Ecotourism and primate habituation: Behavioral variation in two groups of white-faced capuchins (Cebus capucinus) from Costa Rica / Ecoturismo y habituación de primates: variación en comportamiento de dos grupos de monos carablanca (Cebus capucinus) en Costa Rica

The increase of ecotourism operations within Costa Rica during the last 20yrs has brought more and more humans into close, direct contact with several wildlife species. One of these species is the white-faced capuchin (Cebus capucinus), highly gregarious, and with exposure over time, willing to come into close vicinity of humans and their developments. Such contact has its advantages and disadvantages for the ecotourism industry. We observed white-faced monkeys in order to assess the impact of human presence and development on monkey behavior, with a focus on aggressive, affiliative, and foraging behaviors in Curú Wildlife Refuge (CWR), located in Puntarenas, Costa Rica, and to ascertain the degree of over-habituation of capuchin populations at CWR. Though there exists no discrete behavioral parameters that measure over-habituation, it can be defined as an extreme state of habituation in which non-human primates not only lose fear of humans, but also actively include humans in social interactions or treat them as a food resource. We used instantaneous focal animal and group scan sampling during 8wks in March and April 2012. Two groups (approximately 20-30 individuals each) of capuchins were observed; the first near the tourist development at the Southwestern area of CWR, representing a habituated population that regularly foraged, rested, and groomed in the presence of humans. The second, was observed in the Northeastern area of CWR, did not visit the center of human activity and exhibited fear of humans. The habituated group exhibited significantly fewer instances of threatened behavior in response to human presence (p<0.0001) than the non-habituated group, and spent significantly more time eating and foraging (p<0.0001). While the habituated monkeys at CWR may not be over-habituated, they could become that way as development, especially ecotourism, increases. Over-habituation is a problem that affects capuchins in certain ecotourism sites in Costa Rica. It is critical that the consequences of habituation be studied more carefully, primarily in areas where ecotourism operations draw visitors to wildlife habitats. Rev. Biol. Trop. 62 (3): 909-918. Epub 2014 September 01.

El aumento de actividades ecoturísticas en Costa Rica durante los últimos 20 años ha ocasionado que más y más personas entren en contacto directo y cercano con varias especies de vida silvestre. Una de estas especies es el mono carablanca (Cebus capucinus), que es muy gregario y, al pasar el tiempo, tiende a acercarse a los humanos y sus instalaciones. Tal contacto tiene ventajas y desventajas para la industria del ecoturismo. Observamos monos carablanca con el fin de evaluar el impacto de la presencia humana y la infraestructura en el comportamiento de estos animales, enfocando los comportamientos de agresión, acicalamiento y forrajeo para determinar el grado de habituación excesiva de las poblaciones de monos capuchinos en el Refugio de Vida Silvestre Curú, Puntarenas, Costa Rica. Aunque no existen parámetros específicos de comportamiento para medir la habituación excesiva, se puede definir esta condición como un estado en que los primates no humanos no solamente pierdan su temor a los humanos, sino que también incluyen a las personas activamente en sus interacciones sociales o las consideran como una fuente de alimentación. Los monos carablanca fueron observados a través del muestreo instantáneo focal y por escaneo grupal durante ocho semanas de marzo y abril de 2012. Dos grupos (aproximadamente 20-30 individuos cada uno) fueron observados; uno cerca del desarrollo turístico en la parte suroeste del refugio, que representó una población habituada que de manera regular comía, descansaba y se acicalaba en presencia de humanos; el segundo grupo, que se observó en el noreste del refugio, no visitaba el centro de actividad humana y mostraba temor hacia los humanos. El grupo habituado mostró significativamente menos ocasiones de comportamiento amenazante ante la presencia humana (p<0.0001) y empleó más tiempo comiendo y buscando alimento (p<0.0001). Aunque el grupo de habituados en Curú probablemente no tenga habituación excesiva, esta condición podría surgir más adelante, especialmente si aumenta el desarrollo, y en particular el ecoturismo. La habituación excesiva es un problema que afecta a los monos carablanca en ciertos sitios secoturísticos de Costa Rica. Es de suma importancia que las consecuencias de la habituación excesiva se estudien más a fondo, principalmente en las áreas donde las actividades ecoturísticas atraen visitantes a los hábitats de la vida silvestre.

Histochemistry profile of the biceps brachii muscle fibres of capuchin monkeys (Cebus apella, Linnaeus, 1758) / Perfil histoquímico das fibras do músculo bíceps braquial do macaco-prego (Cebus apella, Linnaeus, 1758)

A general analysis of the behaviour of “Cebus” shows that when this primate moves position to feed or perform another activity, it presents different ways of locomotion. This information shows that the brachial biceps muscle of this animal is frequently used in their locomotion activities, but it should also be remembered that this muscle is also used for other development activities like hiding, searching for objects, searching out in the woods, and digging in the soil. Considering the above, it was decided to research the histoenzimologic characteristics of the brachial biceps muscle to observe whether it is better adpted to postural or phasic function. To that end, samples were taken from the superficial and deep regions, the inserts proximal (medial and lateral) and distal brachial biceps six capuchin monkeys male and adult, which were subjected to the reactions of m-ATPase, NADH-Tr. Based on the results of these reactions fibres were classified as in Fast Twitch Glycolitic (FG), Fast Twitch Oxidative Glycolitic (FOG) and Slow Twitc (SO). In general, the results, considering the muscle as a whole, show a trend of frequency FOG> FG> SO. The data on the frequency were studied on three superficial regions FOG=FG>SO; the deep regions of the inserts proximal FOG=FG=SO and inserting the distal FOG>FG=SO. In conclusion, the biceps brachii of the capuchin monkey is well adapted for both postural and phasic activities.

Uma análise geral do comportamento do “Cebus apella” mostra que este primata quando desloca para se alimentar ou realizar outra atividade apresenta diferentes maneiras de locomoção. Estas informações mostram que o músculo bíceps braquial deste animal é usado freqüentemente nas suas atividades de locomoção, mas deve ser lembrado ainda que este músculo é usado também para desenvolvimento de outras atividades como esconder-se, procurar objetos, vasculhar arboredos, além de cavar o chão. Considerando-se o exposto acima decidiu-se pesquisar as características histoenzimológicas do músculo bíceps braquial do macaco-prego com o objetivo de comparar se este músculo esta melhor adaptado para funções posturais ou fásicas. As amostras foram retiradas das regiões superficiais e profundas; inserções proximais (medial e lateral) e distal de seis macacos-prego machos e adultos, os quais foram submetidos às reações de m-ATPase, NADH-Tr. Baseado nos resultados das reações, as fibras foram classificadas em Fast Twitch Glycolitic (FG), Fast Twitch Oxidative Glycolitic (FOG) e Slow Twitch (SO). Quanto à área dos diferentes tipos de fibras, os resultados encontrados foram semelhantes em todas as amostras estudadas, e as fibras de contração rápida foram sempre maiores do que as de contração lenta (FG=FOG>SO). Os dados obtidos sobre a frequência foram: nas três regiões superficiais estudadas FOG=FG>SO; nas regiões profundas das inserções proximais FOG=FG=SO e na inserção distal FOG>FG=SO. Baseado nestes dados pode-se concluir que o músculo bíceps braquial do macaco-prego está bem adaptado tanto para atividades posturais como fásicas.

Anatomy of the nervous of forearm and hand of cebus libidinosus (Rylands, 2000) / Anatomía de los nervios del antebrazo y mano de cebus libidinosus (Rylands, 2000)

The knowledge on the macroscopic internal structure of Cebus will provide data for histological and biochemical studies and too will contribute to ethological studies. Behavior, memory, use of tools and encephalization index have put the Cebus genus near to chimpanzees in relation to these aspects. The objective of this study is to characterize the nervous model of the forearm and hand of the Cebus monkey. For this, the main nerves and their branches located in the forearm and hand of the Cebus monkey were anatomically characterized, taking into consideration their frequency, number, origin and distribution. The data were compared with the same nerves found in specialized literature in humans, also specialized in other non-human primates. In this study, 7 Cebus libidinosus monkeys were used. The monkeys were provided by IBAMA (Brazilian Institute for the Environment and Renewable Natural Resources), from the city of Sete Lagoas, State of Minas Gerais, in 1970, and housed at the anatomy collection of the Goißs Federal University (UFG). For the nerves of the forearm of Cebus, no variations were observed in the innervation pattern of the muscles, except for the deep flexor muscle of the fingers, which in Cebus and baboons is innervated by the ulnar nerve and in humans and chimpanzees by the median nerve; however, these nerves exchange fibers in the arm and in the brachial plexus. Innervation variations may occur in the fingers of Cebus in relation to other primates, but these variations have been reported with variations in humans. This identical innervation pattern in relation to the nerves of the arm and forearm and hand in Cebus justify its use as model for anthropological evolutionary studies.

El conocimiento sobre la estructura macroscópica del interior del Cebus proporcionará datos para los estudios histológicos y bioquímicos y también contribuirá a estudios etológicos. El comportamiento, la memoria, el uso de herramientas y el índice del encefalización del género Cebus se plantean en torno a los chimpancés, en relación con estos aspectos. El objetivo de este estudio fue caracterizar el modelo de los nervios del antebrazo y la mano del mono Cebus. Para ello, los principales nervios y sus ramos situados en el antebrazo y la mano se caracterizaron anatómicamente, teniendo en cuenta sus frecuencia, número, origen y distribución. En este estudio se utilizaron 7 monos Cebus libidinosus, todos adultos sanos, con variaciones en tamaño y edad. Los monos fueron suministradas por el Ibama (Instituto Brasileño de Medio Ambiente y los Recursos Naturales Renovables), ciudad de Sete Lagoas, Estado de Minas Gerais, en 1970 de la colección anatómica de la Universidad Federal de Goiás (UFG). En el antebrazo de Cebus no se observaron variaciones en las características de los nervios de los músculos, excepto para el músculo flexor profundo de los dedos, que en Cebus y babuinos, está inervado por el nervio ulnar y en los seres humanos y los chimpancés por el nervio mediano; sin embargo, estas fibras nerviosas cambian en el cuello y en el plexo braquial. Las variaciones de los nervios pueden ocurrir en los dedos de Cebus con respecto a otros primates, pero estos cambios están relacionados con las variaciones que ocurren en los seres humanos. Este patrón similar de los nervios de los nervios del brazo y antebrazo y mano en Cebus, justifica su uso como modelo evolutivo para estudios antropológicos.

Comparative anatomical description of forearm and hand arteries of cebus libidinosus / Descripción anatómica comparativa de las arterias del antebrazo y de la mano del cebus libidinosus

Recent data justify the insertion of Cebus on behavioral and evolutionary studies in relation to the human specie, reason why researches on behavior, memory, use of tools and encephalic index demonstrate that Cebus and chimpanzees are similar. Comparative anatomical studies between Cebus and chimpanzees based on anatomical data corroborate these data on evolutionary convergence associated to muscles, nerves and vessels of the thoracic members; however, the anatomy of the forearm and hand vessels has not yet been investigated in last years. The forearm and hand arteries of Cebus are identical to other here studied primates; however, the paknaris arch, which is only one in Cebus and baboons, and princeps pollicis artery, which originated from the paknaris arch, are the main differences found for the arterial model of Cebus and for other primates. The vascularization model is identical to others primates and humans, but the hand vessels are different and more similar to baboons.

Los datos recientes justifican la inserción de Cebus en los estudios sobre la evolución y el comportamiento en relación con la especie humana ya que, investigaciones sobre su comportamiento, memoria, uso de herramientas y índice encefálico han demostrado que los chimpancés y Cebus son similares en estos aspectos. Por otra parte, estudios anatómicos comparados de los Cebus y chimpancés sobre los datos anatómicos corroboran estos hechos sobre la convergencia evolutiva asociada a los músculos, nervios y vasos de los miembros torácicos, pero la anatomía de las arterias del antebrazo y mano no se ha investigado. En el antebrazo y mano de los Cebus las arterias son idénticas a otros primates estudiados aquí, pero el arco palmar es sólo uno en los Cebus y babuinos y, la arteria principal del pulgar se origina a partir del arco palmar. Éstas son las principales diferencias encontradas para el modelo arterial de Cebus y de otros primates a excepción de los babuinos. El modelo general de la vascularización del Cebus es idéntico al de otros primates y seres humanos, pero las características particulares de algunas arterias son diferentes a éstos últimos y más similares a babuinos.

Behavioral flexibility of a group of bearded capuchin monkeys (Cebus libidinosus) in the National Park of Brasília (Brazil): consequences of cohabitation with visitors / Flexibilidade comportamental de um grupo de macacos-prego (Cebus libidinosus) no Parque Nacional de Brasília (Brasil): conseqüências da convivência com os visitantes

Increasing urbanization and deforestation have enhanced the opportunities of contact between humans and monkeys and the impact of human activities on primate behavior is receiving growing attention. This study explores whether activity budgets and diet of a group of capuchin monkeys (Cebus libidinosus) inhabiting the area of the swimming pools of the National Park of Brasília is affected by the presence of visitors providing food to them. During one year, both in the dry and the wet seasons, we scored capuchins' behavior via scan sampling every ten minutes. Results showed that this group spent less time foraging for wild foods than other comparable groups living in similar habitats. Moreover, capuchins relied more on human food during the dry season, when pulpy fruits were less available, than in the wet season. Our findings confirm other studies on different monkey species that have shown that access to human food decreases the time spent foraging for wild food and the home range size. They also show that capuchins are able to modify their diet, to exploit alternative food sources, and to change their activity budget in response to the availability of new food opportunities and to seasonal food availability.

Recentemente, o impacto de atividades humanas sobre o comportamento de primatas tem recebido maior importância dado o crescente desmatamento e urbanização, que têm favorecido o aumento do contato entre humanos e macacos. O presente estudo descreve os padrões de atividade e a dieta de um grupo de macacos-prego (Cebus libidinosus) que vive no Parque Nacional de Brasília. O Parque é freqüentado diariamente por visitantes, de modo que os animais estão habituados à presença humana, bem como ao consumo de itens de sua dieta. Observações comportamentais do grupo foram realizadas ao longo de um ano, compreendendo a estação seca e a chuvosa, utilizando-se registro de varredura a cada 10 minutos. Resultados obtidos indicaram que o grupo despendeu menos tempo forrageando itens naturais do que outros grupos vivendo em habitats similares. Além disso, durante a estação seca, quando há menor disponibilidade dos frutos de polpa, os macacos-prego alimentaram-se mais de itens da dieta humana como uma fonte alternativa de recurso. Como demonstrado em estudos anteriores realizados com outras espécies de macacos, a alimentação baseada em itens da dieta humana pareceu diminuir a motivação dos animais para forragear no seu habitat natural, assim como promoveu a redução do tempo gasto no forrageamento e a redução de sua área de uso. Nossos resultados indicaram ainda que o consumo de comida humana reflete o caráter adaptável dos animais em explorar fontes alternativas de recurso, bem como a sua habilidade em modificar a sua dieta e padrões de comportamento face às mudanças ambientais.

Comportamiento social del mono capuchino común Cebus olivaceus (Primates: Cebidae) en tres exhibiciones zoológicas de Caracas, Venezuela

Social behavior of the Wedge-capped Capuchin Monkey Cebus olivaceus (Primates: Cebidae) in three zoological exhibits of Caracas, Venezuela. Captivity represents an extreme situation for primates, especially for those with large home ranges, and its effect on their behavior might be considerable. The Wedge-capped Capuchin Monkey Cebus olivaceus is the most common primate in Venezuelan zoos. To estimate the effect of confinement on C. olivaceus behavior, we analyzed the social behavior of three groups that differed in captivity conditions, in zoological exhibits in Caracas (Caricuao, Parque del Este, El Pinar). Caricuao’s group moved freely over a non-fenced area of 15 ha, Parque del Este’s and El Pinar’s groups lived in relatively small outdoor enclosures. Social behaviors were described using focal-animal sampling, group scans and ad libitum sampling. The frequency, duration and time devoted to each behavior (per focal period per individual) were estimated. Relative dominance between pairs of individuals was established as well as affiliative associations. The repertory of social behaviors was similar between groups and to which has been observed in nature, but the duration and frequency of affiliative and agonistic interactions differed between groups. Affiliative behaviors were less frequent but longer in Caricuao than in the other two groups, while agonistic behaviors were more frequent in El Pinar and Parque del Este. Differences between groups are explained by variation in captivity conditions. We suggest that confinement generates social tension and favors agonism, while affiliative encounters help reduce this tension. On the other hand, differences in agonism between captive and natural groups may result form prolonged association, restrictions to keep optimal spacing or leave the group. All groups had some social structure (e.g., dominance ranks, association and repulsion between individuals) but the social dynamic was partly disrupted. Dominance ranks were not clear throughout the group, the top male was not dominant over the top female, dominant individuals did not interact affiliatively more than other individuals, and females did not affiliate frequently with other females. All of these observations are contrary to which has been observed in nature. As a whole, C. olivaceus tolerates captivity well because its behavioral repertoire is similar to that in natural conditions, and abnormal or undesirable behaviors (e.g., self-mutilation, stereotyped actions), were not observed. Nonetheless, there is an effect of captivity, reflected in a disruption of the social dynamic. Rev. Biol. Trop. 56 (3): 1503-1520. Epub 2008 September 30.

El confinamiento es una situación extrema para los primates con áreas de vivienda extensas, y su efecto sobre la conducta puede ser considerable. Cebus olivaceus es el primate más común en los zoológicos de Venezuela pero su conducta en esta condición no ha sido documentada. Para estimar el efecto del confinamiento sobre el comportamiento social de C. olivaceus, observamos tres grupos en zoológicos de Caracas (Caricuao, Parque del Este, El Pinar), que diferían en las condiciones de cautiverio. El grupo en Caricuao, podía desplazarse libremente en un área no cercada, mientras que en Parque del Este y El Pinar estaban en fosas relativamente pequeñas. Se determinó el repertorio de conductas sociales y la frecuencia, duración y tiempo dedicado por individuo a cada comportamiento. Se realizaron observaciones focales de cada individuo, barridos del grupo y observaciones ad libitum. Se estableció la dominancia relativa y las asociaciones afiliativas entre individuos. El repertorio de conductas sociales fue similar entre grupos y respecto a lo observado en condiciones naturales. Sin embargo, las conductas afiliativas fueron menos frecuentes pero más largas en el grupo de Caricuao, mientras que las conductas agonísticas fueron más frecuentes en Parque del Este y El Pinar. Además, el agonismo fue menos frecuente en los grupos observados que en la naturaleza. Las diferencias entre grupos se explican por la condición del cautiverio. Sugerimos que con el confinamiento incrementa la tensión social y la probabilidad de encuentros agonísticos, en contraposición, la afiliación reduciría esta tensión. Por otra parte, la convivencia prolongada, la imposibilidad de mantener distancias individuales óptimas o de migrar del grupo promoverían la reducción del agonismo, a largo plazo, lo que explicaría las diferencias con los grupos naturales. En los tres grupos hubo cierta estructura social (relaciones de dominancia, afiliaciones y repulsiones entre individuos), pero algunos aspectos de la dinámica social están alterados. Los rangos de dominancia no fueron claros, el macho alfa no dominaba a la hembra de mayor rango, los dominantes no interactuaban afiliativamente más que otros individuos, y las hembras no se afiliaban preferentemente con otras hembras. Estas observaciones son contrarias a lo descrito en la naturaleza. Globalmente C. olivaceus tolera bien el cautiverio porque presenta un repertorio de conductas similar al observado en la naturaleza y no muestra conductas anormales (auto agresión, movimientos estereotipados); sin embargo la dinámica social es afectada.

Changes of ongoing activity in Cebus monkey perirhinal cortex correlate with behavioral performance

A Cebus apella monkey weighing 4 kg was trained in a saccadic eye movement task and while the animal performed the task we recorded the extracellular activity of perirhinal cortical neurons. Although the task was very simple and maintained at a constant level of difficulty, we observed considerable changes in the performance of the monkey within each experimental session. The behavioral states responsible for such variation may be related to arousal, motivation or attention of the animal while engaged in the task. In approximately 20 percent (16/82) of the units recorded, long-term direct or inverse correlations could be demonstrated between the monkey's behavioral state and the cells' ongoing activity (independent of the visual stimulation or of the specific behavior along a trial). The perirhinal cortex and other medial temporal structures have long been associated with normal memory function. The data presented here were interpreted in terms of recent reports focusing on the subcortical afferents to temporal lobe structures and their possible role in controlling arousal, motivation, or attention.

Gastric acid secretion response in the Cebus apella: a monkey model of chronic Chagas' disease

The objective was to study the secretory pattern, both basal and stimulated either by histamine (0.1 mg/kg) or pentagastrin (64 micrograms/kg) in eighteen Cebus apella monkeys chronically infected with different T. cruzi strains (CA1, n = 10; Colombian, n = 4 and Tulahuen, n = 4) and to describe the morphological findings in the gastrointestinal tract in twelve infected (6 sacrificed and 6 spontaneously dead) and four healthy monkeys. All infected monkeys and 35 healthy ones were evaluated by contrast X-ray examination. No differences were observed in basal acid output between control and infected groups. Animals infected with the Tulahuen and Colombian strains showed significant lower values of peak acid output in response to histamine or pentagastrin (p < 0.01 and p < 0.05 respectively; t test) in comparison to the controls. Barium contrast studies showed enlargement and dilatation of the colon in three infected animals. Histopathological lesions were seen in 75% of the autopsied animals either in colon alone (33%) or both, in colon and esophagus (42%). The normal secretion observed in the CA1 infected group could be due to a lower virulence of the strain, a lower esophageal tropism or the necessity of a longer post-infection time to cause lesions

O ciclo reprodutivo de um primata brasileiro (cebus apella): curva citológica, dosagem de progesterona plasmática e exame endoscópico do ovário / Reproductive cycle of a Brazilian primate (cebus apella): cytologic curve, serum progesterone levels and endoscopic examination of the ovary

O estudo de eventos reprodutivos do "Cebus apella", um primata americano que apresenta menstruaçäo, poderia nos fornecer um animal de experimentaçäo em fisiologia ginecológica. Foram realizados a citologia vaginal diária, a dosagem de progesterona sérica no 5-, 7-, 12- e 14- dia do ciclo e o exame endoscópico do ovário no período periovulatório por duas ou três vezes com 24-48 horas de intervalo. O ciclo menstrual foi de 22,5 ñ 2 dias com a ovulaçäo ocorrendo entre 8- e 10- dia do ciclo. A progesterona sérica mostrou valores de 8,21 ñ 2,52 (ng/ml) nos 5- e 7- dias e, 35,33 ñ 7,64 (ng/jl) nos dias 12 e 14. A citologia vaginal, embora pouco precisa, permitiu a d3eterminaçäo das fases do ciclo: menstrual, folicular, periovulatória e lútea. Desta forma orienta a laparoscopia que mostrou com clareza os eventos ovarianos (folículo, estigma e corpo amarelo). Este primata apresenta perspectivas para estudos nas áreas de maturaçäo folicular, luteinizaçäo e luteólise