Diurnality and nocturnality in nonhuman primates: comparative chronobiological studies in laboratory and nature

Looking for differences in circadian clock characteristics of diurnal and nocturnal nonhuman primates, this article summarizes results of chronobiological studies carried out in various nocturnal, diurnal, and cathemeral prosimian and anthropoid primate species under controlled laboratory conditions, under seminatural conditions, and in the wild. In almost all circadian parameters investigated, no differences were discernible between the two main chrono-ecotypes, either in circadian period length and the influence upon it of after-effects, of light intensity, and ambient temperature, or in the PRC, re-entrainment behavior, rhythm splitting, and internal desynchronization. Diurnal and nocturnal or cathemeral species differed only in the phase of artificial or natural LDs to which their circadian activity phase was adjusted as well as in the characteristics of masking activity upon the rhythms produced by the direct inhibiting or enhancing effects of light. Pronounced lunar periodicity—observed in the activity rhythm of nocturnal neotropical owl monkeys, genus Aotus, in seminatural and natural environments as well as in wild cathemeral Malagasy lemurs, genus Eulemur—is shown to result from masking effects of moonlight. In captive Eulemur fulvus albifrons, a change from dark-active over cathemeral to light-active behavior, without concurrently changing the circadian phase-setting of activity to D, was produced by direct masking effects of a stepwise reduction of darktime luminosity on an LD 12:12 cycle. Long-term activity recordings carried out in wild diurnal Malagasy sifakas (Propithecus verreauxi) and cathemeral redfronted lemurs (Eulemur fulvus rufus), as well as in wild nocturnal owl monkeys (Aotus a. azarai) of the North Argentinean Chaco, yielded in all species distinct bimodal long- and short-day activity patterns with pronounced peaks during dusk and dawn. Applying Pittendrigh's two-oscillator concept to these results, it is hypothesized that the differences in chrono-ecotype behavior may result from variations in internal coupling and external phase-setting of morning and evening oscillators (m, e) to dawn and dusk, interacting with direct masking effects of light.

Keywords:

• circadian rhythms
• activity patterns
• photic and nonphotic entrainment
• phase-response
• light masking
• lunar periodicity
• cathemerality
• prosimian and anthropoid primates

Acknowledgements

I am very grateful to my colleagues Drs. Peter Kappeler (German Primate Center), Eduardo Fernandez-Duque (Fundación Eco, Argentina), Jairo Muñoz-Delgado (Instituto Mexicano de Psiquiatría, Mexico), and Domingo Canales (Universidad Veracruzana, Mexico) for quite a pleasant and highly productive cooperation in carrying out long-term activity recordings in wild lemurs and owl monkeys, as well as in spider monkeys kept under seminatural conditions. Many thanks also to Angelika Scheideler (Maximilian University, Munich) for her help with the statistics and diagram production. Furthermore, I would like to thank Drs. Jim Waterhouse and Roberto Refinetti for their invitation to contribute to this special issue of Biological Rhythm Research and for kindly reviewing and improving the manuscript. Last but not least, I'm very much obliged to all my students for their highly appreciated contributions to our comparative approach in primate chronobiology. All studies were supported by grants from the Deutsche Forschungsgemeinschaft.