Lunar periodic modulation of the circadian activity rhythm in a wild North Colombian night monkey (Aotus griseimembra).

South American night monkeys (genus Aotus) are the only nocturnal simian primates. Early activity recordings in North Colombian A. griseimembra monkeys kept under semi-natural conditions and extensive chronobiological studies carried out in laboratory settings revealed a strictly nocturnal behavior and strong activity enhancing (disinhibiting) effects of moonlight or corresponding luminosities during the dark time. To check whether the results from captive individuals correspond to the behavior of wild monkeys, we carried out long-term activity recordings of a wild female A. griseimembra in a tropical rainforest near San Juan de Carare, Northern Colombia. Our data from about 150 days of continuous activity records with an "Actiwatch Mini" (CamNtech, UK) accelerometer-data logger device, confirmed: (1) strictly nocturnal behavior, (2) a pronounced bimodal activity pattern with prominent peaks during dusk and dawn, and (3) a lunar periodic modulation (masking) of the night monkey's circadian activity rhythm due to distinct activity inhibiting effects of the absence of moonlight throughout the night. The results from this wild-living tropical night monkey are consistent with those from captive conspecifics studied decades earlier.

Diel and infradian (7-day) activity rhythms in Mexican spider monkeys (Ateles geoffroyi) kept with and without visitor contact.

Diel activity rhythms in mammals are regulated by an endogenous (circadian) timing system which is synchronized by environmental 24-hr periodicities called zeitgebers. Additional direct responses to stochastic environmental factors ensure the fine-tuning to the actual situation and may mask the circadian time course. Following an observational study on behavioral effects of visitor activities in a group of spider monkeys (Ateles geoffroyi) kept free-ranging on a small island of Lake Catemaco, Veracruz, Mexico, we analyzed the effect of weekly varying numbers of visiting tourist boats on the monkeys' diel activity rhythm. With small accelerometer-data logger devices we recorded the monkeys' locomotor activity continuously for several months each. Then we compared the data with those from spider monkeys living without tourist contact. Neither the duration of the monkeys' activity time (α) nor its phase relationship to the 24-hr solar day did change on different weekdays in either site. However, their activity level showed a clear 7-day rhythm. The monkeys of the tourist site showed highest activity on Saturday and Sunday, when the frequency of visiting tourist boats was highest, whereas those of the non-tourist site were least active on Sunday and Monday, when human activities were lowest there. While the monkeys of the non-tourist site usually displayed a distinct bimodal activity pattern peaking in the morning and late afternoon, the pattern in those of the tourist site mostly lacked a morning peak and varied more over time. Based on our results, we suggest that circadian entrainment is not involved in the differences between the diel activity rhythms of the spider monkeys from the two keeping sites and the differing 7-day variation in their activity level. Rather, these differences seemingly reflect direct responses to the differing human activities and thus may correspond to circadian masking effects.

Effects of housing conditions and season on the activity rhythm of spider monkeys (Ateles geoffroyi) kept under natural conditions within their distributional range in Central Mexico.

The timing and pattern of mammalian behavioral activities are regulated by an evolutionary optimized interplay of the genetically based biological (circadian) clock located in the brain's suprachiasmatic nuclei and direct responses to environmental factors that superimpose and thus mask the clock-mediated effects, the most important of which is the photically induced phase-setting (synchronization) of the circadian rhythmicity to the 24-hour solar day. In wild and captive animals living under the natural conditions prevailing in their habitat, to date, only a few attempts have been made to analyze the role of these two regulatory mechanisms in the species' adaptation to the time structure prevailing in their habitat. We studied the impact of housing conditions and season on the daily timing and pattern of activity in Mexican spider monkeys (Ateles geoffroyi). To this end, we carried out long-term activity recordings with Actiwatch® AW4 accelerometer/data-logger devices in 11 adult Ateles living under identical natural lighting and climatic conditions in either a large wire netting cage or a 0.25 ha forest enclosure in the primatological field station of Veracruz State University near Catemaco, Mexico. In a gravid female in the forest enclosure, we obtained first-hand information on the effect of late pregnancy and parturition on the monkey's activity rhythm. The Ateles behaved strictly diurnal and undertook about 90% of daily total activity during this activity time. Due to a higher second activity peak in late afternoon, the bimodal activity pattern was more pronounced in monkeys living in the forest enclosure. Although the spider monkeys kept there had an earlier activity onset and morning activity peak than their conspecifics in the cage, no consistent differences were found in the parameters characterizing the phase-setting of the circadian system to the environmental 24-h periodicity, either by comparison or correlation with the external time markers of sunrise (SR) and sunset (SS). The most obvious effect of late pregnancy, parturition and lactation was a distinct reduction of the activity level during the week of parturition and the next. Seasonal variations in the form of significant differences between the long-day summer half year and the short-day winter half year were established in the phase-angle differences of the morning activity peak to SR, in the evening activity peak and activity offset to SS, as well as in the activity time and the peak-to-peak interval, but not in the phase position of activity onset to SR or in the height of the morning and evening activity peak. These findings in combination with a high variability of the phase angle differences indicate that in A. geoffroyi, a relatively weak circadian component and strong masking direct effects of environmental factors are involved in the regulation of the daily activity rhythm.

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.

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.

Photic entrainment and masking of prosimian circadian rhythms (Otolemur garnettii, Primates).

Besides rods the retina of the nocturnal greater bushbaby, genus Otolemur, also contains small cones which, however, do not allow color vision. In order to find out whether these cones might be involved in circadian photoreception in the Garnet's galago Otolemur garnettii we determined the threshold for photic entrainment. Activity recordings revealed a short circadian period of 22.6+/-0.7 h subjected to pronounced long-lasting aftereffects. The animals had a relatively high threshold for photic entrainment at about 3-30 lux. This indicates that the cones and/or other, as yet unidentified photoreceptive retinal cells may be involved in circadian photoreception. The galagos' threshold for photic entrainment also depended on the luminosity during the dark phase of the light dark cycles. Results furthermore showed that in Otolemur aftereffects may play a crucial role for circadian entrainment. Light time luminosities just below the individuals' threshold for photic entrainment strongly inhibited the galagos' locomotor activity and, thus, produced pronounced negative masking effects on their free-running circadian activity rhythm. From this it may be inferred that masking direct effects of light are not induced or mediated via the circadian system, i.e. via the circadian pacemaker in the hypothalamic suprachiasmatic nuclei, but at a higher central nervous integrational stage.

Chronobiological background to cathemerality: circadian rhythms in Eulemur fulvus albifrons (Prosimii) and Aotus azarai boliviensis (Anthropoidea).

Cathemeral activity, in which the animals' motor activity is almost evenly distributed throughout the dark and the light portion of the day, has been described in various lemur genera (Eulemur, Hapalemur) and in the owl monkey Aotus azarai of the Argentinean Chaco. Proximate and ultimate factors responsible for this behaviour are still being debated. However, the chronobiological background of the behaviour has largely been ignored. We studied E. fulvus albifrons and A. a. boliviensis under controlled laboratory conditions to assess whether their activity rhythm is endogenously regulated by a circadian timing system that obeys general rules found in other mammals, or whether there are characteristic differences. To this end, we carried out long-term activity recordings on individuals of both subspecies kept under constant light and various light-dark cycles (LDs) using a PC-controlled electro-acoustic device in combination with telemetric body temperature measurements. Both subspecies developed free-running circadian activity and body temperature rhythms with periods deviating from 24 h in constant light, and LDs turned out to be the most efficient Zeitgeber synchronizing this endogenous rhythmicity to the external 24-hour day. The luminosity prevailing during the dark time of the LD had a decisive effect on levels of activity in the lemurs and induced strong masking effects on their circadian activity pattern. The results indicate that, from a chronobiological viewpoint, both species should be considered as dark active primates. Their diel activity rhythm is regulated by a normally responding circadian timing system and strong activity inhibiting or enhancing direct effects of light intensity. Thus, hypotheses on proximate and/or ultimate factors of cathemerality in primates must also consider its circadian background.

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.

Astronomical and meteorological parameters and rest-activity rhythm in the spider monkey Ateles geoffroyi.

UNLABELLED: All animals including primates show regular variations in their behavioural activities and physiological functions. In numerous species diel, ultradian, infradian, annual and/or lunar rhythms have been established; however, the use of the focal sampling method does not provide information on hour-to-hour nor day-to-day variations. In behavioural field studies dealing with primate activity rhythms and their modulation by environmental variables the possible dual, synchronizing and/or masking effect of these variables is often ignored. In the present study, we analyze the relation between astronomical and meteorological parameters and various parameters of the rest-activity rhythm in Ateles geoffroyi, a species scarcely investigated with respect to biological rhythms. These Ateles were kept under semi-natural conditions, exposed to natural light, temperature and humidity cycles, and sky state. Motor activity was recorded with actiwatch accelerometers during 180 days (5-min intervals), starting from the autumn equinox. RESULTS: Ateles is active throughout the day, rests during the night and presents bimodal activity. Activity time, onset and end of activity as well as the times of their two activity peaks were significantly correlated with duration of the solar day and sunrise or sunset time. The behavioural parameters also correlated with ambient temperature. Climate factors and sky-state significantly influenced the duration and times of onset and end of activity. Our findings identified a clear modulation of the rest-activity pattern by astronomical variables serving as Zeitgebers, such as the natural light-dark cycle, and by masking effects of meteorological factors (temperature, weather and cloudiness), as well as of artificial variables introduced by the interaction with man.

Actualización por temas. Moon cycle effects on humans: myth or reality?

Durante siglos se ha mantenido la creencia popular de que el ciclo lunar influye en los factores fisiológicos y conductuales de los seres humanos. Esta idea podría explicarse por la cronobiología, pues esta perspectiva sugiere que los patrones conductuales de los organismos son el resultado de la interacción entre el programa temporal endógeno, que genera los ritmos biológicos, y las modificaciones causadas por los estímulos externos, como los ambientales y los sociales. Sin embargo tales interacciones pueden ser enmascaradas por efectos no naturales, como la luz eléctrica y los ruidos de la ciudad, entre otros. Diversas investigaciones han buscado la relación causal entre el ciclo lunar y los factores fisiológicos: las admisiones a los hospitales psiquiátricos, los traumas mentales, la conducta anormal, la actividad criminal, los intentos de homicidio y el suicidio, etc. No obstante los estudios han tenido un carácter epidemiológico, con extensas muestras poblacionales, y han obtenido resultados contradictorios debido, principalmente, a la manipulación estadística de los datos. Las relaciones entre el ciclo lunar y el periodo de sueño-vigilia de los seres humanos ha sido poco estudiado y no ofrece resultados convincentes. Por otro lado, los estudios sistematicos en los que se han usado métodos robustos, en los animales han proporcionado fuertes evidencias acerca de la alteración de los ritmos de reposo-actividad, en relación con las fases del ciclo lunar. Proponemos que se hagan estudios comparados en los seres humanos, con métodos confiables de registro y de observación sistemática que aporten datos más objetivos, capaces de distinguir los factores que probablemente estén enmascarando los efectos del ciclo lunar en la vida humana.

Characteristics of the circadian activity rhythm in common marmosets (Callithrix j. jacchus).

The circadian activity rhythm of the common marmoset, Callithrix j. jacchus was investigated by long-term recording of the locomotor activity of 15 individuals (5 males, 10 females) from 1.5 to 8 years old, both under constant illumination and under LD 12:12. The mean period of the spontaneous circadian rhythm was 23.2 ± 0.3 h. Neither sex-specific differences nor a systematic influence of light intensity on the spontaneous period were observed, but the period was dependent on the duration of the trial and on the age of the individual. Due to the short spontaneous period, in LD 12:12 there was a distinct advance of the activity phase with respect to the light time and a masking of the true onset of activity by the inhibitory direct effect of low light intensity during the dark time. After an 8 h delay shift of the LD 12:12, re-entrainment of the circadian activity rhythm required an average of 6.8 ± 0.7 days; the average re-entrainment time after an 8 h phase advance of the LD cycle was 8.6 ± 1.3 day. This directional effect is ascribed to characteristics of the phase-response curve. No ultradian components were observed, either in the LD-entrained or the free-running circadian activity rhythm.

Evidence for ecological adaptation of circadian systems : Circadian activity rhythms of neo-tropical bats and their re-entrainment after phase shifts of the Zeitgeber-LD.

Comparative studies on the circadian activity rhythm of five neotropical bat species show, that even exclusively tropical Chiroptera yield considerable differences with respect to their light-induced variation of the period length and the time needed for re-entrainment after phase shifts of the Zeitgeber-LD (Figs. 2 and 3). Species with a wide variation range of the period length resynchronize very fast and vice versa. Both reactions suggest the circadian system to have a higher plasticity or a higher sensibility for the exogenous components respectively. The sensibility for these exogenous components is, according to the hitherto results, in general higher within insectivorous Chiroptera species than within frugivorous/nectarivorous to omnivorous species. It is discussed, whether this can be interpreted as a specific adaptation to the demands of a predatory way of life.

Sunset-related timing of flight activity in neotropical bats.

The times of onset and completion of the hunting flights of three colonies of neotropical bats, each comprising 100-200 individuals, were observed for nine months. The colonies were of different species: Molossus ater (M.a.) and Molossus molossus (M.m.) of the Molossidae, and Myotis nigricans (My. n.) of the Vespertilionidae. Individuals of Phyllostomus hastatus (P.h., Phyllostomidae) were also observed. All the bats roosted in a building near Restrepo, Colombia (4°16'N, 73°34'W). Times of emergence in the evening and the return of the last animals in the morning were recorded on 2 to 3 successive days each month. For all bats, the emergence time changed in parallel with that of sunset, and the return paralleled sunrise (Fig. 1). Accordingly, the duration of the activity period is positively correlated with the duration of the night. No annual periodic changes in phase (re sunset/sunrise) of the onset and end of flight activity could be demonstrated, but there was a close relationship between the timing of activity and particular light intensities during twilight (Fig. 4). The first flyers of M.a. appear at the highest intensity (30-300 lx) and those of My. n. at the lowest (0.1-5 lx); the last flyers to return appear in the opposite sequence. For each species, the return to the roost usually occurs at a lower intensity than the departure. These findings, made with four neotropical bat species, differ from those of Subbaraj and Chandrashekaran (1977) with the emballonurid bat Taphozous that they studied at 9°58' N in India. The ecological factors that may play a role in timing the flight activity of tropical bats are discussed. "Sunset-related timing", based on the combined effect of (a) the circadian oscillation in "arousal" and (b) the transition during twilight to a light-intensity range with reduced inhibition of activity (lightsampling behavior), tends to be the rule in tropical bats; "time-of-day-related timing" is the exception.