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.

Cathemerality in a small, folivorous primate: proximate control of diel activity in Hapalemur meridionalis

“…Southern bamboo lemur activity was principally bimodal, exhibiting peaks around dawn and dusk. This is similar to what has been observed in other cathemeral primates (Aschoff et al 1982;Curtis et al 1999;Kappeler and Erkert 2003;Fernández-Duque 2003;Donati and Borgognini-Tarli 2006;Schwitzer et al 2007;Donati et al 2009Donati et al , 2013Fernández-Duque et al 2010). The lack of a tight dependence of these lemurs to annual variations in day length may also be explained by the presence of flexible visual structures that allow these animals to navigate from full daylight to night without major impairments, in contrast to strictly diurnal (Agetsuma and Nakagawa 1998;Hill et al 2003) or strictly nocturnal primates (Bearder et al 2006).…”

“…increasing nocturnal activity with increasing nocturnal luminosity (Horning and Trillmich 1999;Prugh and Golden 2014). Interestingly, however, many nocturnal primates display lunarphilia (Nash 1986(Nash , 2007Bearder et al 2001;Gursky 2003), a strategy especially common among cathemeral primates (Erkert 1974(Erkert , 1976Charles-Dominique et al 1980;Wright 1989;Colquhoun 1998;Curtis et al 1999;Donati et al 1999Donati et al , 2001Donati et al , 2009Donati et al , 2013Kappeler and Erkert 2003;Fernández-Duque 2003;Donati and Borgognini-Tarli 2006;Fernández-Duque and Erkert 2006;Schwitzer et al 2007;Fernández-Duque et al 2010). This phenomenon has been explained by primates' high reliance on visual cues, resulting in increased foraging efficiency and detection of potential predators (Gursky 2003;Bearder et al 2006).…”

Nocturnal ranging by a diurnal primate: are ring-tailed lemurs (Lemur catta) cathemeral?

“…There was often no travel during periods of night when the moon had not yet risen. This positive relationship between activity and moonlight has been frequently found among primates that are active at night (Colquhoun 1998;Donati et al 2001Donati et al , 2009Fernandez-Duque 2003;Gursky 2003;Kappeler and Erkert 2003;Donati and Borgognini-Tarli 2006;Fernandez-Duque et al 2010). The decline in luminance over time may have caused a concomitant decrease in night ranging across the deployment period.…”

Biogeography of time partitioning in mammals

“…The rotation of the Earth partitions time into regular cycles of day and night, and although all points on the Earth's surface receive roughly equal durations of light and darkness over the course of a year, at mid to high latitudes seasonal variation in day length imposes an uneven distribution throughout the annual cycle. During the hours when the sun is below the horizon, there is seasonal and latitudinal variation in the duration of "biologically useful semidarkness" in the form of twilight and moonlight (1), modified by both the lunar cycle and variable cloud cover, providing changing opportunities for animals able to use visual cues for key behaviors including foraging, predator avoidance, and reproduction (2)(3)(4)(5)(6). Activity during both daylight and semidarkness may be further constrained by covariance between the natural cycles of light and temperature; the metabolic costs of thermoregulation place constraints on the time available for activity (7).…”