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

Abstract

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])

Keywords:

• Activity rhythm
• Aotus
• Cathemeral
• Circadian rhythm
• Dual-oscillator model
• Entrainment
• Lunar periodicity
• Masking
• Natural environment
• Primates

ACKNOWLEDGMENTS

We are grateful to the Ministerio de la Producción, Subsecretaría de Ecología y Recursos Naturales and Dirección de Fauna from Formosa Province for authorizing the study and to the owners and manager of Estacia Guaycolec for their kind permission to carry the study out in their propriety. Many thanks also to our assistants for helping in all aspects of field work. Furthermore, we are deeply indebted to Horacio de la Iglesia for critically reading the manuscript and for his suggestions for improvement. E.F.D. received financial support from the National Science Foundation (BCS-0621020), the Zoological Society of San Diego, the CONICET of Argentina (PIP0051-98), and the Research Foundation of the University of Pennsylvania. Grants of the Deutsche Forschungsgemeinschaft to H.E. (SFB 307-C5) and technical support from the Institute for Zoology of the University of Tübingen, Germany, enabled the activity recordings in the field.

Declaration of Interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.