Environmental enrichment for neotropical

Environmental enrichment for neotropical

(Parte 1 de 4)

Ciência Rural, Santa Maria, v.31, n.3, p.543-551, 2001 ISSN 0103-8478

Recebido para publicação em 04.1.9Aprovado em 30.08.0


1Médico Veterinário, Professor Assistente, MSc, Universidade de Brasília. Departamento de Ciências Fisiológicas, Centro de Primatologia, Universidade de Brasília, 70910-900, Distrito Federal. E - mail: vanner@unb.br. Autor para correspondência.

Captivity is an extreme non-natural environment for primates. The success of a breeding colony depends of management and veterinarian procedures which must rely on the knowledge of primates’ behavioral needs. Environmental enrichment consists of a series of procedures that improve the quality of life of captive animals by meeting their ethological needs. Enrichment can reduce stress, while increasing animal well being in captivity. Suitable ethical conditions, incidences of behavioral disorders, minimal clinical interventions, low mortality, higher reproduction rates and cost/benefit relationship, reflect directly on the quality of captive breeding colonies. Anthropoids like Neotropical primates possess complex neural structures and relate, in a sophisticated manner, to the environment. This review reports important experiences on enrichment procedures for Neotropical primates and the physiological events which could explain improvement of animal well-being.

Key words: environmental enrichment; non-human primates; Neotropical primates; well-being.

Cativeiro é um ambiente de extremos não naturais para primatas. O sucesso de uma criação de primatas depende do manejo e de procedimentos veterinários que devem considerar as necessidades etológicas dos animais cativos. Enriquecimento ambiental é um conjunto de técnicas que modificam o ambiente, resultando em uma melhora na qualidade de vida dos animais, ao satisfazer as suas necessidades comportamentais. O enriquecimento pode diminuir o estresse e melhorar o bem-estar. Primatas neotropicais se caracterizam por complexas estruturas neurais e se relacionam de maneira sofisticada com o ambiente. O enriquecimento ambiental pode aumentar a qualidade de uma criação ao adequar o manejo a padrões éticos aceitáveis, estimular o repertório normal do comportamento, diminuir a casuística clínica, diminuir a mortalidade, incrementar a taxa reprodutiva e maximizar a relação custo/benefício em uma criação. Esta revisão relata experiências relevantes nos procedimentos de enriquecimento para primatas neotropicais, além de comentar as bases fisiológicas em que essas intervenções melhoram o bem-estar dos animais cativos.

Palavras-chave: enriquecimento ambiental, primatas não humanos, primatas neotropicais; bemestar.

Breeding primates in captivity serves to research, educational, conservation and recreation purposes. In captivity, the success of a breeding colony depends on the management and veterinarian procedures which must rely on the knowledge of primates’ behavioral needs. Environmental enrichment consists of a series of procedures that modify the physical or social environment, improving the quality of life of captive animals by meeting their ethological needs. Environmental enrichment, well-being and stress are associated concepts regarding techniques, physiology and behavior aspects. Enrichment can reduce stress, while increasing animal well-being and health in captivity. Ethological needs of anthropoids like Neotropical primates (Infraorder Platyrrhini), although similar to those of other animals, have great cognitive and emotional components. Maintaining enriched home cages is not only justified by technical aspects. Moral and ethical issues are implicitly involved, especially due to the growing concept that human beings are more and


Ciência Rural, v. 31, n. 3, 2001.

more similar to other species from a functional perspective. The general public absorbs massive information from the media (regarding animal welfare, animal behavior, cruelty, conservation), and in turn demand more ethical and moral guidelines for maintenance of breeding colonies (MENCH & KREGER, 1996). Various countries have implemented legislation, regulating the use and treatment of animals, increasing demands on captivity maintenance.

Optimal conditions in natural environments are not usually found. However, wild animals develop adaptive responses, adjusting more easily to unforeseen disruptive events. Facing daily, and potentially life-threatening challenges, these animals undergo a selective process, in which certain individuals are better suited to cope with present and future events. There are ontogenetic and phylogenetic basis on this issue. In fact, each individual is the outcome in itself of this selective process that occurred in their ancestors. Animals must adapt to harsh and varying environments, search for food, select suitable shelters, interact with conspecifics, reproduce, play, avoid predators and recognize surroundings. Daily routines impose constant need for alternative and diversified strategies, in which events must be learned, selected, and interrelated to arrive at immediate and future decisions. Individuals do not merely respond automatically to stimuli, but interact selectively and are permanently alert to significant novelties affecting their lives. Therefore, compared to other mammals, primates are strongly predisposed to continuously select and respond to novel stimuli in the environment.

Discrepancies in these processes, due to captive environments, have profound effects on physiological, cognitive and emotional states. Captivity is an incomparably more stationary environment, reducing attention and propensity to seek and relate to novelty. Prolonged periods of low stimulation lead to gradual losses of attention and search capabilities of new stimuli. The environment loses significance and the individual remains in a constant state of boredom. “Environmental poverty”, defined as inappropriate social and physical surroundings, related to their ideal needs, can trigger a series of extreme non-adaptive responses. These can either be subtle (e. g., lymphopenia), (BOCCIA et al., 1992; LEONARD & SONG, 1996), or may develop into more serious disorders, such as stereotyped behaviors, cognitive deficits, emotional disturbances (overt aggressiveness or depression), inadequate mating and death (MEYERHOLZAPFEL, 1968; HARLOW et al., 1971; UNO et al., 1989; MASON, 1991a). Dramatic data on the viability of primate populations in captivity have been reported, estimating, for example, that two in every three primates captured in the wild and taken into captivity, die (CASTRO, 1977). Such an example illustrates the high cost of animal life for starting and implementing captive breeding colonies, decreasing biological diversity and implying in economic losses. Good colony management, including enriched environments, may decrease such unacceptable statistics. By implementing few, general and basic measures of captivity maintenance and enrichment, mortality rates have dropped several times in some colonies (ROBERTS, 1989; personal observation). Ultimately, extreme non-adaptive responses are due to chronic stress, a neuroendocrinal and psychological response of the organism in an attempt to maintain homeostasis when facing prolonged unfavorable situations. Complete neurological development is enhanced by enriched conditions, potentially influencing behavioral complexity. Induced protein synthesis in nerve tissue, increased weight of key structure involved in cognitive processes, and local synaptic strengthening are observed (ROSENZWEIG, 1996). Adaptive physiological and behavioral responses when facing stressful events depend on neural integrity. Animals in enriched environments are more able to solve problems, as in the maintenance routines of manipulations, clinical check-ups, restraining, weighing, social regrouping and home cage relocations.

Immediate responses to environmental shifts are mediated by two main interdependent control systems, the Autonomic Nervous System (ANS) and the hippocampus and HPA axis (Hypothalamic-Pituitary-Adrenal). U nder strong stimulation, ANS activates the adrenal medulla, releasing catecholamines into the bloodstream. Epinephrine, the main hormone released by the adrenal medulla, rapidly anticipates the body for “fight or flight” reactions, through mobilization of glucose and functional inhibition of systems not essential for immediate survival, like the reproductive and digestive systems (SAPOLSKY, 1993). Prolonged action of epinephrine can rapidly lead to cardiac and respiratory collapse. The hippocampal formation and amigdala, constitutes an important station for selecting sensory and emotional information inputs. Its structures and nuclei are considered the bottle-neck structures of

Environmental enrichment for neotropical primates in captivity.

Ciência Rural, v. 31, n. 3, 2001.

memory and learning processes (MARKOWITSCH, 1996). During stressful episodes, activation of the HPA axis occurs through afferent projections, both of the hippocampus and amigdala, to hypothalamus. The final result is secretion of glucocorticoids (cortisol) by the adrenal cortex, which mobilizes stored energy, activates gluconeogenesis, impairs anabolism, and acts as a negative feedback mechanism of the ANS and hippocampus-HPA activation. Efficiency of this process depends on the integrity and balance between Type I (or MR, mineralocorticoid) and Type I (or GR, glucocorticoid) r eceptors (SAPOLSKY,1993). Under intense stress, the ability to regulate the hypothalamic-pituitary-adrenal system in adaptive responses is compromised, due to a impairment of feedback control. Glucocorticoids, through neural metabolism change, diminishing spines of dendrites, mainly in the CA3 region of hippocampus, perform a counterbalance role to protect neurons from action of excitatory neurotransmitters (SAPOLSKY,1993). However, certain levels of atrophy in the hippocampus (UNO et al.,1989) or neuronal death in the gyrus dentate (GOULD et al., 1998), may also be identified during extreme stress. Prolonged and relevant experiences, as in extended periods of stress, alter cellular genetic expression (McEWEN, 1996; ROSENZWEIG, 1996). Reduced ability to sustain tetanic stimulation by excitatory neurotransmitters facilitates neural damages (SAPOLSKY, 1993) through increased calcium uptake, activation of second-messengers, and intracellular metabolite depletion. Neural fatigue, accelerated cell degeneration, and cell death

(apoptosis) usually follow. The action of glucocorticoids is time-dependent: severe stress, during certain stages of development, increases aging neural degeneration. However, early and slight age-dependent stimulation postpones this condition (McEWEN, 1996). As cortisol acts permissively towards actions of other hormones, various other systems may be affected. Neurochemical evidences indicate that severe stress, adequately represented by impoverished environments, alter anti-oxidative capabilities in neurons. Other neural pathways, employing different neurotransmitters, are also involved, causing serious motor disorders and consumptive behaviors. Dopaminergic pathways of the mesolimbic and nigro-striatum pathways are associated to rewarding (pleasant) events and voluntary movements, respectively. Changes in dopaminergic sensibility are associated to sustained periods of social isolation, a type of severe stress in primates (LEWIS et al., 1990; IMPERATO et al., 1991). Stereotyped behaviors may experimentally be induced by administration of high doses of amphetamines, drugs which increase dopamine levels in the synaptic cleft. Endorfinergic pathways have been implicated in stereotyped behaviors. Recurrent behaviors may lead to an increased internal wellbeing by promoting a state of euphoria (POOLE, 1991). Auto-mutilation syndrome results from dysfunctional interactions between noradrenergic and serotoninergic systems, both of which are implicated in the expression and control of aggressiveness (KRAEMER & CLARKE, 1990). It has been showed that animals with high aggressive and impulsive behavior have lower brain serotonine levels than tame animals (TRUT, 1999). Finally, movement and exploratory restrictions decrease acetylcholine synthesis in cortical areas of the brain related to cognition (MITSUSHIMA et al., 1998). The outcome from this interaction originates motor, motivational, attention, emotional, and cognitive systems activation, and the expression of behaviors. These, in turn, act mainly to modify the environment. In non-responsive or hostile environments, effects influence neural metabolism directly, modifying behavior.

Simple structural modifications, changes in daily routines and proper socialization are sufficient measures to stimulate and improve the psychological state and welfare of the colony (Figure 1). Stimuli may not necessarily be protective or pleasant. Mild stress stimuli, like brief exposures to simulated predators, may induce behaviors similar to those occurring in the wild, and are, therefore, desirable (CHAMOVE & MOODIE, 1990; VITALE et al., 1991). Some behaviors will only be expressed in captivity. Marmosets in captivity, for example, sleep in nest-boxes, behavior not observed in natural environments. Other aspects of captive colony management must be evaluated, as seen fit, deciding if changes to be introduced will compromise the group’s physical and mental health. Nonetheless, environmental enrichment is mainly aimed at introducing changes in the surroundings, eliciting behavioral patterns normally found in the wild. Some experimental protocols, considering their ethical and methodological aspects, require impoverished environments. However, whenever possible, augmenting stimulation opportunities, maintaining optimal sanitary conditions, providing adequate nourishment and social fulfillment must be taken into consideration. Adequate and enriched surroundings improve animal health, reflect on research quality and influence colony maintenance costs (NOVAK & SUOMI, 1988).

Ideally, an adequate diagnosis of the environment requires an evaluation of both


Ciência Rural, v. 31, n. 3, 2001.

physiological and behavioral indicators (MENDOZA, 1991). A simple health parameter consists in periodically evaluating the weight and growth curves of the animals. Clinical history showing frequent occurrences of diseases and skin lacerations indicate to inadequate captive environments. Other auxiliary laboratory parameters are used to evaluate chronic stress, such as cortisol and its metabolite levels in the plasma, urine, feces or saliva (COE & ROSENBLUM, 1978;

SALTZMAN et al., 1994; SMITH & FRENCH, 1997). In this case, one have keep in mind that physiological cortisol levels in Neotropical primates is too higher than Old World monkeys (BRANDON et al, 1989). Leukocyte evaluation is also useful, where linfopenia was found to be associated, to some extent, to stress and behavioral disorders (LEONARD & SONG, 1996). Ethological indicators are measures more easily accessible to detect inadequate individual needs in captivity. Prior to any change to be introduced, one must have good background knowledge of the species in consideration. In the absence of available data for that species, one must consider the closest taxonomic level. Some behaviors are especially disturbed by stress: increased aggressiveness, abnormal behaviors, and disorderly locomotor activities, with lower body contacts and grooming (CHAMOVE et al., 1988; SCHOENFELD, 1989). Frequent scratching and reduced exploratory behaviors are observed in anxiety, a psychological and physiological state of anticipated fear (BAKER & AURELI, 1997;

BARROS et al., 2000). Animals maintained in impoverished environments seem to have lower expectations towards stimuli in their surrounding, decreasing motor performance, motivation and consumptive behaviors (CARLSTEAD, 1996). This unresponsive scenario constitutes a state of boredom that, under the impact of intense stimuli, may lead to sudden death. Under these same conditions, some individuals develop alternative strategies in the hope of increasing environmental stimulation, such as coprophagy, hyperaggressiveness, hy persexuality, inappropriate sexual behavior (copulating attempts with objects), abnormal postures, low socialization,


Callithrix jacchusAlternated access to an exercise cageIncreased locomotor activityHEARN et al., 1978

C. jacchusArtificial “gum tree”Active exploration of the apparatusMcGREW et al., 1986

C. jacchusIncrease home cage size and complexityPositive behaviors where mainly due do environmental complexity, than increased home cage size.

KERL & ROTHE, 1996

C. jacchusAdd new support substrates and increase foraging difficulty

Increasing foraging; for infants, increased foraging, play and social grooming

PELEGRINO et al., 1997

CallithrixTrunks and branches, ground covered with plants, infra-red lamp

Stress decreased and successful mating occurred; effective protection against the cold

CARROL, 1991

Callithrix and Saguinus

Branches and tree trunks, periodically rearranged in the home cage

Increased exploration and provided appropriate substrates SNOWDON & SAVAGE, 1989

Saguinus mystax, S. labiatus

Foraging tray and dispenser with an increasing access difficulty device

Successful acceptance of foraging tray, however unsuccessful with the dispenser

EVANS et al., 1989

S. oedipusIncrease number of feeding trays, shifts in food location, food “search” apparatus and introduction of new items

Increased exploratory activity; lower aggressive behaviors GLICK-BAUER, 1997

Saimiri sciureusLarger and more complex home cage; feeding device

Increased locomotor in the beginning, followed by a decrease in movement; specie-specific patterns of behavior


S. sciureusIntroduction of novel objects; a apparatuses with food rewards

Increased manipulation, while decreasing stereotyped behaviors BOINSKI et al., 1994

(Parte 1 de 4)