Do zoo-housed primates retreat from crowds? A simple study of five primate species.

An animal's welfare state is directly influenced by the mental state, which is shaped by experiences within the environment throughout the animal's life. For zoo-housed animals, visitors to the zoo are a large part of that environment and a fluctuating influence within it. This study examines the impact of zoo visitors on the space use of five species of zoo-housed primates (Eastern black-and-white colobus monkeys, Colobus guereza, n = 5, Allen's swamp monkeys, Allenopithecus nigroviridis, n = 2, DeBrazza's monkeys, Cercopithecus neglectus, n = 3, Bolivian gray titi monkeys, Callicebus donacophilus, n = 3, and crowned lemurs, Eulemur coronatus, n = 3). Specifically, we considered whether primates' distance from visitor areas changed as crowd sizes increased. Data were collected using the ZooMonitor app. Observers recorded spatial coordinates for each animal over periods ranging from 12 to 32 months. Data were analyzed using two types of regression models (linear and logistic) to examine the influence of visitors on the location of the primates. Both analyses revealed a statistically significant but small decrease in primate distance from visitor viewing glass as the number of visitors increased. Behavioral indicators of welfare were also unaffected by the presence of visitors. These results suggest that, with additional validation, distance from visitors may be one promising, simple way to evaluate the influence of visitors on primate welfare.

Wavy multistratified amacrine cells in the monkey retina contain immunoreactive secretoneurin.

The goals of this study were to describe the morphology, neurotransmitter content and synaptic connections of neurons in primate retinas that contain the neuropeptide secretoneurin. Amacrine cells were labeled with antibodies to secretoneurin in macaque and baboon retinas. Their processes formed three distinct plexuses in the inner plexiform layer: one in the outermost stratum, one in the center and one in the innermost stratum. In light microscopic double immunolabeling experiments, GABA was colocalized with secretoneurin in these cells, but glycine transporter 1 and Substance P were not. ON bipolar cell axon terminals labeled with antibody to the cholecystokinin precursor, G6-gly, have ON responses to stimulation of short wavelength sensitive (S) cones. Axons of these bipolar cells made contacts with amacrine cell dendrites containing secretoneurin. Secretoneurin-IR amacrine cells also made contacts with retinal ganglion cell dendrites labeled with antibody to the photopigment melanopsin, which have OFF responses to stimulation of S cones. Using electron microscopic immunolabeling, 436 synapses from macaque retina were analyzed. Axons from bipolar cells were identified by their characteristic synaptic ribbons; their synaptic densities were asymmetric like those of excitatory synapses in the brain. Amacrine cells made and received conventional synapses with symmetric synaptic densities, like those of inhibitory synapses in the brain. Ganglion cell dendrites were identified by their absence of presynaptic specializations; they received inputs from both amacrine cells and bipolar cells. The majority of inputs to the secretoneurin-IR amacrine cells were from other amacrine cells, but they also received 21% of their input from bipolar cells. They directed most of their output, 54%, to amacrine cells, but there were many synapses onto bipolar cell axons and ganglion cell dendrites, as well. The synaptic connections were very similar in the three plexuses with one notable exception; output synapses to bipolar cells were significantly less common in the innermost one, where the S-ON bipolar cells terminate. Taken together, these findings suggest that the secretoneurin-IR amacrine cells in primates receive excitatory input from S-ON bipolar cells and, in turn, inhibit intrinsically photosensitive retinal ganglion cells.

Inferences about food location in three cercopithecine species: an insight into the socioecological cognition of primates.

Many animal species use a variety of cognitive strategies to locate food resources. One strategy is to make inferences by exclusion, i.e., perceiving the absence of reward as a cue that another location should be investigated. The use of such advanced cognitive strategies may be more prominent in species that are known to frequently solve social challenges, and inferential reasoning has mainly been investigated in social species such as corvids, dogs, dolphins and non-human primates. In this paper, we investigate how far social intricacy may explain the disparity of reasoning performances observed in three cercopithecine species that differ in the density of their social network and the diversity of their social partners. We used standard reasoning tasks, testing the volume concept and inference by exclusion using visual and auditory modalities. We showed that Old World monkeys can infer the location of invisible food by exclusion. In addition, Tonkean macaques and olive baboons had greater performances in most tasks compared to rhesus macaques. These responses are consistent with the social complexity displayed by these three species. We suggest that the cognitive strategies required to navigate through a demanding social world are involved in the understanding of the physical domain.

Frequency of feeding enrichment and response of laboratory nonhuman primates to unfamiliar people.

Although environmental enhancement plans for nonhuman primates vary between facilities, feeding enrichment represents a component of most programs. As part of a facility's feeding enrichment program, offering hand-fed food items by trained staff provides an opportunity for positive human interaction. We hypothesized that increased implementation of such enrichment would be associated with increased likelihood of a monkey accepting a hand-fed treat from a stranger. Several species of monkeys were tested at the Tulane National Primate Research Center. In 2002 and 2005, we recorded the number of caged monkeys that accepted a treat tablet from an unfamiliar person within 10 s. We compared the frequency of caretaker-implemented feeding enrichment documented for each animal room during the month proceeding data collection with the proportion of animals within the room that accepted the treat from the stranger. In 2002, 29.8% of the 500 subjects accepted the treat from the unfamiliar person. The proportion of animals that accepted the treat was significantly correlated with the number of days during which feeding enrichment had been implemented. In 2005, feeding enrichment frequency had increased by 76%, and 53.4% of the 676 subjects accepted the treat. These findings suggest that this simple form of enrichment may improve monkeys' responses to unfamiliar people, and that it holds promise as a method for mediating the stress imposed by human activity in animal rooms. In addition, a stranger's treat-feeding attempts may be a useful indicator of an institution's implementation of their environmental enrichment program.

The evolution of male-infant interactions in the tribe Papionini (Primates: Cercopithecidae).

In Old World monkeys, intense affiliative interactions between adult males and infants have mostly been observed in the tribe Papionini. Although these male-infant interactions have been reported in most species of the genera Papio, Theropithecus and Cercocebus, they have only erratically been reported in the genus Macaca. In this article I show that the distribution of male-infant interactions within the genus Macaca can be accounted for by the phylogenetic relations among macaque species and by the evolution of the genus Macaca relative to the other Papionini.