Moonstruck primates: owl monkeys (Aotus) need moonlight for nocturnal activity in their natural environment

Abstract

Primates show activity patterns ranging from nocturnality to diurnality, with a few species showing activity both during day and night. Among anthropoids (monkeys, apes and humans), nocturnality is only present in the Central and South American owl monkey genus Aotus. Unlike other tropical Aotus species, the Azara's owl monkeys (A. azarai) of the subtropics have switched their activity pattern from strict nocturnality to one that also includes regular diurnal activity. Harsher climate, food availability, and the lack of predators or diurnal competitors, have all been proposed as factors favoring evolutionary switches in primate activity patterns. However, the observational nature of most field studies has limited an understanding of the mechanisms responsible for this switch in activity patterns. The goal of our study was to evaluate the hypothesis that masking, namely the stimulatory and/or inhibitory/disinhibitory effects of environmental factors on synchronized circadian locomotor activity, is a key determinant of the unusual activity pattern of Azara's owl monkeys. We use continuous long-term (6-18 months) 5-min-binned activity records obtained with actimeter collars fitted to wild owl monkeys (n = 10 individuals) to show that this different pattern results from strong masking of activity by the inhibiting and enhancing effects of ambient luminance and temperature. Conclusive evidence for the direct masking effect of light is provided by data showing that locomotor activity was almost completely inhibited when moonlight was shadowed during three lunar eclipses. Temperature also negatively masked locomotor activity, and this masking was manifested even under optimal light conditions. Our results highlight the importance of the masking of circadian rhythmicity as a determinant of nocturnality in wild owl monkeys and suggest that the stimulatory effects of dim light in nocturnal primates may have been selected as an adaptive response to moonlight. Furthermore, our data indicate that changes in sensitivity to specific environmental stimuli may have been an essential key for evolutionary switches between diurnal and nocturnal habits in primates.

Figure 1. Locomotor activity patterns of two A. azarai males free-ranging in their natural environment.

A. Double plot of original activity recordings. Days are stacked vertically and black bars indicate the average locomotor activity during 15 min throughout each 24-h period. Black circles represent new-moon days. SS, summer solstice, WS, winter solstice. Arrows highlight representative mornings of lower activity following full-moon nights. B. Mean wave profiles of the daily activity of the same animals shown in (a). Each point represents the average locomotor activity taken for each 15-min interval throughout the recordings shown in (A). Bars represent standard errors of the mean.

Figure 2. Relationship between locomotor activity levels of A. azarai monkeys free-ranging in their natural habitat and luminance levels.

Intermediate light intensities positively mask (increase) locomotor activity in A. azarai. Each point represents the average normalized activity (± SE) of 9 animals for the range of luminances between one log-unit below and the luminance indicated in the x-axis (for instance, the point corresponding to 10⁻² lux includes the average activity recorded under luminances >10⁻³ and ≤10⁻² lux). Luminances corresponding approximately to full-moonlit nights, as well dawn and dusk are indicated. The curve represents a 3^rd degree equation best fitted to the points that generated each average shown.

Figure 3. Masking of nocturnal activity by lunar eclipses in wild owl monkeys of the Argentinean Chaco.

Activity patterns averaged across individuals for each of the three days when the total lunar eclipses occurred. Averages were calculated for the 2 h before the penumbra phase (left white bar with clock time for the onset of the 2-h window), for the 2-h after the end of the penumbra phase (right white bar with clock time for the offset of the 2-h window), as well as for the penumbra phase (light gray bars), the partial eclipse phase (dark gray bar) and the full eclipse (black bar). The averages represent the mean activity per 5-min interval for the specific phase, regardless of the phase duration. The date of each eclipse is indicated at the top of each graph and the number of recorded subjects is indicated between parentheses. The two hours prior to the eclipses from Nov 8, 2003 and Oct 27, 2004 occurred at times when brighter light intensity likely led to lower levels of activity.

Figure 4. Relationship between locomotor activity levels of A. azarai monkeys free-ranging in their natural habitat and ambient temperature.

Each point represents the average normalized activity (±SE) of 9 animals for the range of temperatures below the temperature marked in the x-axis. For instance, the point corresponding to 10°C includes the average activities measured between 5 and 10°C. The analysis includes recordings obtained only at optimal luminances for activity, between 10⁻¹ and 10³ lux (Figure 2).