Prologue
Capuchins in human worlds
CAPUCHINS IN HISTORY
Five hundred years ago two events occurred that, although unrelated at the time, have become linked in science, especially in primatology. First, the Europeans (re-)discovered the Americas and were astonished by the novel natural landscapes. Second, a group of friars belonging to the Franciscan Order wanted to return to a literal observance of the rule of St. Francis of Assisi and so split from the founding monastic order to become the autonomous branch named, to this day, the Order of Friars Minor Capuchin. These friars wore distinctive robes of rich brown, with generous cowls, or hoods, covering their heads. When European explorers encountered small monkeys whose crowns of brown hair resembled the cowls of capuchin monks, they named them capuchins! In the Histoire Naturelles des Mammifères (1824), the French Enlightenment scientists Geoffroy Saint-Hilaire and Cuvier described a specimen (possibly a Cebus xanthosternos) noticing that [translated from French] “his muzzle of a tanned color, . . . with the lighter color around his eyes that melts into the white at the front, his cheeks . . . , give him a look which involuntarily reminds us of the appearance that historically in our country represents ignorance, laziness, and sensuality” (i.e., the monks) (Le saï a grosse tête mâle, p. 1, 1824, Vol. 1). The conflicts between scientists and clerics at the time are clearly evident in this statement. Even today, there may be some initial confusion if one says “I study the capuchins in the forest”; people wonder why the friars are residing in the forest.
The chronicles of the Europeans traveling in the Americas in the fifteenth and sixteenth centuries often contain references to capuchin monkeys (Urbani 1999a). A few travelers (e.g., Galeotto Cey, citation in Urbani) reported that monkeys were actively traded to Europe and that some of them (possibly capuchins) threw stones and branches at humans. Several monkeys, most of them dead, reached scientists who started to describe them meticulously without knowing, in most cases, from where these animals originated. Others were relegated to the ménageries of noble, aristocratic people and became a status symbol (see Figure 0.1). For example, in Versailles the Marquise de Pompadour kept and successfully bred capuchins (Buffon 1770, Vol. 12).
Figure 0.1. Catharine of Aragon by Lucas Hombolte (1494–1544). After the rediscovery of the Americas by Europeans, young capuchins (as well as other New World primates, such as marmosets) were taken to Europe as pets for the noble class. In fact, several portraits show them as the status symbols of their fortunate owners, instead of more common pets, such as dogs.
When the first capuchin monkeys survived the trip to Europe and zoologists had the opportunity to observe them alive, they found them particularly attractive. Not only did these monkeys have four dexterous hands (!), an interesting semi-prehensile tail, unusually shaped genitals, a petulant and curious personality and bird-like vocalizations; they were also very friendly to humans. Geoffroy Saint-Hilaire and Cuvier (1824) write of a capuchin that (translated from French) “he was extremely sweet and so intelligent: his eyes were remarkably penetrating; he seemed to read in my eyes what was going on inside me . . .” (Vol. 1, Le saï a gorge blanche mâle, p. 2).
Capuchins are visitors’ favorites in zoos and monkey parks (Vermeer 2000). What makes them so attractive? People who visit our laboratories (including those already familiar with other monkey species, such as macaques) are impressed by the deep involvement they feel in the presence of capuchins, and by how closely and intensely capuchins look at them. There are a number of good reasons for this. First, capuchins are generally friendly and tolerant of each other and toward humans. Second, unlike macaques, they do not perceive a stare (our wondering gaze) as a threat, because in affiliative contexts they often watch each other with a similar intensity. Third, during courtship they use some of the same behaviors we do (e.g., gaze into each other’s eyes, tilt their heads, raise their forehead, and blink their eyes). So, what is friendly and touching for us is moving for them as well. In addition, because humans are easily prompted to imitate monkeys (but not vice versa), visitors might try to copy the friendly behaviors of the capuchins and leave our laboratories with the feeling that a friendly exchange has occurred.
Thomas Belt was an English mining engineer and naturalist, whose book The Naturalist in Nicaragua (1874/1985) was considered by Charles Darwin as “the best of all natural history journals which have [sic] ever been published” (Darwin F. 1888, p. 188, letter of Charles Darwin to Sir J. D. Hooker). Belt was fascinated by the white-faced capuchin (Cebus capucinus, see Table 1.1 and color plate 2). He described its feeding habits in the forest while it “is incessantly on the look out for insects, examining the crevices in trees and withered leaves, seizing the largest beetles and munching them up with great relish” (p. 118), as well as its intelligent and mischievous behavior. This pet capuchin was an expert tool user who fished for ducklings using pieces of bread, retrieved things that were out of reach by means of sticks, and “could loosen any knot in a few minutes” (p. 118).
CAPUCHINS AS THEY ARE PERCEIVED IN THEIR NATIVE COUNTRIES
Ancient Egyptians considered the hamadryas baboon (Papio hamadryas) to be a god responsible for the art of writing, and often depicted them as dictating to a kneeling human scribe (Kummer 1995). Similarly, in their funerary ceramics ancient Mayans portrayed scribes that appear to have a mixture of characteristics belonging to humans and monkeys. In fact, the Mayans associated monkeys with writing, painting, music, and dance (Coe 1978). Given their current distribution, howlers (Alouatta palliata and A. pigra) and spider monkeys (Ateles geoffroyi) are thought to have been the monkeys represented in Mayan iconography. However, on the basis of morphological and behavioral comparisons among capuchin, howler, and spider monkeys, and on historic accounts, faunal analysis and linguistic evidence, Baker (1992) has argued that Mayans were inspired by capuchins in their depictions of monkey scribes.
The subsistence economy of traditional indigenous societies includes hunting. Especially for those people living so far from rivers that fishing is not an option, monkeys are an important source of protein (Hill and Padwe 2000, Sponsel 1997; see Figure 0.2). However, some indigenous groups, such as the Xavante community in Central Brazil studied by Leeuwenberg and Robinson (2000), do not hunt for primates. According to Vickers’ (1984) study of eight indigenous and four mestizo communities in Amazonia, mammals account for most of the meat that is hunted (64–74% of the individuals hunted and 91–92% of the meat weight) and monkeys rank second (by individuals) and third (by weight). Larger monkeys (spider monkeys, woolly monkeys, howlers, and capuchins) are preferred to other primates (Peres 2000a). On the basis of 867 hunts by 13 Waorani hunters, Yost and Kelley (1983) report that among the nine species of monkeys hunted, C. albifrons was third in terms of number of individuals hunted and by weight. Similarly in Suriname, where most rural people eat monkeys, interviews as well as data on freshly killed animals show that C. apella and C. olivaceus are among the most popular (Mittermeier 1991). The capture of infants for pets is usually a by-product of hunting for meat, and 45% (38 out of 84) of the monkey pets are tufted capuchins (Mittermeier 1991).
Figure 0.2. Left, capuchins are killed for meat. An Amerindian hunter (of the indigenous group of the Tirio, at the border between Suriname and Brazil) holds a recently killed Cebus apella. (Photograph courtesy of Mark Plotkin.) Right, Guajá in the Carú Reserve in western Maranhão (Brazil) have pet monkeys. The capuchin in this picture belongs to the very rare subspecies C. olivaceus kaapori. (Photograph courtesy of Loretta Cormier.)
A very interesting “ethnoprimatological” project was carried out by Cormier (2002, 2003) on the Guajá Amerindians in the Carú Reserve in western Maranhão (Brazil) to study the relations between humans and nonhuman primates. This reserve hosts eight species of primates: the Guajá (Homo sapiens), the red-handed howler monkey (Alouatta belzebul), the black-bearded saki (Chiropotes satanas), the brown capuchin (C. apella), the recently identified Ka’apor capuchin (C. kaapori [or C. olivaceus kaapori], see Table 1.2), the owl monkey (Aotus infulatus), the squirrel monkey (Saimiri sciureus) and the golden-handed tamarin (Saguinus midas). These monkeys serve as both food and pets for the Guajá Amerindians.
Guajá show a heavy seasonal reliance on monkeys; in the wet season, they account for 30% of the animals eaten. Orphaned monkeys whose mothers were hunted are brought back to the village and treated as human children by the women. The infant monkey is in constant physical contact with a Guajá woman, is breast-fed, played with, bathed, sung to, and even given previously masticated food to eat from the woman’s mouth. The monkey is also given a personal name and a kinship term of address. In contrast, the Guajá are known to severely mistreat dogs, even puppies. Therefore a pet monkey acquires a nearly human status, and because in the Guajá culture a woman is sexually attractive especially when pregnant and/or lactating, it follows that the presence of a monkey (regardless of the species, and usually clinging to the woman’s headdress) increases her “sex appeal” and her image of fertility. The presence in Cormier’s study area of 90 monkey pets and 110 humans shows the importance of having one or more monkeys per woman. Cormier argues that the apparent incongruity of having monkeys as surrogate children and as preferred food should be considered in the light of the role of the symbolic endocannibalism (eating of kin) in the Guajá religion in which “Eating is not an act that merely satisfies hunger; it also has the transformational power to make another sacred” (Cormier 2002, p. 79). In the Guajá culture, monkeys, and especially howlers, are considered very close to humans and eating what is similar to you is a way of making it sacred. Therefore, eating is no less respectful to the monkeys than keeping them as pets (Figure 0.2).
Unfortunately, as they grow older, monkeys gradually become independent, sometimes aggressive, and certainly less suited to be “pet-babies”. Juvenile monkeys (especially capuchins, given their destructive propensities, see Chapters 2 and 7) become a nuisance; consequently they are tied up and become more and more isolated from humans. This dramatic change in the way monkeys live has deleterious psychological consequences and they develop stereotyped and abnormal behaviors and many die. Hunting a monkey, having it as a pet, a child, a brother, or eating it, so that the monkey becomes sacred and lives a “paradisiacal existence” in the “sky-home”, are all fundamental aspects of the life and culture of the Guajá Indians. For Westerners, the only way to understand the puzzling lifestyle of the Guajá is to take a multidisciplinary approach, as Cormier has done, and not to lose sight of any of its aspects.
At the present time, some capuchin groups live in parks of several South American cities and towns, and research has begun on their behavior in such urban environments (Amaral and De Yong 1999, Balestra and Bastos 1999). Monkeys are not hunted in urban parks and people generally have positive attitudes toward them. However, people do not know how to behave properly towards monkeys, interpret their behavior, or assess their needs. Instead they usually think of capuchins as animals that can be hand-fed any food to see what they will do with different items. For example, in Brasilia people go to swim or picnic in the Parque Nacional de Brasilia, a 430km2 ecological reserve established in 1969. In recent years, the capuchins in this park have come to rely more and more on human food and to be increasingly brazen in stealing food (Figure 0.3). Their population has grown tremendously. It is very likely that the capuchins will shortly be considered a nuisance or even a pest, and face a changed attitude on the part of the citizens of Brasilia. It is possible that this will lead to a decrease in provisioning of human food (preventing access to garbage cans by frequent emptying), an increase in social conflicts, higher mortality rates, and a decrease in the population size. We believe that urban monkeys such as these provide an excellent opportunity for studying, among other interesting questions, the effects of human disturbance on monkey populations and vice versa, and the ways in which both parties can learn to live together.
Many people believe that capuchins have surprising skills and succeed in doing things that other species cannot. In the Northeast, Central and Amazonian parts of Brazil, natives tell stories of capuchins raiding corn plantations and of how they collect and transport more than one ear at a time by tying them together around the neck (Carlos Tomaz, pers. comm.). Even the castanheira (Bertholletia excelsa, see Figure 2.4d), the tough husk (pyxidium) that encases 12–22 Brazil nuts, seems not to be a problem for the ingenious capuchin. Natives in Belem (Pará, Brazil) say that the monkey has a trick: it inserts a finger into the operculum (hole) and the husk . . . magically opens (Carlos Tomaz, pers. comm.). Note that this does not actually work! In Brazil, there is also another large husked fruit of the Lecythidaceae family in the forest that is called “the monkey cup” because local people report having seen capuchin monkeys drinking from it. In Caratinga (Minas Gerais, Brazil) the elderly report that when workers are making treacle sugar, a few capuchins threaten and distract them, while others steal the sugar; moreover, the young adults also remove the tiles from the roof of a granary and steal the corn (José Rimoli, pers. comm.). Therefore, it is not surprising that the capuchin is called the “pivete da floresta” (the rascal of the forest). In a beginners’ Brazilian-Portuguese language class, we learned this idiom: macaco velho não põe a mão em cumbuca (an old capuchin does not insert its hand in a pumpkin). In other words, an experienced capuchin learns not to insert its hand through a small hole to retrieve something out of it, and by doing so prevents getting its fist stuck. Finally, in 1992, the Skank, a rock band from Belo Horizonte (Brazil) released a song with the title Macaco prego, the Brazilian name for C. apella (this name means “nail monkey” and alludes to the nail-shaped penis of the male). In this song a male capuchin advertises himself to a female with a swinging hair cut, and boasts of all his “merits” – including his determination, his Elvis Presley tufts, his free time and his lust for satisfaction.
Figure 0.3. Left, capuchins living close to urbanized areas learn to exploit picnic leftovers. Here is a Cebus libidinosus in the Parque Agua Mineral Brasilia, Brazil. (Photograph by Elisabetta Visalberghi.) Right, capuchins are easy to train. This C. albifrons is an organ grinder monkey; the photograph was taken in Lima (Peru). (Photograph courtesy of Russell Mittermeier.)
Given their obvious skills at raiding crops and people’s attitudes toward them, it is not surprising that as soon as capuchins and people compete for the same foods, capuchins become the enemy and are hunted in all possible ways. In Costa Rica, where C. capucinus are called Monos muy bravos (monkey very brash, obnoxious, tough, destructive; Fedigan, pers. obs.), Guaymi Amerindians are reported to prefer eating the meat of spider monkeys, but choose to shoot capuchins because they raid their crops (Gonzales-Kirchner and Sainz de la Maza 1998).
CAPUCHINS AS PETS
Capuchins were and still are commonly kept as pets in their native countries, as well as in the United States and Europe (Cormier 2002, 2003). In most cases Westerners own capuchins as a result of coming across them fortuitously in a pet shop or during a trip abroad where a young capuchin needed care (luckily, the international trade in primates has been curtailed significantly since the drafting of the Convention of Trade in Endangered Species of Wild Flora and Fauna (CITES) in 1973 and the imposition of export bans by producing countries; see Chapter 1). Barnard (1960, p. 1) at the beginning of a book on the adventurous life of a pet capuchin describes the typical emotional reaction of a young girl when she first saw the capuchin: “I have seen the saddest little monkey in that awful pet store where there are always dead birds in the cages and dead fish in the tanks. It must be a baby, because it’s hardly got any teeth, but all it has to eat is an enormous dog-biscuit. And it’s so cold! It’s sitting there without even a blanket, shivering and trying to fold all its arms and legs inside each other and then wrap its tail round everything: Ma, what can we do? I’m sure we can do something.” A typical rescue follows and the mother agrees to keep the tiny monkey at home. Unfortunately, monkeys grow and behave like monkeys and, sooner or later, despite all possible efforts keeping them at home becomes a nightmare. Some of them end up in a zoo. However, integrating human-reared monkeys into social groups is not always possible, and the longer the pet has been kept in a home the more difficult it is to “rehabilitate” it to live with other monkeys.
Until a few years ago, there was a sign at the Jersey Zoo by the exhibit of Piccolo, a capuchin, telling the story of the lonely C. apella who came from Brazil. “He was a pet of a sailor who sold him to a local restaurateur, who in turn gave him to the Zoo, way back in 1960. When he arrived here, he was already permanently crippled, having been kept in a small cage and fed on an inadequate diet. Despite expert veterinary care, his condition has not improved. He is kept on his own as he does not get on with other monkeys. He does like people, however, and has many friends who visit him regularly. Provided he is not in any pain, he will be able to live out his days here. Once he goes to the tropical rain forest in the sky, he will not be replaced”. Visitors were also warned not to have a monkey as a pet. When Piccolo died at about 45 years of age, the Jersey Preservation Trust (now the Durrell Wildlife Conservation Trust) built a tomb in his memory to remind people of the sad lives of pet monkeys. Unfortunately, capuchin monkeys are still available for sale in many countries!
Sometimes curiosity and interest in the animal’s behavior play an important role. As a young student in Vienna, Konrad Lorenz (who later won the Nobel prize for his ethological studies), could not resist the temptation of taking as a pet a capuchin that he named Gloria (Lorenz 1949). Gloria was left free to roam in his room while he was at home but was otherwise kept in a cage. One evening, on entering his room, Lorenz realized that something had happened: Gloria had escaped and left a trail of destruction. Among many other disasters, Gloria had dropped the lamp in the aquarium (which resulted in a short circuit and electrified its contents); then Gloria opened the latch of the book cabinet and dunked pages and pages of Lorenz’s huge and heavy medical volumes into the aquarium. The sea anemones were all dead and paper was hanging on their tentacles!
Dressed in clothes and trained to perform tricks, play music, and hold out collection cups, capuchins often accompany organ-grinders on city streets in the New World (in the Old World, macaques were used for the same purposes) (Figure 0.3). Though not common nowadays, this can still be seen in both old and recent movies. In The Cameraman (1928, directed by Edward Sedgwick), Buster Keaton is helped by an organ-grinder monkey (who switches from asking for money to operating the camera) in filming the riots in the Chinese neighborhood. The duo survives all kinds of hilarious risks; unfortunately, at the very end of this adventure Keaton’s character discovers that he forgot to load the camera with film, so that the whole event ends up being undocumented! Capuchins had roles in all kinds of movies from drama (e.g., Citizen Kane, 1941, directed by Orson Welles) to comedy, such as Babes in Toyland with Stanley Laurel and Oliver Hardy (1934, directed by Gus Meins).
Hollywood movie and television productions continue to portray capuchins as the “typical” monkey and sometimes place capuchins in countries where they do not belong, such as Egypt (Raiders of the Lost Ark, 1981 directed by Steven Spielberg). In Outbreak (1995, directed by Wolfgang Petersen), a capuchin (playing the part of an African monkey) is supposed to have spread a deadly Ebola-like virus from Africa to the United States. In Monkey Trouble (1995, directed by Franco Amurri), a capuchin is a good money-maker not only because it adorably holds out its hat but also because it is trained by a thief to be a pickpocket. And the capuchin Marcel (whose role is played by two females) was briefly a major attraction of the TV show Friends, a NBC Production that was first aired in the 1990s. A capuchin monkey participated as a cheerleader for a team that played in the 2002 World Series of baseball. Named Rally Monkey, it became so popular that fans in the stadium waved little stuffed toy monkeys at every opportunity to cheer on their team. The movie Monkey Shines – An Experiment in Fear (1988, directed by George A. Romero inspired by Stewart’s book Monkey Shines, 1983) deals with a theme of interest to primatologists: the use of capuchin monkeys as aides for quadriplegic humans and the strong emotional relationship that develops between the monkey and the human.
CAPUCHINS AS AIDES FOR DISABLED HUMANS
In the 1970s, Willard, a behavioral psychologist in the United States, started the Helping Hands project which aimed at placing trained capuchin monkeys with quadriplegic humans to provide them with functional and psychological help (Willard et al. 1982, 1985). Their dexterous hands and high trainability make capuchins well suited to perform simple tasks that are impossible for a quadriplegic person. Though the procedure followed by Helping Hands has varied somewhat through time, it involves hand rearing by volunteer families. Then, when the capuchin is sufficiently mature, it is trained by positive reinforcement for about 1 year. Eventually, after careful scrutiny of the needs and dispositions of both the disabled person and the monkey, the latter is moved to its new home and trained to perform specific tasks to assist a particular individual. This initiative raised strong concerns among the public and scientific community, one of the reasons being that by preventing the capuchin from engaging in normal social interactions, its psychological well-being would be compromised. Nevertheless, this project was followed by similar ones in Israel (founded in 1984 with the assistance of the American project), France, and Belgium (Programme d’Aide Simienne aux Personnes Tétraplégiques, Deputte and Busnel 1997).
One aim of the latter project was to investigate the learning processes involved in training and in human–monkey communication, so as to evaluate the effectiveness of the training procedures (Deputte et al. 1995, Deshaies et al. 1996, Hervé and Deputte 1993, Lejeune et al. 1998). A second aim of the project, because there was a lack of information about the costs (e.g., time, money, number of monkeys, etc.), was to assess the success of the placement program both from the disabled person’s point of view and in relation to the psychological consequences for the monkeys throughout their lives. At the moment, we know from a few reports that the presence of a capuchin has a positive influence on the social environment of the disabled (Hien and Deputte 1997; see also Willard et al. 1985) and that some of the matches between the disabled and the monkey succeed whereas other capuchins went back to zoos or similar facilities. In Israel the project was terminated for several reasons: (a) only a small number of disabled persons fit the criteria as candidates or were interested in having a monkey; (b) as the project progressed it was realized that standards for the quality of life of the capuchins would be difficult to meet in a home; and (c) the program operated on a voluntary basis, making its activities very difficult to sustain (Tamar Fredman, pers. comm.). After termination of the project, the monkeys were found a suitable home and some have since participated in experimental behavioral research (Custance et al. 1999).
CAPUCHINS IN BIOMEDICAL RESEARCH
In addition to habitat destruction and hunting, the demand for primates as laboratory animals has added further pressure on neotropical species (Mittermeier et al. 1994). Capuchins (especially C. apella) are among the neotropical primate species commonly used for biomedical research, although to a lesser extent than squirrel monkeys or owl monkeys.
Capuchins have been extensively used in research in immunology (de Palermo et al. 1988), in reproductive biology (Nagle et al. 1989, 1994), pharmacological and metabolic studies (Bergeron et al. 1992), parasitology (Garcez et al. 1997, Pereira et al. 1993), physiology (Terpstra et al. 1991), neuroscience (Bortoff and Strick 1993, Leichnetz and Gonzalo Ruiz 1996, Yamada et al. 1996), and neurotoxicity (Lifshitz et al. 1991, 1997, O’Keeffe and Lifshitz 1989). For example, evidence for a local mechanism controlling the alternating ovulatory performance of the ovaries in primates has come from capuchin monkeys (Nagle et al. 1994). They have also participated extensively in studies investigating the effects of antipsychotic medications, as they can develop some of the extrapyramidal side effects (e.g., tardive dyskinesia and dystonias) seen in schizophrenic patients (Casey 1984, Linn et al. 2001). Capuchins are also popular in behavioral pharmacology research as models for schizophrenia (Linn et al. 1999, Linn and Javitt 2001) or cognitive deficits associated with aging and Alzheimer’s disease (Bartus et al. 1980, 1983, Bartus et al. 1982, Bartus and Dean 1988).
CAPUCHINS IN BEHAVIORAL RESEARCH
Capuchins were the object of scientific behavioral investigation up to the 1940s and again from the 1970s until now. It is unclear why there were 30 years of relative disinterest. Cruz Lima (1945) wrote that “Cebus are the most common and most generally known neotropical monkeys, although from a scientific point of view the opposite is the case” (p. 133–134). However, it is possible that the life history of a very influential psychologist of this century, Harry Harlow, had something to do with switching the interest of comparative psychologists toward another species. Few people know that Harlow’s contributions to the field of primatology include a film, an unpublished manuscript, a one-page essay, and a few lines in various articles on primate learning that testify to his interest and experimental work on capuchin monkeys (Cooper and Harlow 1961, Harlow 1951, Harlow and Settlage 1934, Harlow unpubl.). In particular, Harlow carried out a few experiments on tool use in capuchin monkeys, including the combined use of a climbing pole and a box to reach a suspended reward. In this task, the monkey’s behavior following the initial success was “short of perfection” (1951, p. 219; see Figure 10.3). The only detailed description Harlow gave is of a capuchin monkey spontaneously using a stick to strike a conspecific and, on another occasion, some rhesus monkeys (Cooper and Harlow 1961). This anecdote was reported in a scientific journal 25 years after observation because the authors were reluctant to report “this unusual observation until they had achieved established reputations” (Cooper and Harlow 1961, p. 418). Their reluctance was probably due to the general conviction at that time that capuchins are not as intelligent as Old World monkeys (Yerkes 1916; cf. Chapter 7 and 9).
Harlow gave up his research on capuchins following a tuberculosis epidemic in his colony, which killed all his specimens.1 Harlow decided to concentrate all future efforts solely on the more convenient rhesus monkeys. Therefore, this practical consideration strongly selected for the use of macaques in comparative psychology and subsequently in biomedical research. Despite the fact that Harlow was aware that “the rhesus monkey lacks the gay abandon of Cebus” and that the difference between the two species “is all the difference between a Southern belle and a New England store keeper” (Harlow unpubl., p. 15), the rhesus became the classic laboratory monkey worldwide.
For many years capuchins seemed forgotten by behavioral scientists for no obvious reason. It is only in the last two decades that capuchins have been the object of renewed interest. Visalberghi (1997) documented the recent surge of studies on the behavior of capuchin monkeys. Through a computer search on the bibliographic database of the Primate Information Center of the Washington Regional Primate Research Center (USA) using Cebus and behavior and Cebus and cognition as subject entries, she found that the number of articles published in a recent 5-year block (1991–1995) had increased 10 times in comparison with an earlier 5-year block (1976–1980). A similar increase in the number of studies between these two time blocks was also found for the genus Pan, the chimpanzees and bonobos.
CONSERVATION STATUS AND THE WELL-BEING OF CAPTIVE CAPUCHINS
In the past, capuchins were extremely popular in zoos: their social attitudes and manipulative skills were much appreciated by visitors. However, their destructive behavior, their cleverness in escaping and the fact that they are generally not threatened in their natural habitats were all contributing factors to their decline in popularity in zoo exhibits. Recently, however, an international breeding program, coordinated by an International Recovery and Management Committee established by the Brazilian government, was set up for C. xanthosternos and C. apella robustus (recently re-classified as C. nigritus robustus, see Table 1.2). These two capuchins are now considered to be “Critically Endangered” and “Vulnerable”, respectively (Hilton-Taylor 2002), within their habitat, Brazil’s Atlantic Forest, now among the “hotspots” for conservation priorities (Myers et al. 2000; see Chapter 1 and Table 1.4 for further information).
Visalberghi and Anderson (1999) provide specific information on the husbandry, and physical and social environments suited for captive capuchins (see also the more general advice of the Committee on Well-Being of Nonhuman Primates 1998 and Appendix IV). In particular, they stress the capuchins’ need for social companionship despite the risks involved in group formation and in the integration of individuals into groups (Cooper et al. 2001, Fragaszy et al. 1994a; see also Visalberghi and Anderson 1993). Recently, Dettmer and Fragaszy (2000) reported that for pair-living individuals, gaining access to the social companion took precedence over gaining access to food even when the monkeys were very hungry. The presence of objects may allow capuchins to compensate for reduced opportunities for social play; Visalberghi and Guidi (1998) showed that young capuchins lacking same-age peers to play with increase their play with objects.
Given their manipulative propensities, capuchins benefit from access to objects they can handle and play with (blocks of wood, tennis balls and sturdy toys are excellent for their destructive play) as well as devices that encourage foraging activity (see also Anderson and Visalberghi 1991). While captive capuchins respond to the introduction of novel objects, it is nevertheless important to maintain or renew their interest by alternating frequently the types of objects provided. The provision of litter (5–10 cm deep) on the floor, such as ground corn cobs, woodchips, wood wool or peat, encourages locomotion and foraging (Ludes and Anderson 1996). Wood wool (long shavings of wood) and peat were more effective as enrichment; wood wool promoted the most play, while peat elicited communal peat-bathing and enhanced social contacts (Ludes-Fraulob and Anderson 1999).
Boinski et al. (1999a) used plasma and fecal cortisol measures and behavioral data to assess the effectiveness of four forms of enrichments for singly housed C. apella. The study shows significant reductions in abnormal and undesirable behaviors and an increase in normal behavior as the level of enrichment increases (control condition, two plastic toys, foraging box, toys plus foraging box). Though they did not differ significantly across conditions, the plasma cortisol measures decreased as the proportion of normal behavioral measures increased. Boinski, Gross and Davis (1999b) also found that the frequency of alarm vocalizations (usually elicited by terrestrial predators in wild monkeys and common in other stressful situations in captivity) are a good indicator of the effectiveness of the enrichment. Alarm vocalizations varied significantly across conditions, being significantly less frequent in the enriched conditions than in the control condition. Moreover, alarm vocalizations were positively related (though not significantly) to the plasma cortisol values. Therefore, at least for singly housed monkeys, measuring the frequency of alarm vocalizations might be an easy way to evaluate monkeys’ current psychological well-being.
Undoubtedly, capuchins are a very special and important primate genus. They are widely popular as pets and in exhibits, easy to keep in good health, active, highly trainable, interesting to zoologists in their own habitat, and kept by medical and behavioral scientists for reasons of expedience as well as for their special characteristics. In the following chapters the reader will find other reasons why they are so special for us and for scientific study.
1 Capuchins are less susceptible to tuberculosis than rhesus monkeys when kept in good conditions and provided with an adequate diet.