Investigation of stress in primates maintained in zoo and its main implications on behavior and well-being

Brazil is considered the country which holds the largest number of known primate species. At captives without environmental enrichment program, especially in zoos, it is common for the animals to be easily discouraged from captive life, being bound to develop chronic stress condition. This review aimed to provide veterinary professionals and students with updated bibliography on stress in zoo captive primates, focusing on reactions resulting from these changes, as well as their implications for behavior and well-being. Integrative literature review using descriptors "Captivity", "Stress", "Primates", "Zoos" and "Wellbeing", on the main scientific research bases. The present work highlighted stress responses and its consequences on primate’s health and behavior captive in zoo through bibliographic survey, performing selected articles analysis, results interpretation, and discussion. It is concluded behavioral profile individual variations expose primates differently to stressful conditions. Public visitation, lack of structure, reduced enclosure, improper nutritional management, and unstimulated environment may be potential stress sources for some housed primates in zoo.


Introduction
Brazil is considered the country which holds the largest number of known primate species (AURICCHIO, 2017

Conceição, Conceição
Investigation of stress in primates maintained in zoo and its main implications... Treatment Center) throughout the country. Overpopulation in these establishments is often caused by the large number of seizures and the lack of structure and space to keep the animals for an extended period (SOUSA, 2014). The captivity which presents better conditions, and the possibility of animal welfare is the zoo, once the institutions mentioned above are overcrowded (SOUSA, 2014).
The Zoo can be defined as an establishment authorized by IBAMA, which houses several wild animals' species kept alive in captivity or in semifreedom. Its role is to replicate the natural environment, preserving the sheltered species habits. The animals are exposed to public visitation, as well as to serve scientific, conservationist, educational and socio-cultural purposes (IBAMA, 2008).
The Order of Primates represents a group of mammals, generally found in tropical regions of the planet, occupying the most varied types of habitats, from savannas to dense tropical forests (FORTES & MARQUES, 2005). They are highly active animals in free life that usually spend a good part of their day looking for food and getting around. Due to such characteristics, the insertion of these animals in an ex-situ environment such as captivity may develop health and well-being problems, frequently related to chronic stress situation (COSTA & PINTO, 2003), triggering high levels of stress and stereotyped behaviors (BERTOLI, 2017;POMERANTZ MEIRI & TERKEL, 2013).
Several studies that address the physiology of stress emphasize the need for understanding of physiological mechanisms, mainly neurophysiology, once the response to stress in mammals is mediated via the sympathetic nervous system and the neuroendocrine system (DUARTE, 2016;MARGIS et al, 2003). The stress investigation in primates kept in zoo and its implications for behavior and well-being may be a useful element in forming environmental awareness programs aimed at captive environment improvements. Such measures must take account of health promotion of the Conceição, Conceição Investigation of stress in primates maintained in zoo and its main implications... animal welfare housed in captive zoo environment. In short, as primates are strongly affected by habitat fragmentation and found in large number in zoos, research evaluating the species' interactions with humans and its impacts on their behavior and well-being is necessary.
Therefore, the present review aimed to study the causes of stress in primates kept in zoos, focusing on the reactions resulting from these changes as well as their implications for behavior and well-being. It also identified some techniques which may be used to minimize the effects that the stressful condition may cause in confined primates.

Material and methods
The integrative review method was used to analyze the causes of stress in primates kept in zoos, focusing on the reactions resulting from these changes, as well as their implications for behavior and well-being. For During selection process, it was chosen articles written in English, Portuguese, and Spanish, published over a period of more than 10 years.
The online availability of articles also influenced the choice, once several articles were blocked for access. Subsequently, the most recent articles composed of the main criteria and keywords were evaluated.
Based on the concepts presented by the authors, 26 articles were selected to carry out and develop this integrative review. Based on the inclusion and exclusion criteria, the number of articles found and included in the study was defined and data are shown in Table 1.
Publications found in more than one source were added to the count only on the first interface on which they were found.
Therefore, from 48 articles found, 26 were included in the study, adding up to total of the 3 information resources used in this review.

Stress
Following the definition of stress, the individual's exposure to a particular stressor will cause several body changes, which will try to adapt to new conditions to maintain homeostasis (SEYLE, 1946;MOBERG, 2000;MARGIS et al., 2003;ORSINI & BONDAN, 2006;GALVÃO-COELHO et al., 2015;FERREIRA, 2017;KOSCINCZUK, 2014). This process is defined as General Adaptation Syndrome (SGA), which is the set of responses triggered by a stressor and, according to Seyle (1946) and Moberg (2000), it can be divided into three stages: alarm or alert; resistance or adaptation; exhaustion or exhaustion.
Alarm or alert -the primate faces the stressor, and the balance is disrupted. In this process, activation of sympathetic autonomic nervous system occurs, which will cause the animals to be alert, causing cardiovascular changes such as elevated blood pressure, tachycardia, decreased blood circulation from peripheral regions to vital organs. Due to respiratory rate increase, there is greater oxygen availability; moreover, there is glucose release by the liver leading to increase the energy availability of muscles (DICKSON 1996;GALVÃO-COELHO et al., 2015;ORSINI, 2006  As a result, the study stated that individuals isolated in "individual cages" and individuals in the "dual male" treatment demonstrated less "typical" behaviors of species and higher abnormal behaviors levels due to the lack of movement possibility and social interaction, resulting in many stereotypes.
Such author concluded that social isolation is one of the factors that can contribute to the compromise of well-being.
The study by Sousa (2014)  In this literature, capuchin monkeys kept in quarantine in the absence of environmental stimuli showed more stereotyped behaviors resulting from stress than the group maintained in semi-captive environments.
Emphasizing that behaviors associated with stress are common in isolation.
Additionally, Ferreira (2017) also described the existence of different behavioral profiles within the same population, which react differently to stress. The correlations of results and level of MFG analysis showed several stereotyped behaviors exhibited by the species against certain environmental conditions. Such study also concluded that more sociable animals are more resilient, both at the physiological and behavioral levels to the stresses of captivity. Guimarães (2012) and Barlow et al. (2006) demonstrated the changes due to visitor's presence on the primate species behavior: Diana monkey (Cercopithecus diana diana) red howler monkey (Alouatta guariba) and capuchin monkey (Sapajus Apella) in zoos. Barlow et al. (2006) described that certain individuals of Diana monkey species are more likely to exhibit stress-indicative behavior (CIE) when visitor density is increased.
Additionally, for part of individuals, it caused positive responses, showing significant increase in affiliative behavior, such as play.
On the other hand, Guimaraes (2012)

Conclusion
Through the survey of works carried out, it was possible to arrive at three major themes which surround such research such as: chronic stress, impact of public visitation, environmental enrichment, and well-being. It is concluded that individual variations in the behavioral profile expose animals differently to stressful conditions. Public visitation, lack of structure, reduced enclosure, improper nutritional management, and unstimulated environment, may be potential stress sources for some housed primates in zoo. Different strategies to cope with stress must be developed for each species of captive primate in zoos, as an attempt to find and apply the best environmental enrichment project to help reducing the stress of primates of different species inserted in the zoo. *** Conceição, Conceição Investigation of stress in primates maintained in zoo and its main implications... facilmente com a vida cativa, principalmente em zoológicos, podendo desenvolver uma condição de estresse crônico. Esta revisão teve por objetivo contribuir para a promoção de maior bem-estar aos indivíduos que vivem em cativeiros e servir de auxílio para os profissionais e estudantes de veterinária com atualizações da bibliografia referente ao estresse em primatas cativos no zoológico, enfocando as reações decorrentes dessas alterações, bem como suas implicâncias no comportamento e bem-estar. Revisão integrativa da literatura utilizando os descritores "Cativeiro", "Estresse", "Primatas", "Zoológicos" e "Bem-Estar" nas principais bases de pesquisa cientifica. O presente trabalho obteve a identificação das respostas geradas pelo estresse e as suas consequências na saúde e no comportamento de primatas cativos em zoológicos por meio de levantamento bibliográfico, realizando a análise dos artigos selecionados na pesquisa, a interpretação e a discussão dos resultados obtidos.