Effects of housing conditions and season on the activity rhythm of spider monkeys (Ateles geoffroyi) kept under natural conditions within their distributional range in Central Mexico

Abstract

The timing and pattern of mammalian behavioral activities are regulated by an evolutionary optimized interplay of the genetically based biological (circadian) clock located in the brain's suprachiasmatic nuclei and direct responses to environmental factors that superimpose and thus mask the clock-mediated effects, the most important of which is the photically induced phase-setting (synchronization) of the circadian rhythmicity to the 24-hour solar day. In wild and captive animals living under the natural conditions prevailing in their habitat, to date, only a few attempts have been made to analyze the role of these two regulatory mechanisms in the species' adaptation to the time structure prevailing in their habitat. We studied the impact of housing conditions and season on the daily timing and pattern of activity in Mexican spider monkeys (Ateles geoffroyi). To this end, we carried out long-term activity recordings with Actiwatch® AW4 accelerometer/data-logger devices in 11 adult Ateles living under identical natural lighting and climatic conditions in either a large wire netting cage or a 0.25 ha forest enclosure in the primatological field station of Veracruz State University near Catemaco, Mexico. In a gravid female in the forest enclosure, we obtained first-hand information on the effect of late pregnancy and parturition on the monkey's activity rhythm. The Ateles behaved strictly diurnal and undertook about 90% of daily total activity during this activity time. Due to a higher second activity peak in late afternoon, the bimodal activity pattern was more pronounced in monkeys living in the forest enclosure. Although the spider monkeys kept there had an earlier activity onset and morning activity peak than their conspecifics in the cage, no consistent differences were found in the parameters characterizing the phase-setting of the circadian system to the environmental 24-h periodicity, either by comparison or correlation with the external time markers of sunrise (SR) and sunset (SS). The most obvious effect of late pregnancy, parturition and lactation was a distinct reduction of the activity level during the week of parturition and the next. Seasonal variations in the form of significant differences between the long-day summer half year and the short-day winter half year were established in the phase-angle differences of the morning activity peak to SR, in the evening activity peak and activity offset to SS, as well as in the activity time and the peak-to-peak interval, but not in the phase position of activity onset to SR or in the height of the morning and evening activity peak. These findings in combination with a high variability of the phase angle differences indicate that in A. geoffroyi, a relatively weak circadian component and strong masking direct effects of environmental factors are involved in the regulation of the daily activity rhythm.

Visitor effect on the behavior of a group of spider monkeys (Ateles geoffroyi) maintained at an island in Lake Catemaco, Veracruz/Mexico

“…We placed the devices in tiny waterproof metal boxes attached to collars and then attached them to the monkeys' necks. The collar does not cause any type of interference with the individuals' daily activity (Muñoz‐Delgado, Corsi‐Cabrera, Canales‐Espinosa, Santillán‐Doherty, & Erkert, ; Muñoz‐Delgado et al, ; Muñoz‐Delgado, Sánchez‐Ferrer, Pérez‐Galicia, Canales‐Espinosa, & Erkert, ). After this recording period, the collars were removed and the data was downloaded using an Actiwatch Reader (Mini Mitter, Bend, OR) and the Actiware Software (Cambridge Neurotechnology Ltd.).…”

Diel and infradian (7‐day) activity rhythms in Mexican spider monkeys (Ateles geoffroyi) kept with and without visitor contact

“…that the activity rhythm shown by the monkeys of the tourist site would differ from that of the monkeys from the non‐tourist site. The spider monkeys kept in a forest enclosure, which is situated in a remote part of the Pipiapan Primate Centre, usually showed clear bimodal diel activity patterns (Muñoz‐Delgado et al, ) that correspond to the pattern reported for wild‐living animals (Gonzáles‐Zamora et al, ). By contrast, the more often disturbed monkeys kept in a large wire‐mesh cage, located in the more frequently visited (by caretakers, scientists, and students) entrance area of this study site, showed deviating activity patterns (Muñoz‐Delgado et al, ).…”

“…The daily activity‐rest rhythm of the strictly diurnal neotropical spider monkey ( Ateles geoffroyi ) has also been shown to be based on a circadian rhythm (Muñoz‐Delgado et al, ) and masking effects of various astronomical and meteorological parameters (Muñoz‐Delgado, Corsi‐Cabrera, Canales‐Espinoza, Santillan‐Doherty, & Erkert, ). In individuals kept under semi‐natural environmental conditions in Central Mexico, the onset and end of daily activity time are highly correlated with the times of sunrise and sunset, respectively (Muñoz‐Delgado et al, , ). This suggests a stable phase setting of the monkeys’ circadian rhythm to the natural LD cycle and, thus, the function of the LD cycle as a main zeitgeber for the activity rhythm regulating central clock of their circadian system (Helm et al, ; van der Veen et al, ).…”

“…This suggests a stable phase setting of the monkeys’ circadian rhythm to the natural LD cycle and, thus, the function of the LD cycle as a main zeitgeber for the activity rhythm regulating central clock of their circadian system (Helm et al, ; van der Veen et al, ). Significant correlations of the animals’ activity level with several more stochastically varying meteorological parameters suggest additional masking effects (Muñoz‐Delgado et al, , ).…”

“…To evaluate this idea, we carried out quantitative long‐term activity recordings in seven females of the spider monkey group kept on this island from 2012 to 2016. To test whether or not the weekly variations found in the island monkeys’ activity rhythm may have been a response to the local visitors' activities, we compared these recordings with data from previous long‐term activity records from spider monkeys that lived, without tourist contact, approximately 10 km from the island in an electric‐fenced forest patch (enclosure) of equal size at the Pipiapan Primate Centre of the Universidad Veracruzana (Muñoz‐Delgado, Sánchez‐Ferrer, Pérez‐Galicia, Canales‐Espinosa, & Erkert, ).…”