A review of nutritional and motivational factors contributing to the performance of regurgitation and reingestion in captive lowland gorillas (Gorilla gorilla gorilla)

A review of nutritional and motivational factors contributing to the performance of regurgitation and reingestion in captive lowland gorillas (Gorilla gorilla gorilla)

Applied Animal Behaviour Science 63 Ž1999. 237–249 A review of nutritional and motivational factors contributing to the performance of regurgitation ...

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Applied Animal Behaviour Science 63 Ž1999. 237–249

A review of nutritional and motivational factors contributing to the performance of regurgitation and reingestion in captive lowland gorillas žGorilla gorilla gorilla / Kristen E. Lukas

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School of Psychology, Georgia Institute of Technology, Atlanta, GA, 30324, USA TECHlab, Zoo Atlanta, 800 Cherokee AÕenue, SE, Atlanta, GA, 30315, USA Accepted 18 November 1998

Abstract Regurgitation and reingestion ŽRrR. is a common phenomenon in captive lowland gorillas Ž Gorilla gorilla gorilla., but it has never been reported in wild populations. Although changes in diet have been shown to reduce the behavior, little is known about the underlying mechanisms that lead to its development and maintenance. In this paper, a comparative analysis of ruminatory behavior in humans and stereotypic behavior in captive, domesticated animals reveals several nutritional and motivational factors that may contribute to the sustained performance of this behavior in captive gorillas. Additional research is needed to evaluate temporal, seasonal, gustatory, social, individual, and medical influences on this behavior. q 1999 Elsevier Science B.V. All rights reserved. Keywords: Gorilla ingestion; Stereotypic behavior; Primates; Rumination

1. Introduction Regurgitation and reingestion ŽRrR. is a familiar, but poorly understood, phenomenon in captive lowland gorillas Ž Gorilla gorilla gorilla. ŽLoeffler, 1982; Akers and Schildkraut, 1985; Gould and Bres, 1986a,b; Wiard, 1992; Velderman, 1997.. Similar to rumination in humans, it consists of the voluntary retrograde movement of food andror )

Curator of Primates, Lincoln Park Zoo, 2150 N. Cannon Drive, Chicago, IL 60614, USA. Tel.: q1-312-742-7232; fax: q1-312-742-7220; e-mail: [email protected] 0168-1591r99r$ - see front matter q 1999 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 8 - 1 5 9 1 Ž 9 8 . 0 0 2 3 9 - 1

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fluid from the esophagus or stomach into the mouth, the hands, or a substrate, followed by subsequent consumption of the regurgitant ŽStrombeck, 1979; Shay and Johnson, 1984; Gould and Bres, 1986a.. Regurgitation is different from vomiting, a reflex behavior elicited by autonomic activity preceded by hypersalivation, contractions of abdominal muscles, and nausea ŽStrombeck, 1979; Shay and Johnson, 1984.. RrR in captive gorillas is remarkably similar in temporal patterning, topography, and environmental elicitation to rumination disorder in humans ŽGould and Bres, 1986b.. In many ways, RrR functionally resembles post-prandial, or post-meal, stereotypic behavior in confined domestic animals, such as the sow. In this paper, I will review some nutritional and motivational factors that may contribute to the sustained performance of RrR in captive gorillas by synthesizing information reported on human rumination and stereotypic behavior in other captive species. Although many people would agree that repetitive regurgitation and reingestion of food is unpleasant to observe, it is often difficult to characterize this behavior in relation to other gorilla behaviors. RrR may be considered an ‘abnormal’ ŽRuempler, 1992; Baker and Easley, 1996. or ‘not a natural’ ŽWiard, 1992. behavior simply because it has never been reported in wild populations of gorillas. As hind-gut fermenters, gorillas are simply not physiologically designed to ruminate food in the normal course of digestion, as are many herbivorous, ungulate animal species ŽElftman and Atkinson, 1950.. However, survey results reported by Loeffler Ž1982., Akers and Schildkraut Ž1985., and Gould and Bres Ž1986a., confirm that RrR is ‘statistically normal’ in captivity with roughly 65% of confined gorillas exhibiting this behavior. Zeller Ž1991. reported that zookeepers, veterinarians, and field researchers classified RrR in captive chimpanzees as ‘not abnormal’. RrR, therefore, may be an adaptive response to elements of boredom, diet, stress, space restriction, or lack of control in the captive environment. Unfortunately, it may be maladaptive if it results in health problems. Human bulimics often suffer esophageal damage and dental erosion as a result of repetitive vomiting ŽHaller, 1992., and humans that engage in rumination similarly suffer weight loss, impaired growth, malnutrition, dehydration, gastric disorders, tooth decay and erosion, electrolyte imbalance, anemia, and otherwise declining health ŽJohnston, 1993.. Although the effect of RrR on the health of gorillas has not been systematically evaluated, these findings in humans suggest this chronic behavior could be deleterious for gorillas. However, RrR has not emerged as a causal factor for health problems in gorillas at Zoo Atlanta, for example ŽR. McManamon, personal communication.. Another way to characterize RrR is as an ‘undesirable’ behavior ŽBloomsmith, 1989., not only for many of the above reasons, but because it often occupies a disproportionate amount of time for captive gorillas compared to the activity budgets reported for wild populations. It may take the place of natural consumptive behaviors that would occur if the captive environment provided adequate opportunities for feeding and foraging. For example, wild mountain gorillas spend approximately 45% of time feeding ŽHarcourt and Stewart, 1984., exhibiting a bimodal diurnal feeding pattern in which food is consumed in small quantities over several hour periods in the morning and afternoon ŽSchaller, 1963.. Conversely, captive gorillas spend approximately 20–25% of time feeding ŽBower, 1980; Gould and Bres, 1986a; Lukas, 1995; Hoff et al., 1996,

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1997., although lower values have been reported Ži.e., Akers and Schildkraut, 1985.. Unlike wild gorillas, captive gorillas are not usually surrounded by limitless quantities of plant material from which they can continuously forage; instead, they are bound by an individual zoo’s feeding protocol that often consists of several discrete meals distributed throughout the day. Given this disparity, it would be preferable to see rates of RrR decline in exchange for higher, more species-typical rates of feeding and foraging. There have been a number of hypothesized functions for RrR. For example, Loeffler Ž1982. surveyed the beliefs of captive managers of gorillas regarding possible causes of RrR. Managers cited boredom, stress, environment Žlack of objects or presence of smooth surfaces., ‘enjoyment from reingesting a favorite food’ Žp. 8., and extending feeding periods ŽLoeffler, 1982.. However, relatively few empirical studies have been conducted on RrR in gorillas and no single hypothesis has been either supported or disconfirmed. The limited research that has been conducted on gorilla RrR to date includes: 1. Collecting descriptive information through surveys ŽAkers and Schildkraut, 1985, N Žnumber of gorillas. s 206; Gould and Bres, 1986a, N s 117; Loeffler, 1982, N s 183.. 2. Describing motor patterns and behavioral sequences during RrR ŽGould and Bres, 1986a, N s 3.. 3. Determining effect of feeding browse on RrR ŽGould and Bres, 1986a, N s 2.. 4. Determining effect of exchanging vegetables for fruit on feeding duration and RrR ŽVelderman, 1997, N s 2.. 5. Timing interval between ingestion of specific food items and RrR ŽWiard, 1992, N s 2.. 6. Measuring amount of RrR following ingestion of specific food items ŽLoeffler, 1982, N s 4; Wiard, 1992.. 7. Evaluating effect of liquefying a meal on RrR ŽGould and Bres, 1986a, N s 4.; and effect of feeding only browse and vegetables on RrR ŽRuempler, 1992, N s 1.. Despite findings that provision of browse and removal of fruit from the diet reduces RrR ŽLoeffler, 1982; Gould and Bres, 1986a; Ruempler, 1992; Wiard, 1992; Velderman, 1997., no one has yet documented the elimination of this behavior from an individual’s repertoire. Ruempler Ž1992., however, reported that one gorilla’s RrR had completely ceased for over a year after removing all but huge portions of vegetables and browse Ž18 kg per adult animal per day. from the diet at Cologne Zoo in Germany. For comparison, an adult male gorilla consumes approximately 6 kgrday at Zoo Atlanta ŽG. Hamor, personal communication., 13 kgrday at Brookfield Zoo ŽC. Demitros, personal communication., and 30 kgrday in the wild Ž G.g. beringei, Goodall, 1977.. Unfortunately, systematic behavior observations were not conducted in the Ruempler Ž1992. study, severely limiting the interpretation of the reported results. Even if the Ruempler Ž1992. diet was an effective way to eliminate RrR, it is an impractical diet for most zoos, which are limited in the human, financial, and spatial resources required to locate, grow, harvest, and store such large quantities of browse throughout the year. These limited research findings suggest that increasing browse content and removing fruit from captive gorilla diets reduce RrR, but they do not denote a cause. Without identifying a causative factor, it can be difficult to manipulate husbandry procedures to

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effectively reduce or eliminate RrR. For example, is the reduction in RrR observed following browse ingestion due to the altered nutritional content of the meal or is it merely an occupational effect, occurring simply because the two behaviors ŽRrR and feeding on browse. are physically incompatible? Would other foods containing the same nutrient content as browse have the same effect? If the results are due to nutrition, which variables are responsible for the effect: increased fiber content or increased dry matter content? Finally, is the reduction of RrR due to negative feedback resulting from increased stomach distention following ingestion of bulky, fibrous foods? In other words, do the gorillas just not ‘feel full’ without consuming large quantities of bulky foods and therefore prolong the feeding period by engaging in RrR? Alternatively, would providing the animal with alternative, non-feeding means of occupation, immediately following a meal, result in similar reductions in RrR? A reduction of RrR during post-meal training sessions ŽMorgan et al., 1993. suggests that the effect may be occupational. In addition, once the behavior is established, humans have reported that it is pleasurable ŽMayes et al., 1988., which may account for the limited success in eliminating it in gorillas. Further research is therefore needed to identify causal factors leading to the development and maintenance of RrR in captive gorillas. Because RrR is an oral, food-related behavior, nutrition will likely surface as a predominant causal factor. However, there does not yet appear to be a direct causal link between any one precipitating element and the performance of this behavior. Factors such as boredom, distress, environment, individual learning, social learning, palatability of regurgitant, reinforcing and habitual properties, early trauma, maternal neglect, rearing history, and development will all need to be considered before this behavior will be reduced or eliminated in the captive gorilla population. Additional insight into the underlying causes and function of RrR in gorillas may be gained by considering parallel behaviors in humans and stereotypic behaviors in other captive animals. 2. Rumination in humans Rumination disorder is described in the American Psychiatric Association’s Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition ŽDSM-IV., not as an ‘Eating Disorder’ such as anorexia or bulimia, but as a ‘Feeding and Eating Disorder of Infancy or Early Childhood’ Ž1994.. In human infants, it is often preceded by psychosocial problems such as stress, lack of stimulation, neglect, and object loss, including the loss of a parent or of a parent’s attention ŽBlinder et al., 1988; Mayes et al., 1988; American Psychiatric Association, 1994.. Infant rumination is often thought to extend the feeding process, provide comfort, or increase stimulation ŽChatoor et al., 1984; Franco et al., 1993.. Both human rumination and gorilla RrR are characterized as repetitive or cyclical and are usually preceded by stereotypic, eliciting behaviors such as stomach twisting, rocking back and forth, lip movements, bending forward, and head shaking ŽGould and Bres, 1986a; Johnston, 1993.. Johnston Ž1993. refers to rumination as a ‘skill’, with individuals acquiring their own unique style for facilitating rumination over time. In

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fact, he differentiates between infants, who often require manual stimulation to provoke rumination, and more developed individuals, who use less obvious motor movements to elicit the behavior, by stating, ‘‘ . . . manual stimulation may represent an early point in skill development, whereas the absence of any overt facilitating movements may constitute the zenith of ruminative prowess,’’ ŽJohnston, 1993, p. 94.. Although it is most commonly observed in normal human infants, rumination also occurs in normal and mentally retarded human adults ŽAmerican Psychiatric Association, 1994.. Mayes et al. Ž1988., distinguished between two types of rumination disorder: psychogenic rumination of infancy and self-stimulating rumination of the mentally retarded. Both types of rumination are characterized as ‘‘self-induced, purposeful, and pleasurable’’ ŽMayes et al., 1988, p. 300., occurring in three to four times more males than females ŽJohnston, 1993.. However, psychogenic rumination of infancy occurs in developmentally normal infants at a mean age of five months, and is usually preceded by disturbed familial relationships ŽMayes et al., 1988.. This type of rumination is often associated with object loss, including loss of a parent or a parent’s attention ŽBlinder et al., 1988.. Alternatively, rumination in the mentally retarded population may begin at any age from infancy through adulthood, and is thought to serve a self-stimulating function ŽMayes et al., 1988.. Given this dichotomy, gorilla RrR resembles the latter type of rumination in that it occurs in gorillas of all ages and appears to be self-stimulatory ŽGould and Bres, 1986b.. Gould and Bres Ž1986a. reported that only 19% of gorillas under the age of 5 years engaged in RrR while 84% of gorillas over the age of 5 exhibited the behavior. Age of RrR onset was estimated for 53 of the 183 gorillas in the Loeffler Ž1982. survey. Only 3.7% were reported to first exhibit the behavior before 1 year of age, 32.1% between 1 and 2 years of age, 54.8% of gorillas between 2 and 8 years of age, and 9.4% after 8 years of age. No sex differences in the incidence of RrR have been reported for gorillas ŽLoeffler, 1982; Akers and Schildkraut, 1985; Gould and Bres, 1986a.. According to Johnston Ž1993., rates of rumination in humans are highest in the immediate post-prandial period and subsequently decrease with time. The relationship between ruminative behavior in humans and the nutritional and mechanical properties of food has been studied extensively by Johnston et al. ŽRast et al., 1981, 1984, 1985a,b, 1988; Johnston et al., 1991, 1990; Greene et al., 1991; Johnston and Greene, 1992.. Their findings suggest that although slight increases in food quantity correspond to slight increases in rumination ŽRast et al., 1985a,b; Johnston et al., 1991., there is an overall inverse relationship between food quantity and rumination ŽRast et al., 1981, 1984; Johnston and Greene, 1992.. One way to treat rumination is by altering the nutritional content of meals and administering a satiation diet in which a person consumes as much food as possible in a given meal ŽStarin and Fuqua, 1987; Clauser and Scibak, 1990; Johnston, 1993.. Because weight loss often accompanies rumination in humans ŽJohnston, 1993., satiation diets are beneficial in two ways: rumination is stopped and weight is gained. Of course, in order to prevent excessive weight gain, a low-calorie satiation diet can be substituted ŽJohnston et al., 1991; Johnston, 1993.. In addition, there is a moderate, inverse relationship between rumination and caloric content of the diet ŽJohnston et al., 1991; Greene et al., 1991.. For example, declining rates of rumination following consumption of peanut butter were not associated with the

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consistency of the peanut butter, but with its caloric content ŽGreene et al., 1991.. Although the consistency of a meal becomes progressively pureed following repetitive cycles of rumination or RrR, Johnston et al. Ž1990. demonstrated that feeding pureed meals led to a 25% increase in rumination. Along with these nutritional variables, mechanical properties of feeding additionally contribute to rumination. For example, increasing stomach distention, oropharyngeal stimulation Žchewing., and esophageal stimulation Žswallowing. during a meal led to moderate decreases in rumination in humans ŽRast et al., 1985a,b, 1988.. Nutritional variables, therefore, contribute to the maintenance of ruminatory behavior in humans. Unfortunately, little is known about why certain dietary variables have an inhibitory effect on rumination ŽJohnston, 1993.. Identifying and interpreting the mechanisms behind post-prandial rumination in humans may be the first step in eventually eliminating RrR in captive lowland gorillas. Further research is needed to identify the psychological and nutritional factors associated with post-meal, stereotypic behavior. An improved understanding of the role of feeding motivation in the development and maintenance of post-prandial behavior may be achieved through examination of the literature on stereotypic behavior in other captive animals. 3. Stereotypic behavior Recent research in behavioral stereotypy underscores the heterogeneous nature of abnormal behavior development, providing an excellent reference for future studies on gorilla RrR. Whether or not RrR is technically a ‘stereotypic’ behavior has yet to be determined; it is not typically mentioned as an example of such in the literature. However, the rigid, invariant, repetitive nature of the behavior, as well as its unknown function, seem to qualify its inclusion in this area. Stereotypic behavior is generally defined as behavior that is fixed in form, repetitive in nature, and without an obvious goal or purpose ŽOdberg, 1987.. Occurring under restricted conditions, stereotypies may indicate that an environment is deficient in one or more aspects for an individual or species ŽMason, 1991a; Marriner and Drickamer, 1994; Carlstead, 1996; Carlstead, 1998.. Many stereotyped behaviors, such as repetitive leg-kicking or arm-waving, are observed in normal human infants with characteristic stereotypies preceding specific motor stages of development ŽThelen, 1981.. Mason Ž1991a. maintains that stereotypies resemble normal behavior in that inflexibility of normal behavior may develop following mere repetition of behavior patterns in an unvarying environment. Once developed, both stereotypic and normal behavior may be emancipated from the original, eliciting cause, and eventually occur under a wide range of conditions ŽMason, 1993.. Stereotypic behavior is observed in a wide range of populations, including zoo animals, laboratory animals, farm animals, normal humans, and mentally impaired humans. Unfortunately, stereotypy research has been fractionalized, with scientists typically targeting only one or two of these populations when consulting the literature or conducting scientific studies. Only recently are efforts being made to improve communication between these disparate fields of study ŽOdberg, 1993; Sprague and Newell, 1996.. Regardless of the study subject, the origin and maintenance of stereotyped

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behaviors can be investigated from a number of perspectives including physiological, neurochemical, behavioral, developmental, environmental, social, and ecological ŽRojahn and Sisson, 1990.. For example, neurochemical theories have implicated both dopamine and endorphin as controlling factors in maintaining stereotypic behavior. Behavioral models, on the other hand, might evaluate the role of individual or social learning, schedules of reinforcement, stimulus control, and automatic reinforcement in behavior development. Environmental factors under investigation include enclosure size, complexity, novelty, and deprivation. Generally, the management of stereotypic behavior in a particular setting subsequently corresponds to the theoretical perspective used in the analysis of the behavior. While stereotypies, by definition, have no obvious goal or purpose, their sheer persistence implies that they may serve some function for the individual. They are often thought to serve either an arousal function, compensating for sensory deprivation or boredom, or a de-arousal or compensatory function, occurring in response to distressful or excessively stimulating situations ŽDantzer, 1986; Shulman et al., 1996.. The latter function forms the basis of the ‘coping’ hypothesis of stereotypy, which suggests that stereotypic behavior reduces physiological responses to stress ŽRushen, 1993.. This hypothesis has not consistently been supported by physiological data ŽRushen, 1993., which reinforces the idea that stereotypies, as a class, are not homogenous in cause or function ŽMason, 1991a.. Further research is needed to delineate the function of stereotypies in the reduction of general arousal. Specific motivational factors have also been linked to the performance of stereotyped behaviors in intensely confined animals. In particular, feeding motivation has been implicated in the development of a number of feeding-related behavioral responses exhibited by domestic, laboratory, and zoo animals. For example, stereotypic pacing in carnivores ŽCarlstead and Seidensticker, 1991., adjunctive drinking in sows ŽRushen, 1984., oral stereotypies in sows ŽTerlouw et al., 1991; Lawrence and Terlouw, 1993; Bergeron and Gonyou, 1997; Mason and Mendl, 1997., and oral stereotypies in cattle Žde Passille et al., 1993; Redbo and Nordblad, 1997., have all been attributed to frustrated feeding motivation. Ingestion of food has been linked to the subsequent performance of established stereotypic behavior during the post-meal period in sows ŽTerlouw et al., 1993.. The topography of many pre- and post-prandial stereotypies resemble appetitive Žfood-seeking. or consummatory Žfood-ingesting. behaviors; because animals’ nutritional needs are presumably met by captive diets, the performance of mealtime stereotypic behavior is thought to reflect an ethological need to perform species-typical levels of appetitive or consummatory behaviors Žcf. Hughes and Duncan, 1988.. Normal appetitive feeding behavior has been shown to affect digestive hormone secretion and satiety, regardless of nutritional consumption, and may therefore play an important role in the feeding process for captive animals on restricted diets Žde Passille et al., 1993; de Passille and Rushen, 1997.. Lawrence and Terlouw Ž1993. argue that post-meal stereotypies develop in food-restricted animals as a result of increased feeding motivation in the post-meal period, which results from an interaction between internal hunger states, external feed-related cues, and sensory feedback from the act of feeding. For example, sows and broiler breeders often exhibit oral stereotypies, especially in the post-feeding period ŽLawrence

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and Terlouw, 1993.. According to Lawrence and Terlouw Ž1993., such post-meal stereotypies occur because a diminutive meal does not provide sufficient negative feedback to reduce feeding motivation, which is elevated at feeding time by both internal hunger cues and environmental ‘feeding time’ cues. In addition, the act of eating is a positive feedback mechanism, increasing feeding motivation ŽWiepkema, 1971.. What results, then, is an overall increase in feeding motivation in the post-meal period that may lead to the persistence of feeding behavior following a meal. Because these animals are housed in physically restrictive environments, behavioral opportunities during this period are limited. Through social learning, individual learning, or environmental ‘channeling’ ŽLawrence and Terlouw, 1993., a specific stereotypic behavior may develop and persist in certain individuals. Through neural sensitization ŽDantzer, 1986., behavior is maintained and subsequently elicited by general arousal. 4. Feeding motivation and R r R If gorilla RrR occurs primarily during the post-meal period, a frustrated feeding motivation theory may have explanatory power for this behavior. A preliminary model of the relationship between feeding motivation and RrR, based on the model of Lawrence and Terlouw Ž1993. Žp. 2822., is presented in Fig. 1. A combination of

Fig. 1. A preliminary model of the relationship between feeding motivation and RrR. Note: From ‘A review of behavioral factors involved in the development and continued performance of stereotypic behavior in pigs,’ by A.B. Lawrence and E.M.C. Terlouw, 1993, Journal of Animal Science, 71, p. 2822. Copyright 1993 American Society of Animal Science. Adapted with permission.

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environmental and internal cues surrounding the pre-meal period likely lead to an increase in feeding motivation for captive gorillas. Environmental cues may include movement to a new area specific to feeding, approach of the caretaker, visual or olfactory access to food, visual or auditory access to others feeding, time of day, etc. Internal hunger cues may include a drop in blood glucose levels, diurnal fluctuations of hunger, etc. Over time, conditioning may influence the development of both environmental and internal hunger cues. This increase in feeding motivation leads to the performance of appetitive behavior, and the act of eating additionally influences feeding motivation ŽWiepkema, 1971.. In the wild, gorillas’ feeding behavior presumably leads to satiation, which provides negative feedback to the cycle of hunger. However, the low fiber content and diminutive size of captive gorilla diets may prevent satiety and subsequently, prevent the suppression of feeding motivation. The persistent elevation in feeding motivation in the post-prandial period may then lead to the continued performance of appetitive and consummatory behaviors ŽHughes and Duncan, 1988; Lawrence and Terlouw, 1993.. Because there are limited behavioral opportunities during the post-meal period, and little or no favorable food is available, environmental channeling may occur in which the expression of highly motivated behavior is restricted by environmental constraints ŽLawrence and Terlouw, 1993.. Through individual or social learning, the regurgitation of food may replace normal appetitive behavior while the subsequent reingestion of regurgitant may replace normal consummatory behavior. Eventually, the repetitive performance of appetitive behavior ŽRushen, 1984; Terlouw et al., 1991; de Passille et al., 1993. or consummatory behavior ŽHughes and Duncan, 1988. may lead to satiety, providing negative feedback to the motivational system and leading to the cessation of feeding behavior. As with other stereotypic behaviors, once RrR is established in an individual’s behavioral repertoire it may be subsequently elicited during conditions of general arousal Ždistress, boredom, etc.. ŽDantzer, 1986; Lawrence and Terlouw, 1993.. In addition, once learned, the behavior may be used to prolong feeding on preferred food items ŽLoeffler, 1982; Gould and Bres, 1986b.. The frustrated feeding motivation hypothesis has merit only if RrR occurs in the post-prandial period. Earlier research has suggested that RrR in gorillas does indeed occur primarily in the post-feeding period, with a late afternoon peak that is independent of meal content ŽLoeffler, 1982; Akers and Schildkraut, 1985; Gould and Bres, 1986a.. In a case study of RrR in a 10-year old male chimpanzee, Morgan et al. Ž1993. reported a similar trend, where RrR occurred just after each meal, with the highest incidence following the PM fruit meal. In contrast, Baker and Easley Ž1996. reported between-meal peaks of RrR in a captive group of 13 chimpanzees, possibly suggesting an alternative controlling mechanism in that population. One possible explanation may be that the smaller body size of chimpanzees, as compared to gorillas, accommodates higher levels of satiation immediately following a small meal. Subsequent elevations in feeding motivation may not occur until several hours after the main meal, resulting in RrR at that time. The much larger gorilla, however, may experience little satiety following a small meal and therefore higher post-meal elevations in feeding motivation, resulting in high levels of RrR during the post-meal period. Of course, variations in feeding protocol may have more influence on post-meal satiety than species differences.

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The similarities between post-prandial ruminatory behavior and post-prandial stereotypic behavior suggest that frustrated feeding motivation may explain both rumination in humans and RrR in captive gorillas. Further support for this hypothesis is provided by the elimination of human rumination following administration of a satiation diet. 5. Future research Lawrence and Terlouw Ž1993. emphasized the importance of determining the underlying mechanisms of stereotypic behavior before attempting to change or eliminate it. Because social, individual, environmental, and physiological variables interact in the control of appetite and feeding behavior, a multifactorial approach to understanding rumination and RrR is required. Future research should include investigating health problems resulting from RrR, determining the palatability of regurgitated food, identifying social factors that contribute to the development and continued performance of RrR, designing nutritional management techniques that greatly reduce or eliminate RrR, and studying individual differences in predisposition for development of the behavior. For example, if the development of gorilla RrR can be linked to frustrated feeding motivation in captive settings, a question remains: why doesn’t every captive gorilla exhibit the behavior? Scientists are progressively acknowledging the importance of species and individual differences in understanding the development and maintenance of stereotypies. Individual factors such as rearing history, age, and experience, as well as individual differences in reactivity, overall behavioral rigidity, and motivation may affect whether or not an individual develops stereotypic behavior in a particular environment ŽMason, 1991b, 1993.. In addition, whether or not an individual is exposed to others who engage in stereotypic behavior may influence the likelihood of stereotypy development. Research on tethered sows ŽAppleby et al., 1989., caged birds ŽPalya and Zacny, 1980., and autistic human children ŽWolery et al., 1985. suggests social facilitation of stereotypy development or performance. An improved understanding of abnormal behavior will require integration of numerous perspectives on behavior development. If frustrated feeding motivation is responsible for the performance of regurgitation, then eating until satiety is achieved may be an ideal treatment option. In order to prevent the captive population of gorillas from becoming obese, an appropriate satiation diet would necessarily consist of many low-fat, high-fiber food items, subsequently resulting in a menu that would more accurately resemble the natural diet of western lowland gorillas ŽRogers et al., 1990; Popovich et al., 1997.. Because high-fiber diets have been shown to reduce hunger sensations in humans Žcf. Blundell and Burley, 1994., the same effect may occur in gorillas. The behavioral implications of a high-fiber diet for gorillas could therefore include negative feedback for feeding motivation in the postprandial period, and potentially result in reductions in or elimination of oral stereotypies such as RrR or coprophagy, increases in feeding duration, and improvements in digestion. Clearly, additional research is needed to further understand and treat this behavior. By retaining a comparative perspective, and synthesizing findings from both human and animal research, significant improvements may be achieved in captive gorilla husbandry to prevent or reduce stereotypic RrR behavior.

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Acknowledgements The author gratefully acknowledges Zoo Atlanta for providing financial support during the research and writing of this manuscript. In addition, several people provided invaluable ideas and comments by engaging in discussions that contributed to the development of this paper or by proofreading this manuscript, including: Fredda Blanchard-Fields, Mollie Bloomsmith, Maria Crane, Debra Forthman, Benjamin Freed, Gloria Hamor, Charles Horton, Michael Hoff, James Johnston, Meredith Jones, Terry Maple, Jack Marr, Rita McManamon, Tara Stoinski, and Corey Taylor. The author also thanks three anonymous reviewers for providing thoughtful comments and suggestions.

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