Taste perception and food choices in capuchin monkeys and human children

Despite more than 40 million years of independent evolution, capuchin monkeys and human children share several features that make a comparison in the domain of feeding behaviour interesting. As with humans, capuchin monkeys have a long life span and
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  Taste perception and food choices in capuchin monkeys andhuman children Elsa Addessi 1,1, Amy T. Galloway 2, Leann Birch 3, and Elisabetta Visalberghi 1 1 Institute for Cognitive Sciences and Technologies, Rome, Italy 2 Appalachian State University, Boone, NC, USA 3 The Pennsylvania State University, PA, USA Summary Despite more than 40 million years of independent evolution, capuchin monkeys and human childrenshare several features that make a comparison in the domain of feeding behaviour interesting. Aswith humans, capuchin monkeys have a long life span and an extended infancy period; moreover,they are omnivorous and food neophobic. In both species, taste provides an immediate and powerfulfeedback when selecting foods. In humans, acceptance and rejection responses are evident beginningin early infancy, before experiencing any consequences from the ingestion of sweet or bittersubstances. Similarly, capuchins initially prefer novel foods with a high sugar content that is readilyperceived through taste. However, after repeated encounters with these foods, capuchins change theirpreferences, responding to the feedback coming from the foods' energy content, in order to maximizethe net gain of energy. Also in children, positive consequences of the ingestion of a food can beassociated with the flavour of that food and can increase its consumption. Preschool children learnto prefer food with a high caloric content over food with a low caloric content and use differentflavours as immediate cues to distinguish foods. Another factor influencing the consumption of anovel food is how often it is encountered. For capuchins, a food remains unfamiliar only for the firstfew encounters. Similarly, children’s neophobic response decreases with repeated exposures to novelfoods. Furthermore, in both species social influences may help to overcome food neophobia and toaccelerate the acceptance of novel foods into the diet. In conclusion, we argue that capuchin monkeysprovide a good model for investigating the factors affecting the acquisition of diet in human children. Key words children; capuchin monkeys; taste perception; neophobia; social influences Mots clés enfants humains; singes capucins; perception gustative; néophobie; influences sociales 1Corresponding author: Elsa Addessi, Unit of Cognitive Primatology, Institute for Cognitive Sciences and Technologies, CNR, ViaUlisse Aldrovandi, 16/b, 00197, Rome, Italy (e-mail: E-mail: français:Données comparatives sur la perception gustative et les choix alimentaires des singes capucins et des enfants humains NIH Public Access Author Manuscript Primatologie . Author manuscript; available in PMC 2009 July 27. Published in final edited form as: Primatologie . 2004 ; 6: 101128. N I  H -P A A  u t  h  or M an u s  c r i   p t  N I  H -P A A  u t  h  or M an u s  c r i   p t  N I  H -P A A  u t  h  or M an u s  c r i   p t    INTRODUCTION Non-human primates have repeatedly been shown to be useful models for human tasteperception, broadening understanding of how diet selection and food intake are controlled inhumans (Drewnowski, 1997). Whereas environmental factors — such as beliefs and attitudesconcerning weight and dieting — modify food preferences of human adults, in very youngchildren, and non-human primates, many of the considerations that influence adult foodacceptance patterns do not apply. In children, only taste and familiarity account for foodpreferences (Birch, 1979a, 1979b; Drewnowski, 1997). In this paper we will present data onthe feeding behavior of capuchin monkeys and children that show how despite more than 40million years of independent evolution, they share several features that make comparing theirfeeding behavior extremely interesting.Like humans, tufted capuchin monkeys ( Cebus apella ) are omnivorous. This species, whichis widely distributed in South America, has a very broad diet consisting mainly of plant food,especially fruits, and a variety of invertebrates (Kinzey, 1997). Capuchins have been describedas a successful genus (Fragaszy, Robinson and Visalberghi, 1990), whose ecology and diet areextremely adaptable (Kinzey, 1997). Moreover, capuchins have a long life span (the record is53 years, Visalberghi and Anderson, 1999), long infancy and juvenile periods (Fragaszy andBard, 1997), large brains relative to body size (Bauchot, 1982; Stephan, Baron and Fraham,1988; Marino, 1995), and are born with brains that are relatively undeveloped and neurallyimmature (Fragaszy and Bard, 1997; Ross, 1991).In this contribution, we aim (1) to provide a description of several factors that might affectfood choice and ingestive behavior in omnivorous species, (2) to review the most relevantstudies on this topic conducted with capuchin monkeys and human children and discussing thedata, whenever possible, using a comparative perspective. FOOD NEOPHOBIA: AN ADAPTIVE ANSWER TO THE OMNIVORE’SDILEMMA The success of an omnivorous species depends on its propensity to explore and sample novelfoods and to include them in the diet, as well as on its caution toward them, in order to detectand to avoid the risk of ingesting poisonous substances (Freeland and Janzen, 1974; Glander,1982; Milton, 1993). Paul Rozin labeled this conflict as the “omnivore’s dilemma” (Rozin,1977). A partial solution to the omnivore’s dilemma is food neophobia, i.e. the hesitancy toeat novel foods (Barnett, 1963). However, in the long run food neophobia is maladaptive,because omnivores increase chances of survival through variety in the diet. Therefore cautiontowards new, potentially toxic, substances should be balanced with this need for variety (Birch,1998; Scott, 2001). In fact, food neophobia is a behavioral response that prevents the ingestionof large quantities of a novel food, and thus minimizes the risk of being poisoned (Glander,1982; Freeland and Janzen, 1974). At the same time, the ingestion of a little amount of a novelfood is sufficient to induce post-ingestive consequences (see below), leading the animal toavoid or accept that food in its diet. Also animals capable of detoxifying and eliminatingsecondary compounds should treat novel foods with caution, in order to avoid serious damagesto their detoxification systems (Freeland and Janzen, 1974).Capuchin monkeys are neophobic both in captivity and in the wild. Visalberghi and Fragaszy(1995) presented 11 captive capuchin monkeys with 10 novel foods (never tasted by any of the subjects previously) and 2 familiar foods. Each subject was tested individually once withone food at a time. Acceptance of the 10 novel foods ranged from complete acceptance (all the11 subjects tasted the food at least once) to unanimous rejection, and novel foods wereconsumed to a lesser extent than familiar ones. Similarly, when 10 novel foods were presented Addessi et al.Page 2 Primatologie . Author manuscript; available in PMC 2009 July 27. N I  H -P A A  u t  h  or M an u s  c r i   p t  N I  H -P A A  u t  h  or M an u s  c r i   p t  N I  H -P A A  u t  h  or M an u s  c r i   p t    to a group of wild capuchin monkeys ranging from 25 to 30 individuals, results showed thatcapuchins approached and ate very little of the novel food; instead, familiar foods werecompletely consumed (Visalberghi, Janson and Agostini, 2003). However, capuchins livingin a 43.000 ha ecological reserve (Parque Nacional de Brasilia, Brazil), which partially rely onfoods left by the visitors, do not seem to show food neophobia. They have probably learnedthat humans leave behind foods that are safe to eat and are willing to exploit food sources leftby humans in the area (Siemers, 2000; Visalberghi, pers. obs.).Infant and youngster capuchins are less neophobic than adults. When Fragaszy, Visalberghiand Galloway (1997) investigated food neophobia in 11 infant capuchin monkeys (4.5–12months), they found that infants did not treat novel foods with caution. Instead, infants pickedup and ate novel foods more frequently than familiar ones. A similar trend has been shown forwild capuchins: youngsters were far more responsive than adults to the novel foods, andcontacted, manipulated, explored, and ate the novel foods significantly more than adults(Visalberghi, Janson and Agostini, 2003). Since infants and juveniles are less efficient foragersthan adults (Janson and van Schaik, 1993; Terborgh, 1983; van Schaik and van Noordwijk,1989, Boinski and Fragaszy, 1989), their lower neophobia, compared to adults, may help themto avoid the risk of starvation.Human children are cautious about novel foods, and their rejection of novel foods is a commoncause of parental concern and frustration (Birch, 1983). As mammals, during the first monthsof life human children consume only milk. However, about halfway through the first year of life, an exclusive milk diet is no longer adequate to maintain growth and health, and thetransition from milk to an omnivorous diet occurs (Birch, 1998). Experimental evidenceshowed that infants (4–7 months old) are less neophobic than older children (2–5 years old).Birch, Gunder, and Grimm-Thomas (1998) suggested that neophobia would not be a fullyfunctional response during infancy, when food is provided by parents, whereas it becomesmore important by early childhood, when children have begun to explore the environment andeat by themselves. Nevertheless, omnivorous species should overcome neophobia, becausetheir success depends primarily on their ability to exploit new food sources during theacquisition of a varied diet and/or to face seasonal changes in food availability.The lack of evidence of food neophobia in young capuchins (as also shown in young lemurs;see next chapter by L. Tarnaud) seems to contradict the heightened presence of thisphenomenon in young children. More research is needed to determine whether methodologicaldifferences and/or developmental variations account for the differences in the neophobicbehavior in children and young capuchins. In the latter species, neophobia has never beeninvestigated in relation to weaning. SWEET TASTES BETTER: THE ROLE OF TASTE PERCEPTION Primates are able to assess food quality through the sensory information that comes from thefoods they consume (Dominy, Lucas, Osorio and Yamashita, 2001). Senses, and taste inparticular, enable primates to decide whether swallowing or rejecting a potential food, andthere is increasing evidence that taste perception is an adaptive response to the animals’ needto assess food nutritional contents (Simmen and Hladik, 1998; Laska, Hernandez Salazar andRodriguez Luna, 2000; Hladik, Pasquet and Simmen, 2002; Visalberghi, Sabbatini, Stammatiand Addessi, 2003).Substances high in calories, such as sugars—a very important energy source—are perceivedas sweet by humans and are readily accepted by both humans and non-human primates (Glaser,1993). On the contrary, the tendency to avoid bitter taste is associated with the presence of plant secondary compounds, such as alkaloids and glycosides, whose taste can function as acue to inhibit their ingestion (Ueno, 2001). In fact, secondary compounds can exist in nature Addessi et al.Page 3 Primatologie . Author manuscript; available in PMC 2009 July 27. N I  H -P A A  u t  h  or M an u s  c r i   p t  N I  H -P A A  u t  h  or M an u s  c r i   p t  N I  H -P A A  u t  h  or M an u s  c r i   p t    in concentrations far exceeding those required to cause death or severe physiological damageto almost any mammal that might eat them (Freeland and Janzen, 1974).Human neonates and newborn non-human primates react to gustatory stimuli in stereotypicalways, showing differential orofacial motor reactions (gusto-facial reflex; Steiner and Glaser,1984). They accept sugar solutions by sucking with relaxed facial expressions, and reject bittersolutions with a typically arched form of the mouth (Rosenstein and Oster, 1998). In one study,when sucrose was presented to infants in the form of a sucrose-infused gelatin nipple, theinfants’ sucking response increased in frequency and intensity (Maone, Mattes, Bernbaum andBeauchamp, 1990). Sensitivity to bitterness is relatively unstudied in infants and youngchildren. However, there is some evidence that bitter taste perception heightens in the first yearof life (Kajiura, Cowart and Beauchamp, 1992). In this study, newborn infants (0–6 days old)did not readily distinguish various concentrations of urea, whereas older infants (14–180 days)tended to reject all concentrations of the substance. To our knowledge, the reaction of newborncapuchins to gustatory stimuli has not been investigated, but it is very likely that the gusto-facial reflex and sucking preferences for sucrose are present in this species as well. INVESTIGATING FOOD PREFERENCES IN CAPUCHIN MONKEYS Taste perception seems very relevant for food selection in tufted capuchin monkeys.Visalberghi, Sabbatini, Stammati and Addessi (2003) investigated the acquisition of preferences towards 7 novel foods presented to 26 individual capuchins. The experimentconsisted of three phases: Pre-treatment, Treatment, and Post-treatment. In the Pre-treatmentand Post-treatment, subjects were tested individually, while during Treatment one half (N =13) of the subjects was tested individually (Individual condition) and the other half (N = 13)was tested together with 3–5 other group members (Social condition).In the Pre-treatment, subjects were presented with all 21 possible binary combinations of the7 foods using a two-alternative choice test (for similar studies on spider monkeys,  Atelesgeoffroyi , squirrel monkeys, Saimiri sciureus , and pigtail macaques,  Macaca nemestrina , seeLaska et al., 2000; Laska, 2001). Once the subject made a choice by taking one of the twofoods, it could not take the other one. Treatment was aimed to familiarize the subjects with thefoods presented in the Pre-treatment. During Treatment subjects received a 10-minute sessionper day for five consecutive days. In each session, the 7 foods were scattered on the entire floorof the cage. In the Individual condition, subjects had 8 pieces of each food. In the Socialcondition, the same quantity of food (8 pieces of each food) was available for each of thesubjects (see below). In the Post-treatment, each subject was again presented individually withthe 21 binary choices between the foods. The experimental procedure was the same as duringthe Pre-treatment.Results of the Pre-treatment showed that, already after having eaten small portions of eachnovel food only a few times, capuchins markedly preferred certain foods over others. Theirpreferences were positively correlated with the glucose and fructose content of the foods. So,short-term feedback coming from taste seems to be important for establishing initial foodpreferences. This finding is in agreement with a previous observation showing that, amongnon-human primates, Cebus  spp. have the highest sensitivity to sugars (Glaser, 1986). Sincesweet taste is usually not associated with toxicity, it seems adaptive for an omnivorous species,such as Cebus apella , to rely on sugar content for choosing between novel foods and enlargingthe diet without too much risk.In the wild, palatability of plant foods may change over time in relation to the concentrationof toxic secondary metabolites. Jones (1978) showed that the levels of cyanogenic glucosidesin various plants differ depending on geographical locality. In addition, the concentration of toxic secondary metabolites (e.g. cyanogenic glucosides) changes in relation to plant age Addessi et al.Page 4 Primatologie . Author manuscript; available in PMC 2009 July 27. N I  H -P A A  u t  h  or M an u s  c r i   p t  N I  H -P A A  u t  h  or M an u s  c r i   p t  N I  H -P A A  u t  h  or M an u s  c r i   p t    (McKey, 1975; Janzen, 1983), season (Ellis, Keymer and Jones, 1977a, b), and plant tissuetype (Cooper and Johnson, 1984). In another study, Visalberghi and Addessi (2000)investigated capuchins’ behavioral response to a familiar food changing in palatability overtime. Capuchin monkeys were presented with a familiar food whose palatability changedaccording to the experimental phase. In Phase 1 capuchins were individually presented withthis familiar food. In Phase 2 they received the same familiar food with pepper added to it,making it unpalatable. In Phase 3 they received the same familiar palatable food of Phase 1.Five sessions were carried out in each phase. Capuchins readily adjusted to changes in flavorand palatability of a familiar food since the first session in which the change occurred. Theyreduced (Phase 2) and increased again (Phase 3) the amount of food eaten, and encounters withthe food when unpalatable did not affect its consumption when palatable once again. Therefore,capuchins undoubtedly showed behavioral flexibility when facing negative as well as positivechanges in the palatability of a familiar food. INVESTIGATING FOOD PREFERENCES IN HUMAN CHILDREN Research indicates that human infants’ early experiences with food flavor have decisiveinfluences on their acceptance of food. Infants are first exposed to the flavor of food beforethey are ever born. Flavors are transferred from the mother to the fetus through amniotic fluidthat is periodically ingested through the unborn child’s mouth and nose (Hauser, Chitayat,Berns, Braver, and Muhlbauer, 1985, Mennella, 1995). Moreover, newborns are exposed toflavors through breast milk if they are breastfed (Mennella and Beauchamp, 1991; Gerrish andMennella, 2000). Children who are breast-fed are exposed to a variety of flavors, and there isevidence that babies prefer flavors they have previously experienced through breast milk (Mennella and Beauchamp, 1993; Mennella and Beauchamp, 1996; Mennella and Beauchamp,1998). There is also evidence that breastfed children are more likely to accept pureed vegetableswhen first introduced to solids than formula-fed babies (Sullivan and Birch, 1994). In addition,the positive influence of breastfeeding on the reduction of picky eating is evident in childrenas old as 7 years of age (Galloway, Lee and Birch, 2003).Recent findings suggest that infants who are exposed to a particular flavor before birth (viafood flavors that pass through the placenta) or through breast milk, will prefer that flavor sixmonths after birth more readily than infants never exposed to the flavor (Gerrish and Mennella,2001). In this study, expectant mothers were assigned to one of three conditions: 1) they wereasked to drink approximately one glass of carrot juice for 12 weeks in the last trimester of pregnancy, 2) they were asked to drink approximately one glass of carrot juice everyday for12 weeks during after their babies were born, or 3) they were asked to drink approximatelyone glass of water 12 weeks before and after childbirth. Infants exposed to the carrot juiceeither prenatally or postnatally preferred cereal mixed with carrot juice over cereal mixed withwater when solids were first introduced.Birch (1979a) developed a procedure for directly assessing food preferences in young children.Children are individually presented with a tray of seven to nine foods, small samples of whichare contained in separate transparent cups. The child tastes each item in a self-selected order.After tasting the food, the child is asked to place it in front of one of three cartoon faces thatcorresponds to the child’s affective response to the food: a smile (like), a frown (dislike), or aneutral expression (just okay). Then, the child is asked to rank the foods within each grouping(liked, disliked, and just okay) in order to obtain a complete rank order. This procedure isrepeated for each of the three categories. Rank ordering within categories can be combined tocomprise a complete rank order on the foods. Even though preferences may vary with time of day and through the course of a meal, for most of the three-year-olds and nearly all olderchildren the preference data obtained in this way are reliable and predictive of the relativeconsumption (see also Birch and Sullivan, 1991). Addessi et al.Page 5 Primatologie . Author manuscript; available in PMC 2009 July 27. 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