. In each phase, two observations were taken in each of three time slots

(morning = 1000h – 1230h; mid-day = 1230h – 1500h; afternoon = 1500h – 1700h) on

Mondays through Fridays.

We used group-scan sampling of behavior and location at 2-min intervals for individuals in the focal group. Categories for behavior were exhaustive and mutually exclusive. The ethogram used is listed in Table 3. 41

TABLE 3. Ethogram of selected orangutan behaviors at Cleveland Metroparks Zoo Behavior Definition Locomote moving from one area of the exhibit to another (more than one body length) Social interaction between two or more animals Feed consumption of food or browse

Nest Building manipulation of materials such as burlap sacks to form a platform for laying or sitting; covering one's head with materials Autogroom manipulation of animal's own fur/body/skin Undesirable regurgitation and reingestion of food; hair plucking; coprophagy; glass licking Active Other any behavior not listed but performed without being sedentary Inactive sedentary behavior while awake or asleep Not Visible animal cannot be seen on scan

Animals were also recorded as being in one of three locations including: (1) the

ground, which included the cement floor and artificial logs and rocks lying on the ground, (2) a large artificial rock that was considered an elevated location, and (3) an artificial tree (including the attached ropes) that was considered the most elevated location. Animals could also be recorded as not visible (see Figure 5).

Figure 5. Photograph of the orangutan exhibit at Cleveland Metroparks Zoo with different areas of elevation highlighted. 1 corresponds with the ground that included artificial logs and rocks lying on the ground; 2 corresponds with the large elevated rock; and 3 is the artificial tree (including the attached ropes). 42

Data Analysis

Scan-sampling data were summarized for each individual as the mean percent of

scans in which a behavior occurred in the pre-and post-diet manipulation phase. The

same method was used for calculating percent of scans spent in various locations.

Additionally, group means were calculated by averaging individual means for each

behavior or location of interest. Data were checked for normality using the Kolmogrov-

Smirnov test – some behaviors were normally distributed while others were not.

Despite this, we chose to run paired t-tests to look for differences in group behavior before and after the diet manipulation, because these tests are robust to violations of normality when comparing means (see Kuhar, 2006). For these tests, the sample size was four. Additionally, descriptive statistics of individual animal behaviors and locations are presented. This was done in order to compare behavioral and space-use changes among the animals since only some were targeted for weight loss. These results can help us to understand if changes in the group were based solely on weight loss, or if the diet change altered behavior independent of weight loss. Tests were run with

SigmaStat® 3.0 and alpha was set at 0.05.

Results

Behavior

Comparisons of the group means for each behavior observed before and after the diet change are listed in Table 4. In both phases, the animals were not visible, inactive, and feeding for the largest portions of time (see Table 4). However, time spent

43 locomoting increased to a level that nearly matched the amount of time the animals spent feeding (from 5.5% to 15.4%) in the post-diet phase. A paired t-test revealed significant group changes in three behavior categories: locomote (t = -3.64, df = 3, P =

0.04), social (t = 3.92, df = 3, P = 0.03) and inactive (t= 9.14, df = 3, P = 0.00).

TABLE 4. Activity budget of orangutans at Cleveland Metroparks Zoo before and after dietary manipulation Pre-Diet mean % of Scans Post-Diet mean % of Scans Behaviors (S.E.) (S.E.) P-value Locomote 5.48 (1.07) 15.4 (1.79) 0.04* Social 9.29 (2.77) 4.28 (1.46) 0.03* Feed 14.2 (3.93) 15.8 (4.31) 0.78 Nest Building 1.73 (0.72) 1.78 (0.74) 1 Autogroom 4.7 (1.4) 0.83 (0.56) 0.11 Undesirable 0.48 (0.44) 1.78 (0.68) 0.17 Active Other 0.18 (0.14) 0.24 (0.26) 0.55 Inactive 28.4 (2.74) 34.6 (3.71) 0.00* Not Visible 35.4 (3.47) 24.9 (3.26) 0.34 * indicates significant at p<0.05.

As hypothesized, the diet change resulted in a significant increase in time spent locomoting. The group’s mean time spent in this behavior tripled from 5.48 (+1.07) percent of scans to 15.4 (1.79) percent of scans. Unexpectedly, the group’s mean percent of scans spent social decreased significantly from 9.29 (+2.77) to 4.29 (+ 1.47) percent of scans. Contrary to the hypothesis, time spent inactive increased significantly from 28.39 (+ 2.74) to 34.64 (+ 3.71) percent of scans.

Individual variation in the behaviors that were significantly different are displayed in Table 5. All four of the orangutans, regardless of whether or not they lost

weight, followed the same trend in each behavioral category (increase in locomotion, decrease in time spent social, increase in inactivity).

TABLE 5. Individual variation in selected behaviors of orangutans at Cleveland Metroparks Zoo before and after a diet change.

% of Scans Pre- % of Scans Post- Behavior Subject Diet (SE) Diet (SE) Locomote Adult Male (Tiram) 7.38 (0.22) 18.57 (0.51) Adult Female (Kayla) 2.14 (0.17) 14.99 (0.43) Adolescent Female (Kitra) 5.24 (0.28) 19.05 (0.57) Adolescent Female (Kera) 7.14 (0.25) 9.05 (0.42) Social Adult Male (Tiram) 10.71 (0.68) 5.71 (0.31) Adult Female (Kayla) 5.48 (0.39) 1.43 (0.15) Adolescent Female (Kitra) 3.33 (0.28) 2.14 (0.25) Adolescent Female (Kera) 11.43 (0.66) 5.24 (0.31) Inactive Adult Male (Tiram) 45.47 (0.93) 49.76 (0.89) Adult Female (Kayla) 19.76 (0.59) 26.67 (0.64) Adolescent Female (Kitra) 35.71 (0.76) 43.09 (0.97) Adolescent Female (Kera) 12.62 (0.63) 19.04 (0.52)

Space-Use

Amount of time spent occupying various levels of the exhibit was also compared before and after the diet manipulation. The percent of scans spent at the most elevated level of the exhibit, the artificial tree, increased significantly for the group from 4.82 (+

1.49) to 9.62 (+ 2.83) percent of scans (t= -5.26, df = 3, P = 0.01). This was the only

significant change in the group’s space-use, but supports the hypothesis that use of elevated exhibit levels would increase after the diet manipulation. This change in behavior was observed in all four animals (see Figure 6 and Table 6).

10 SE) Tree on SE)

+ 8 Pre-Diet 6 Post-Diet

4 % of% Scans ( 2

0 Tiram Kayla Kitra Kera Group Avg.

FIGURE 6. Percent of scans spent occupying the tree before and after the diet manipulation.

There was a group trend toward increased use of the second highest level of the

exhibit, the elevated rock. The group mean increased from 23.34 (+ 3.46) percent of

scans before the diet manipulation to 27.70 (+ 2.91) percent of scans after the diet

manipulation. There was also a group trend toward reduced time spent on the ground level of the exhibit which went from 33.63 (+3.55) percent of scans before the diet

change to 20.79 (+3.07) percent of scans after the diet change (Table 6). All individuals

but the adult female followed these trends in elevated rock and ground use.

TABLE 6. Individual orangutan variation in time spent in the tree, on the elevated rock, or on the ground of the exhibit at Cleveland Metroparks Zoo.

Pre-Diet % of Post-Diet % of Location Subject Scans (+ SE) Scans (+ SE) Tree Adult Male (Tiram) 0.24 (0.04) 3.22 (0.42) Adult Female (Kayla) 3.33 (0.34) 10.60 (0.60) Adolescent Female (Kitra) 5.71 (0.35) 10.60 (0.50) Adolescent Female (Kera) 9.99 (0.44) 14.06 (0.63) Elevated Rock Adult Male (Tiram) 3.33 (0.36) 11.52 (0.70) Adult Female (Kayla) 25.48 (0.85) 19.12 (0.59) Adolescent Female (Kitra) 18.81 (0.59) 27.19 (0.51) Adolescent Female (Kera) 49.76 (0.91) 52.99 (0.84) Ground Adult Male (Tiram) 90.71 (1.16) 82.94 (1.46) Adult Female (Kayla) 12.62 (0.97) 47.92 (1.47) Adolescent Female (Kitra) 25.48 (1.08) 31.33 (1.04) Adolescent Female (Kera) 21.66 (1.21) 6.68 (0.45)

Discussion

A diet manipulation involving a reduction of calories that resulted in weight loss

in three (of four) animals significantly increased the group’s locomotion behavior and

time spent at the most elevated level of the exhibit. These findings support the

hypothesis that a calorie-reducing diet modification (mostly obtained through a

reduction of biscuits) would increase activity and elevated space use, although this may have occurred through some mechanism other than what was originally expected.

Initially, the hypothesis that activity and space use would change was formed under the assumption that the diet might result in weight loss that could make it easier for the

animals to move and reach higher levels of the exhibit if they were at a weight closer to

that observed from orangutans in the wild. The individual data from the adult male and female who were targeted for weight loss support this idea – they both increased the amount of time spent locomoting and occupying the highest level of their exhibit.

However, the two adolescent females also followed this trend in space use and behavior. One did lose a small amount of weight (5 kg) after the diet change, but the other did not lose any weight. There are several potential explanations for these changes in behavior: (1) the change in the mature animals’ behavior affected the

adolescent females’ behavior because primates are social animals (and especially in the

case of the related adolescent whom frequently interacts with her dam and sire); (2)

despite the fact that their weights did not change substantially, there may be changes

taking place similar to what is observed in animals on calorie restricted diets that leads

to increased activity (Duffy et al., 1990; Duffy et al., 1991; Goodrick et al., 1983; Ingram et al., 1987) ; or (3) there was another environmental change that influenced behavior that was unknown to the researcher.

Although the aim of this diet manipulation was to bring some of the heavier

animals to a healthier weight, there may be some parallels between this diet change

and research done on calorie restriction in nonhuman animals. Calorie restriction (CR)

research can involve a wide range of restriction, but in general, it attempts to reduce

food intake so that calorie consumption is less than what animals would consume with

ad libitum access to food. Research with CR has resulted in increased average and

maximum lifespan in a number of species (Weindruch & Walford, 1988), and has also

been studied in relation to positive effects on health-related variables (reviewed in

rhesus monkeys by Lane et al., 1997). Some research with rodent models of CR has

shown increased activity in animals on a calorically restricted diet compared to controls

(Duffy et al., 1990; Duffy et al., 1991; Goodrick et al., 1983; Ingram et al., 1987).

Research with rhesus monkeys has also demonstrated that CR results in higher activity

levels than control animals (Weed et al., 1997). There could be metabolic changes that

take place that lead to increased activity under these dietary manipulations, or the

improved body condition observed under CR (e.g., Mattison et al., 2003) may also be

contributing to increased activity in the animals. Behavioral changes resulting from the reduced biscuit diet may be similar to those seen with CR, and suggest that metabolism and/or body condition could have been improved in ways that led to increased activity.

Changes in metabolism or body condition independent of weight loss in the animals here could explain why all of the animals demonstrated behavioral changes, although the drastic difference in weight loss in the adults compared to the adolescents makes it difficult to interpret whether their behavioral changes were indeed the result of physical improvements and not another factor.

A second but potentially less desirable explanation for the increased locomotion is that the animals could have been displaying anxiety-like or food searching behaviors following the diet manipulation. In addition to increased locomotion, Weed et al.

(1997) observed a greater number of stereotypical behaviors in rhesus monkeys on a CR diet compared to controls. In particular, the monkeys increased stereotypies related to

oral stimulation. Although not significant here, there was an increase in undesirable

behaviors that might indicate some feeding frustration. In particular, coprophagy and

glass licking behaviors increased. Before the diet change, coprophagy had not been

observed, although the animals tended to regurgitate and reingest their food more

often. The increase in coprophagy and glass licking could potentially be related to a

feeding frustration stimulated by the reduction in calories. A similar increase in

coprophagy was observed after a group of gorillas was put on a high fiber and low

starch diet (Less, 2012). Additionally, the increased time spent locomoting could be a

form of increased food-searching behavior.

Two other behaviors were significantly different between the diet manipulation

phases – social behavior significantly decreased and inactivity increased. The decreased

time spent in social behaviors might be related to the observation that food availability

is likely to influence the frequency or likelihood of orangutan associations in the wild

(Setia et al., 2010). It is possible that this pattern holds true in the zoo environment as

well and that a decrease in the amount of food provided to the animals could have led

to the decrease in sociality observed. However, another possibility leading to the

decreased sociality is that the maturation of the infant male in the group resulted in

fewer social interactions.

It is unclear why time spent inactive was also significantly increased after the

diet manipulation, but it is most likely related to a change in the percent of time spent

‘not visible’. Although it was not significant, there was a noticeable decrease in the

percent of time spent not visible. Oftentimes, when the orangutans in this group are not visible, they are hiding inside a crevice at the top of the large elevated rock, and it is likely that they are also inactive when they are not visible in that location. As such, the perceived change in inactivity between the conditions is probably related to differences in time spent not visible and not in any actual change of inactive behavior.

These results were obtained by observing a small group of animals and were not

collected as part of a rigorous study designed to evaluate the impacts of a specific diet

manipulation on the behavior of zoo-housed orangutans. As such, these results should

be considered pilot data to inform future studies that investigate more controlled

manipulations of diet with larger numbers of animals. However, despite the limitations,

a diet manipulation that resulted in weight loss in orangutans and data demonstrating

that there were associated behavioral changes is a novel finding. The results also show

that diet manipulations may be a promising area to focus future research efforts given

the health problems observed in orangutans that may be related to a propensity to

become overweight or obese (e.g. Weisenberg et al., 1991; Murphy, 2009; Schmidt et

al., 2006; Gresl, Baum & Kemnitz, 2000). Additionally, the behavioral changes observed

are likely to be well received by caretakers who are interested in increasing the activity and arboreality of zoo-housed orangutans. Thus, it is hoped that these results will increase discussion related to how we can best manage the diet, weight, and activity levels of zoo-housed orangutans. Future investigations should be made to better classify the body condition of zoo-housed orangutans, and to explore the impact of

specific dietary manipulations on body condition, behavior, and measures of cardio-

metabolic health.

Conclusion

The studies presented here provide evidence that simple dietary manipulations

such as providing increased access to browse and decreasing certain high energy foods

such as fruits and biscuits could have beneficial impacts on the behavior of zoo-housed

orangutans. Specifically, reducing the amount of fruit available while providing greater

access to browse could lead to reduced rates of regurgitation and reingestion behavior,

and reducing the number of calories fed could lead to increased activity levels and

elevated space use.

These simple dietary manipulations that appear to reduce R/R and increase

activity could have welfare implications for both psychological and physiological health.

Psychological well-being could potentially be enhanced by increasing time spent feeding. Increasing the time spent feeding could replace some of the time that animals previously spent inactive with a behavior that occupies a large amount of the activity budget of wild orangutans, and is likely to be preferred as a biologically relevant activity.

Additionally, the dietary manipulations explored here are likely to improve health measures that are associated with metabolic syndrome. Although it needs to be studied further, it would be expected that decreasing the sugar (i.e. fruit) and starch (i.e. biscuit) content of orangutan diets while increasing fibrous foods (i.e. browse) would improve physiological health. It is well known that consuming too many energy-dense

52 foods will lead to weight gain, and many studies in humans have shown that there are health benefits such as reduced serum cholesterol, LDL-cholesterol, fasting blood glucose, insulin, and inflammation from increased intake of fiber (Trumbo et al., 2002;

Kendall et al., 2010; Sievenpiper et al., 2009; Ludwig et al., 1999; Jenkins et al., 2003,

2005). Similarly, we have some evidence that increasing fiber and decreasing starch and sugar can successfully improve health measures such as total cholesterol in zoo-housed gorillas (Less, 2012). Given the leading causes of orangutan mortality (McManamon,

2009), studies reporting that orangutans are susceptible to glucose regulation problems

(Gresl et al., 2000), and that they have higher levels of LDL-cholesterol than their wild counterparts (Schmidt et al., 2002), the improvement of orangutan diets so that they are more similar to their wild counterparts is a promising avenue of inquiry that could improve orangutans’ cardio-metabolic health.

The increased levels of activity that were associated with a reduced-calorie diet are also likely to further improve physiological health, as it is known that sedentary behaviors are linked with obesity and subsequently, risk factors related to chronic disease (Chung et al,. 1998; Fung et al., 2000; Manson et al., 2004). There is also some evidence that increased activity is beneficial to the psychological health of humans. In humans, exercise has been explored as a way to prevent and treat depression, to reduce anxiety, and it may impact overall mood (Fox, 1999). Although the reasons for these benefits are not clear and may partially be a result of improved self-perception and associated psychosocial benefits in humans that may not exist in orangutans, there is also some evidence for biochemical and physiological changes from exercise (Fox, 1999)

that could potentially lead to improved psychological state in nonhuman animals as well. Therefore, increased activity could be a way to increase psychological welfare,

especially given the fact that zoo professionals often look to wild animal activity budgets

as a measure of welfare, and increased activity of zoo-housed orangutans would help to

make their activity budget look more like their wild counterparts.

However, it is also worth considering that the increased activity observed after

the reduction in biscuits, coupled with a decrease in social behaviors and the noted

changes in undesirable behavior (i.e. the observation of coprophagy and glass licking), could indicate that this diet manipulation had a negative effect on overall welfare. Such a drastic reduction in calories unaccompanied by other opportunities for activity may have led to animals that were anxiously awaiting their next meal. Future research should explore the psychological ramifications of drastic dietary changes on captive animals, even if the diet changes are being made to improve their overall health.

Finally, it should be mentioned that the dietary manipulations and subsequent behavioral changes seen here could be beneficial for the educational mission of the zoo.

Seeing orangutans that are regurgitating and reingesting their food may disturb zoo visitors, and this is likely to impact the connection that they feel to these animals. Also, when visitors witness orangutans displaying R/R behavior, this misrepresents the behavior of wild orangutans and therefore visitors are not being properly educated about orangutan behavior. Similarly, when visitors see orangutans sitting on the ground and predominantly inactive, the behavior of their wild counterparts is misrepresented.

Additionally, several authors have shown that zoo visitors are more interested in

animals that are active (Bitgood et al., 1988; Mitchell et al., 1992; Fernandez et al.,

2009). If orangutans were fed and housed properly in zoos, we would not only be likely

to see positive health and welfare impacts, but there would be a greater chance that

zoo-housed orangutans would behave more like their wild counterparts and thus better

educate and engage zoo visitors to conserve this endangered species in the wild.

Appendix

A. Letter to Orangutan Institutional Representatives

Dear [Orangutan IR],

Please consider contributing to a short, 2-question survey about the prevalence of regurgitation and reingestion (R/R) behavior in orangutans. In a response to this email, simply answer the following two questions.

1. Provide the name of each orangutan at your institution followed by the number that best describes the individual’s R/R behavior using the following scale:

1 = Frequent – multiple bouts per day 2 = Often – at least once per day 3 = Sometimes – several times a week or with certain foods 4 = Never 5 = Don’t Know

2. Are there are any food items that seem to trigger or exacerbate this behavior in your orangutans?

Feel free to forward this short survey to a keeper or other staff member that may be able to provide this information most accurately. Please submit your response no later than March 28, 2011.

We intend to include the results of this survey in a manuscript about R/R in orangutans that is currently in preparation.

Thank you very much for your help, and please contact me with any questions.

Sincerely,

Christine Cassella

B. Notice of Copyrighted Material

A substantial portion of the text and figures presented in Study 1: Prevalence of Regurgitation and Reingestion (R/R) in Orangutans Housed in North American Zoos and an Examination of Factors Influencing its Occurrence in One Group of Bornean Orangutans (pg 17-35) has been published in the journal Zoo Biology, published by Wiley-Blackwell.

The article’s citation is as follows:

Prevalence of Regurgitation and Reingestion in Orangutans Housed in North American Zoos and an Examination of Factors Influencing its Occurrence in a Single Group of Bornean Orangutans, Cassella, C. M., Mills, A., & Lukas, K.E., Zoo Biology, published online ahead of print, Copyright © 2012, Contributor-owned work

The article can be found online at the following address:

http://onlinelibrary.wiley.com/doi/10.1002/zoo.21000/full

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