Moonstruck Primates: Owl Monkeys (Aotus) Need Moonlight for Nocturnal Activity in Their Natural Environment

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

Cathemerality and Lunar Periodicity of Activity Rhythms in Owl Monkeys of the Argentinian Chaco

Although most South American owl monkeys are mainly nocturnal, Aotus azarai azarai of the Argentinean Chaco regularly shows diurnal activity. In this study we examined the strong influence of moonlight on its diurnal and nocturnal activity, as well as the interaction of moonlight effects with other exogenous factors. We analyzed long-term automated activity recordings obtained with accelerometer collars from 7 owl monkeys during 2003 and 2004. Our data show marked lunar periodic and seasonal modulations of the owl monkeys’ activity pattern. On full moon days they were active throughout the whole night and displayed reduced activity during the day. With a new moon, activity decreased during the dark portion of the night, peaked during dawn and dusk and extended over the bright morning hours. Waxing and waning moons induced a significant increase in activity during the first and the second half of the night, respectively. During the cold winter months the monkeys displayed twice as much activity throughout the warmer bright part of the day than during the rest of the year. These findings indicate that A. a. azarai is mainly a dark-active species, but is still able to shift a considerable portion of activity into the bright part of the day if unfavourable lighting and/or temperature conditions prevail during the night.Fil: Fernandez Duque, Eduardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Centro de Ecología Aplicada del Litoral. Universidad Nacional del Nordeste. Centro de Ecología Aplicada del Litoral; ArgentinaFil: Erkert, Hans G.. Eberhard Karls Universität Tübingen.; Alemani

Seasonal Variation of Temporal Niche in Wild Owl Monkeys (Aotus azarai azarai) of the Argentinean Chaco: A Matter of Masking?

Among the more than 40 genera of anthropoid primates (monkeys, apes, and humans), only the South American owl monkeys, genus Aotus, are nocturnal. However, the southernmostly distributed species, Aotus azarai azarai, of the Gran Chaco may show considerable amounts of its 24-h activity during bright daylight. Due to seasonal changes in the duration of photophase and climatic parameters in their subtropical habitat, the timing and pattern of their daily activity are expected to show significant seasonal variation. By quantitative long-term activity recordings with Actiwatch AW4 accelerometer data logger devices of 10 wild owl monkeys inhabiting a gallery forest in Formosa, Argentina, the authors analyzed the seasonal variation in the temporal niche and activity pattern resulting from entrainment and masking of the circadian activity rhythm by seasonally and diurnally varying environmental factors. The owl monkeys always displayed a distinct bimodal activity pattern, with prominent activity bouts and peaks during dusk and dawn. Their activity rhythm showed distinct lunar and seasonal variations in the timing and daily pattern. During the summer, the monkeys showed predominantly crepuscular/nocturnal behavior, and a crepuscular/ cathemeral activity pattern with similar diurnal and nocturnal activity levels during the cold winter months. The peak times of the evening and morning activity bouts were more closely related to the times of sunset and sunrise, respectively, than activity-onset and -offset. Obviously, they were better circadian markers for the phase position of the entrained activity rhythm than activity-onset and -offset, which were subject to more masking effects of environmental and/or internal factors. Total daily activity was lowest during the two coldest lunar months, and almost twice as high during the warmest months. Nighttime (21:00-06:00 h) and daytime (09:00-18:00 h) activity varied significantly across the year, but in an opposite manner. Highest nighttime activity occurred in summer and maximal daytime activity during the cold winter months. Dusk and dawn activity, which together accounted for 43% of the total daily activity, barely changed. The monkeys tended to terminate their nightly activity period earlier on warm and rainy days, whereas the daily amount of activity showed no significant correlation either with temperature or precipitation. These data are consistent with the dual-oscillator hypothesis of circadian regulation. They suggest the seasonal variations of the timing and pattern of daily activity in wild owl monkeys of the Argentinean Chaco result from a specific interplay of light entrainment of circadian rhythmicity and strong masking effects of various endogenous and environmental factors. Since the phase position of the monkeys' evening and morning activity peaks did not vary considerably over the year, the seasonal change from a crepuscular/nocturnal activity pattern in summer to a more crepuscular/cathemeral one in winter does not depend on a corresponding phase shift of the entrained circadian rhythm, but mainly on masking effects. Thermoregulatory and energetic demands and constraints seem to play a crucial role. (Author correspondence: [email protected]

Relationship between locomotor activity levels of <i>A. azarai</i> monkeys free-ranging in their natural habitat and luminance levels.

<p>Intermediate light intensities positively mask (increase) locomotor activity in <i>A. azarai</i>. 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.</p

Locomotor activity patterns of two <i>A. azarai</i> males free-ranging in their natural environment.

<p><b>A.</b> 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>B.</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.</p