Behavioural profiles of captive capuchin monkeys (Sapajus spp.): analyses at group and individual levels

The use of behavioural indicators of suffering and welfare in captive animals has produced ambiguous results. In comparisons between groups, those in worse condition tend to exhibit increased overall rate of Behaviours Potentially Indicative of Stress (BPIS), but when comparing within groups, individuals differ in their stress coping strategies. This dissertation presents analyses to unravel the Behavioural Profile of a sample of 26 captive capuchin monkeys, of three different species (Sapajus libidinosus, S. flavius and S. xanthosternos), kept in different enclosure types. In total, 147,17 hours of data were collected. We explored four type of analysis: Activity Budgets, Diversity indexes, Markov chains and Sequence analyses, and Social Network Analyses, resulting in nine indexes of behavioural occurrence and organization. In chapter One we explore group differences. Results support predictions of minor sex and species differences and major differences in behavioural profile due to enclosure type: i. individuals in less enriched enclosures exhibited a more diverse BPIS repertoire and a decreased probability of a sequence with six Genus Normative Behaviour; ii. number of most probable behavioural transitions including at least one BPIS was higher in less enriched enclosures; iii. proeminence indexes indicate that BPIS function as dead ends of behavioural sequences, and proeminence of three BPIS (pacing, self-direct, active I) were higher in less enriched enclosures. Overall, these data are not supportive of BPIS as a repetitive pattern, with a mantra-like calming effect. Rather, the picture that emerges is more supportive of BPIS as activities that disrupt organization of behaviours, introducing “noise” that compromises optimal activity budget. In chapter Two we explored individual differences in stress coping strategies. We classified individuals along six axes of exploratory behaviour. These were only weakly correlated indicating low correlation among behavioural indicators of syndromes. Nevertheless, the results are suggestive of two broad stress coping strategies, similar to the bold/proactive and shy/reactive pattern: more exploratory capuchin monkeys exhibited increased values of proeminence in Pacing, aberrant sexual display and Active 1 BPIS, while less active animals exhibited increased probability in significant sequences involving at least one BPIS, and increased prominence in own stereotypy. Capuchin monkeys are known for their cognitive capacities and behavioural flexibility, therefore, the search for a consistent set of behavioural indictors of welfare and individual differences requires further studies and larger data sets. With this work we aim contributing to design scientifically grounded and statistically correct protocols for collection of behavioural data that permits comparability of results and meta-analyses, from whatever theoretical perspective interpretation it may receive.

Encoding mechanisms based on fast oscillations in the retina of the cat and their dependencies on anesthesia

Processing in the visual system starts in the retina. Its complex network of cells with different properties enables for parallel encoding and transmission of visual information to the lateral geniculate nucleus (LGN) and to the cortex. In the retina, it has been shown that responses are often accompanied by fast synchronous oscillations (30 - 90 Hz) in a stimulus-dependent manner. Studies in the frog, rabbit, cat and monkey, have shown strong oscillatory responses to large stimuli which probably encode global stimulus properties, such as size and continuity (Neuenschwander and Singer, 1996; Ishikane et al., 2005). Moreover, simultaneous recordings from different levels in the visual system have demonstrated that the oscillatory patterning of retinal ganglion cell responses are transmitted to the cortex via the LGN (Castelo-Branco et al., 1998). Overall these results suggest that feedforward synchronous oscillations contribute to visual encoding. In the present study on the LGN of the anesthetized cat, we further investigate the role of retinal oscillations in visual processing by applying complex stimuli, such as natural visual scenes, light spots of varying size and contrast, and flickering checkerboards. This is a necessary step for understanding encoding mechanisms in more naturalistic conditions, as currently most data on retinal oscillations have been limited to simple, flashed and stationary stimuli. Correlation analysis of spiking responses confirmed previous results showing that oscillatory responses in the retina (observed here from the LGN responses) largely depend on the size and stationarity of the stimulus. For natural scenes (gray-level and binary movies) oscillations appeared only for brief moments probably when receptive fields were dominated by large continuous, flat-contrast surfaces. Moreover, oscillatory responses to a circle stimulus could be broken with an annular mask indicating that synchronization arises from relatively local interactions among populations of activated cells in the retina. A surprising finding in this study was that retinal oscillations are highly dependent on halothane anesthesia levels. In the absence of halothane, oscillatory activity vanished independent of the characteristics of the stimuli. The same results were obtained for isoflurane, which has similar pharmacological properties. These new and unexpected findings question whether feedfoward oscillations in the early visual system are simply due to an imbalance between excitation and inhibition in the retinal networks generated by the halogenated anesthetics. Further studies in awake behaving animals are necessary to extend these conclusions

Cooperação em sagüis comuns callithrix jacchus: condições e restrições

The cooperative behavior is no longer a dilemma for the theory of evolution, since there are models that explain the evolution of this behavior by means of natural selection at the individual level. However, there have been few studies on the proximal factors that interfere with cooperative behavior. In the study of the influence of cognition on cooperation, many authors have been interested in situations in which individuals decide whether to act cooperatively and select partners with different qualities to cooperate. Of the factors studied, we highlight the need for understanding the apparatus and communication between partners to the occurrence of cooperation. Recently, highlight is the proposal that the ability to cooperate would be greater in species with cooperative breeding system. Thus, the common marmoset (Callithrix jacchus) is a New World monkey which stands as a valuable species for this type of study because it presents cooperative actions in nature, such as sharing food and protection of the community territory. Our experiment investigated whether common marmosets unrelated females (n = 6) were able to cooperate using an electrical and a mechanical apparatus, if this cooperation is a byproduct of individual actions or involve social attention, if it occurs inter-individual variation in the use of devices and formation of roles (producer / scrounger) in dyads. We use the number of rewards obtained by animals (Ratio of Correct Pulls) as indicators of cooperation and glances for partners (Ratio of Correct Glances) as indicators of social attention and communication. The results indicate that the type of apparatus was not a constraint for the occurrence of cooperation between the marmosets, but still has not been verified formation of roles in the dyads. The performance of animals in the two devices showed a large variation in the learning time, not having relationship with the performance in the tests phase. In both devices the level of social glances at control phases were casually correlated with any other phase, but the data showed that there was not social attention, that is, the monkeys realized that they gave food to the partners, but the partners did

Uso de ferramentas por macacos-prego em manguezais

The present study discusses the geographical distribution and the context on the occupation of mangrove swamp areas by capuchin monkeys. In addition, we assess how the dispersion to the mangrove allowed the exploration of different food items, permitting the development of predation by ambush and the use of cracking tools. From 2004 to 2008 we surveyed the main estuaries of Brazilian Amazon coast, from northeastern state of Pará to the eastern boundary of the state of Maranhão, and recorded the presence of two species of capuchin monkeys in the mangrove forest areas. Cebus apella has been widely distributed in the mangrove at the estuaries examined (excluding C. libidinosus areas). Its presence is often related to Amazon forest remnants in the neighbourhood of the mangrove swamps and thus it is possible that some groups live in both kinds of habitats. However, we recorded some populations restricted only to mangrove swamp surrounded by open areas. On the other hand, Cebus libidinosus had a distribution more restricted and isolated in mangroves. Its pattern of habitat use is consistent with geographic distribution in mangrove patches. It seems that the possible contact zone previously proposed in the literature for that two species has no evident barriers in the mangrove. Furthermore, we record cracking sites and systematic observations on the tool use, carnivory and predation by ambush in Cebus libidinosus from 2006 to 2008. Cebus libidinosus is the only Neotropical primate species in which the tool use has been systematically recorded in nature. However all previous studies had been obtained is open areas (Cerrado and Caatinga). Thus, the present study is first one to report that behaviour in forested habitats in which the tool use to cracking by capuchin monkeys is associated with the consumption of meat. In the Caatinga and Cerrado, food shortages and terrestriality has been proposed by different authors to explain the evolution of tool use in primates. Here, we analyzed the relative contribution of these two variables as selective pressures for the tool use by capuchin monkeys in the mangrove forests, an ecological scenario in which food resources is available around the year and terrestriality is limited by structural habitat features, as the presence of stilt roots and muddy soil

Otimização no uso de martelos e bigornas para quebrar sementes por macacos prego (Cebus flavius e C. libidinosus) no Bioma Caatinga

Recently, capuchin monkeys (Cebus spp.) inhabitants of dry environments and with restriction of fleshy fruits, have been the subject of several studies regarding the use of instruments. During behaviour of using stones to crack open nuts there is evidence of selection of more effective hammers, as well as selection of anvils related to reducing the risk of predation. The aim of this study was to determine whether two groups of capuchin monkeys (C.flavius and and C.libidinosus) inhabitants of the Caatinga of Rio Grande do Norte make choice of hammers and anvils. The record of weight and location of stones indicated active choices of with what (choice of hammers) and where (selection of anvils) to crack open encapsulated seeds. The choice of hammers to break nuts depended on the type and degree of ripeness seed. Thus, smaller seeds were smashed with lighter hammers and larger seeds with heavier hammers. Still, C. flavius was the only species that presented a refinement in the choice of hammers that depended on the ripeness of seeds. For both species of capuchin monkeys studied, the nut-crack sites were not spread in accordance with the spatial distribution of seed-producing species, suggesting that the capuchin monkeys promote active choice of anvils. Thus, in environments with more escape routes through the trees, the nut-crack sites were found further apart than in regions that had less chance of escape through the trees. Also, there was a difference in the spacing of the anvils to depend on the type of seed: sites used to crack larger and more caloric seeds were found farther apart than the sites used to crack smaller and less caloric seeds, suggesting a pattern of avoiding direct competition. We conclude that the capuchin monkeys maximize energy savings and reduced risk of predation and the costs of food competition during the behaviour of using stones to crack open nuts

Preferência e competição alimentar em um grupo de Sapajus flavius em fragmento de Mata Atlântica em Caaporã – Paraíba – Brasil

Feeding is the primary selective pressure in all forms of animals. Nutritional ecological models predict consequences of preferred and non-preferred food consumption on behavioural, physiological and morphological adaptations. At same time, socioecological models infer socio-organizarion patterns based on feeding competition faced by animals. A list of preferred foods, and inferences regarding the intensity of feeding competition and its behavioural consequences are information of much importance for management of populations in fragments. In this work we observed the feeding behavior and spatial positioning of a group of more than 100 blond capuchin monkeys (Sapajus flavius) that inhabit a fragment of Atlantic forest, surrounded by sugarcane plantation. We compared the consumption of different food items with their monthly availability in the area to define the preferred and fallback food items. We recorded the vocalizations of aggression and the inter-individual distance (area of Minimum Convex Polygon/n individuals) to infer the type of food competition experienced by animals. In the year studied the fruit feeding time correlated with top consumed fruit productivity, indicating preference for fruits. Our data indicate that the species Elaeis sp., Cecropia palmata, Inga spp. and Simarouba amara are the preferred food items in the diet. Available all year round and uniformly distributed, sugarcane was a regular item in the diet and its was characterized as a staple fallback food for this group. Although fruits are preferential food items, direct competition rate did not correlate to fruit productivity in the area, maintaining the high rates throughout the year (2.45 events/ hour). The inter-individual distance index positively correlated with rain fall indicating scramble food competition. The number of neighbours of females carrying infants was smaller when fruit productivity is low, indicating that females carrying infants are suffering increased indirect competition. Our data indicates that blond capuchins in this fragment make use of sugar cane as a staple fallback food, which evidence the importance of sugar cane landscape for the survival of this critically endangered capuchin species in fragmented habitats in Northeast Brazil. A preliminary list of preferred and important foods is offered, and can assist in the choice of trees for reforestation, better fragments to be preserved and areas of release and translocation of animals. We did not observe an increase of contest competition while using preferred foods, but when using staple FBF. This may be due the altered environment, which results in high competition food throughout the year. Both the food preference as the social and behavioral consequences of high food competition experienced by animals in this fragment must be accompanied over the years to ensure the survival of this population.

Preferência e competição alimentar em um grupo de Sapajus flavius em fragmento de Mata Atlântica em Caaporã – Paraíba – Brasil

Feeding is the primary selective pressure in all forms of animals. Nutritional ecological models predict consequences of preferred and non-preferred food consumption on behavioural, physiological and morphological adaptations. At same time, socioecological models infer socio-organizarion patterns based on feeding competition faced by animals. A list of preferred foods, and inferences regarding the intensity of feeding competition and its behavioural consequences are information of much importance for management of populations in fragments. In this work we observed the feeding behavior and spatial positioning of a group of more than 100 blond capuchin monkeys (Sapajus flavius) that inhabit a fragment of Atlantic forest, surrounded by sugarcane plantation. We compared the consumption of different food items with their monthly availability in the area to define the preferred and fallback food items. We recorded the vocalizations of aggression and the inter-individual distance (area of Minimum Convex Polygon/n individuals) to infer the type of food competition experienced by animals. In the year studied the fruit feeding time correlated with top consumed fruit productivity, indicating preference for fruits. Our data indicate that the species Elaeis sp., Cecropia palmata, Inga spp. and Simarouba amara are the preferred food items in the diet. Available all year round and uniformly distributed, sugarcane was a regular item in the diet and its was characterized as a staple fallback food for this group. Although fruits are preferential food items, direct competition rate did not correlate to fruit productivity in the area, maintaining the high rates throughout the year (2.45 events/ hour). The inter-individual distance index positively correlated with rain fall indicating scramble food competition. The number of neighbours of females carrying infants was smaller when fruit productivity is low, indicating that females carrying infants are suffering increased indirect competition. Our data indicates that blond capuchins in this fragment make use of sugar cane as a staple fallback food, which evidence the importance of sugar cane landscape for the survival of this critically endangered capuchin species in fragmented habitats in Northeast Brazil. A preliminary list of preferred and important foods is offered, and can assist in the choice of trees for reforestation, better fragments to be preserved and areas of release and translocation of animals. We did not observe an increase of contest competition while using preferred foods, but when using staple FBF. This may be due the altered environment, which results in high competition food throughout the year. Both the food preference as the social and behavioral consequences of high food competition experienced by animals in this fragment must be accompanied over the years to ensure the survival of this population.