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.
Highlights
Primates show activity patterns that range from nocturnality to diurnality, with a few species showing activity both during the day and night [1,2,3,4]
Observational studies have shown that most species in the genus are nocturnal [5], but the Azara’s owl monkeys (A. azarai) of the subtropical Gran Chaco of Argentina and Paraguay have switched their activity pattern from strict nocturnality to one that includes regular diurnal activity [7]
Food availability, and the lack of predators or diurnal competitors, have all been proposed as possible ultimate environmental factors favoring evolutionary switches in the activity patterns of primates [1,6,8,9,10,11,12,13,14,15,16,17,18], and other mammals [19,20,21,22]
Summary
Primates show activity patterns that range from nocturnality to diurnality, with a few species showing activity both during the day and night [1,2,3,4]. Observational studies have shown that most species in the genus are nocturnal [5], but the Azara’s owl monkeys (A. azarai) of the subtropical Gran Chaco of Argentina and Paraguay have switched their activity pattern from strict nocturnality to one that includes regular diurnal activity [7]. The A. azarai population of northern Argentina [23,24] offers a unique opportunity to identify the environmental and biological factors that influence the distribution of activity across the 24-h day, which results in this species-specific cathemeral activity pattern [25]. The goal of our study was to evaluate the hypothesis that masking, namely the stimulatory and inhibitory effects of environmental factors on synchronized circadian locomotor activity [26,27], is a key proximate determinant of the unusual activity pattern of Azara’s owl monkeys
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