Internal desynchronization of the circadian activity and feeding rhythm in an owl monkey (Aotus lemurinus griseimembra): a case study

In the free-running circadian locomotor activity rhythm of a 7-year-old male owl monkey (Aotus lemurinus griseimembra) kept under constant light and climatic conditions (LL 0.2 lux, 25°C ± 1°C, 60 ± 5% relative humidity [RH]), a second rhythm component developed that showed strong relative coordination with the free-running activity rhythm of 24.4h and a 24h rhythm. The simultaneously recorded feeding activity rhythm strongly resembled this rhythm component. Therefore, it seems justified to infer that there was an internal desynchronization between the two behavioral rhythms or their circadian pacemakers, that is, between the light-entrainable oscillator located in the suprachiasmatic nuclei (SCN) and a food-entrainable oscillator located outside the SCN. This internal desynchronization may have been induced and/or maintained by a zeitgeber effect of the (irregular) 24h feeding schedule on the food-entrainable oscillator. The weak relative coordination shown by the activity rhythm indicates a much weaker coupling of the light-entrainable oscillator to the food-entrainable oscillator than vice versa. (Chronobiology International, 17(2), 147-153, 2000)     

Thermal biology,torpor and behaviour in sugar gliders: a laboratory-field comparison

Most studies on animal physiology and behaviour are conducted in captivity without verification that data are representative of free-ranging animals. We provide the first quantitative comparison of daily torpor, thermal biology and activity patterns, conducted on two groups of sugar gliders (Petaurus breviceps, Marsupialia) exposed to similar thermal conditions, one in captivity and the other in the field. Our study shows that activity in captive gliders in an outdoor aviary is restricted to the night and largely unaffected by weather, whereas free-ranging gliders omit foraging on cold/wet nights and may also forage in the afternoon. Torpor occurrence in gliders was significantly lower in captivity (8.4% after food deprivation; 1.1% for all observations) than in the field (25.9%), mean torpor bout duration was shorter in captivity (6.9 h) than in the field (13.1 h), and mean body temperatures during torpor were higher in captivity (25.3°C) than in the field (19.6°C). Moreover, normothermic body temperature as a function of air temperature differed between captive and free-ranging gliders, with a >3°C difference at low air temperatures. Our comparison shows that activity patterns, thermal physiology, use of torpor and patterns of torpor may differ substantially between the laboratory and field, and provides further evidence that functional and behavioural data on captive individuals may not necessarily be representative of those living in the wild.     

Influence of different light intensities on the daily grooming distribution of common marmosets Callithrix jacchus

The daily distribution of autogrooming was evaluated in adult marmosets submitted to different illumination intensities in the light phase of the light-dark cycle. Autogrooming and locomotor activity were monitored and the faecal cortisol level assessed as a stress indicator. The distribution of autogrooming showed two distinct tendencies: when the light intensity varied from 500 to 200 lux, a slight increase in frequency and duration was observed, while a significant decrease in both variables occurred at 10 lux. Varying light intensities did not inhibit rhythm synchronization. The daily profile of autogrooming was mainly unimodal with an acrophase in the first half of the light phase. Faecal cortisol levels tended to increase in animals submitted to 100 and 10 lux, but these results are not conclusive. We suggest keeping captive marmosets in light intensities of at least 200 lux in the light phase, allowing animals to maintain autogrooming levels in order to reduce the discomfort caused by captivity and isolation.     

Circadian Rhythms and time Measurement in Locomotor Activity of the Scorpion Leiurus Quinquestriatus (Buthidae)

The circadian rhythms of locomotor activity of the scorpion Leiurus quinqueslriatus were examined under different light-dark cycles and in free-running conditions. The circadian rhythm is bimodal in LD 12:12 with alternating cycles of temperature (35°-25°C) with high intensity (1300 lux) or in LD 12: 12 with constant temperature 35° C with 300 lux. In LD 12:12 (1300 lux), in long or in short light spans with constant temperature, the bimodal pattern is slightly changed with the appearance of a third minor peak of activity. In free-running conditions, the bimodal rhythm of locomotor activity persists in DD with T about 24 hr, but in LL the rhythm becomes unimodal with T about 24 hr. Cosinor and power spectrum analysis showed the presence of more than one periodic component. It seems that there is a correlation between the range of light regimens, temperature, light intensity and the coincidence of these components. These components are independently entrained by the environmental light cycle. The mechanism of entrainment of components is discussed.     

Annual Variation in an Ultradian Component in the Locomotor Activity Rhythm of the Common Marmoset (Callithrix jacchus)

Daily locomotor activity in common marmosets shows a decrease near the middle of the active phase, as observed for captive and wild living animals. An important 8 h period component detected in spectral analysis shows annual variation. To determine the environmental factors that are correlated with this finding, three animals were observed during infant and juvenile stages in outdoor cages under natural temperature, humidity and light cycles. Data were collected from sunrise to sunset, three consecutive days a week, at 5 min intervals randomly distributed inside the clock hours, and were recorded as the total of arbitrary cage sections traveled by the animal each interval. From the Fourier analysis of weekly data series we calculated the relative power of the 8 h period component. Pearson's correlation test showed that the relative power correlates better with environmental temperature and photophase duration than with relative humidity or rainfall. Amplitude but not acrophase showed significant differences (Kruskall-Wallis test, p <0.01) between seasons. These findings suggest that the annual variation in the 8 h period component could result from a temperature modulation on the locomotor activity rhythm.     

Stress-induced adrenal changes and their relation to reproductive failure in captive nine-banded armadillos (Dasypus novemcinctus)

Histological features of adrenal glands from captive and unstressed free-ranging nine-banded armadillos were compared to determine if undefined stress factors associated with captivity were capable of causing changes in adrenal morphology. Animals in captivity less than 3 mo showed histological features identical to unstressed free-ranging animals. Animals in captivity 6 mo or longer, however, showed adrenal changes like those previously described in other mammals exposed to various types of stress, except that there was no accompanying increase in adrenal weight. Similar adrenal changes were found in free-ranging animals exposed to extremely harsh winter weather. Females from both the chronic captive population and this stressed free-ranging population were seen to suffer reproductive failure. Reproductive function in males was not affected. There was no detectable sex difference in gross or histological adrenal changes; however, previous reports indicate there is a sex difference in the secretory product from the adrenals of captive nine-banded armadillos. A possible relationship between reproductive failure in the female and the sex difference in adrenal secretory products is discussed.     

Effect of ambient temperature on the circadian activity rhythm in common marmosets, Callithrix j. jacchus (primates)

Whereas the (zeitgeber) effect of ambient temperature T_a and temperature cycles TaC's on circadian rhythmicity has been well documented for heterofhermic mammals, inconsistent results have been obtained for strictly homeothermic species. Hence, it might be inferred that the susceptibility of the mammalian circadian timing system (CTS) to Ta and TaC's depends on the range of the animals' core and/or brain temperature rhythm. This hypothesis was tested in the common marmoset (Callithrix j. jacchus, n=12), a small diurnal primate with an amplitude in body temperature rhythm that is larger than for other homeothermic primates studied so far. Within the range 20-30°C, no systematic effects of constant Ta on most parameters of the marmosets' light-dark (LD)-entrained and free-running circadian activity rhythm (CAR) were found. Significant differences could be established in the average amount of activity per circadian cycle. It was highest at Ta 25°C (LD) and 20°C (light-light, LL) and most probably reflected a temperature-induced masking effect. A 24h trapezoidal TaC of 20:30°C entrained the free-running CAR in two of six marmosets and produced relative coordination in all others. Accordingly, in all animals tested, it had an effect on the CTS. In marmosets free running in LL at a Ta of 20°C or 30°C, 3h warm and cold pulses of 30°C and 20°C, respectively, produced neither systematic phase responses nor period responses of the CAR. So, there is no evidence of a phase-response mechanism underlying circadian entrainment. The results show that large-amplitude TaC's function as a weak zeitgeber for the marmosets' CTS. Since this zeitgeber effect is significantly larger than that found in owl monkeys, the results are consistent with the starting hypothesis that the zeitgeber effect of a given T,C on the mammalian CTS may be related to the amplitude of the species' core and/or brain temperature cycle.     

Tooth wear in captive wild ruminant species differs from that of free-ranging conspecifics

The mesowear method evaluates the wear patterns of herbivore cheek teeth by visually evaluating the facet development of the occlusal surfaces. It thus allows classification of most herbivorous ungulates into browsers, grazers or intermediate feeders, due to the fact that in grazers, tooth wear is characterized by a comparatively high degree of abrasion, most probably due to the presence of silicacious phytoliths in grasses, a higher amount of dust and grit adhering to their forage, or both. It has been suggested that excessive tooth wear could be a particularly limiting factor in the husbandry of captive large browsing species, and major tooth wear was demonstrated in captive as compared to free-ranging giraffe. If this increased tooth wear in captivity was an effect of feeding type and diets fed, then it would be expected that other browsing species are affected in a similar manner. In order to test this hypothesis, we investigated the dental mesowear pattern in captive individuals of 19 ruminant species and compared the results to data on free-ranging animals. Compared to free-ranging populations, captive browsers show a significantly more abrasion-dominated tooth wear signal. The reverse applies to captive grazers, which tend to show a less abrasion-dominated wear in captivity. Captive ruminants were generally more homogenous in their wear signature than free-ranging ruminants. If grit contamination in the natural habitat is a major cause of dental wear in grazers, then diets in captivity, although similar in botanical composition, most likely contain less abrasives due to feeding hygiene. If dental wear is one of the major factors limiting longevity, then captive grazers should achieve longer lifespans than both captive browsers and free-ranging grazers. In particular with respect to browsers, the results suggest that captive feeding regimes could be improved.     

Behavioral and hormonal response of common marmosets, <Emphasis Type="Italic">Callithrix jacchus</Emphasis>, to two environmental conditions

Captive animals of several species change their behavioral pattern and hormonal profile in response to physical (for example, cage size and temperature) and social (for example, group size and social isolation) modification of their environment. To evaluate the effect of environmental change in captivity, the affiliative (contact/proximity and allogrooming) and individual (approach, leaving, scent mark, locomotion, and autogrooming) behavior of five family groups of common marmosets, Callithrix jacchus, were recorded on weekdays (non-quiet) and at the weekend (quiet) for two months. In addition, fecal samples were collected for four of these groups to measure their cortisol levels under both conditions. The behavioral pattern and hormonal profile of breeding pairs and their offspring were modified by different management routines used in the experimental conditions. We found that the animals spent more time in affiliative interactions at the weekend, whereas on weekdays, they showed more individual behaviors. Moreover, cortisol levels of breeding pairs and their offspring were higher on weekdays, suggesting that common marmosets living in captivity react to environmental modification by changing their behavioral and hormonal pattern.     

Body Weight of Wild and Captive Common Marmosets (Callithrix jacchus)

Captive studies and occasional trappings of wild individuals indicate that callitrichids have small size and body weight and lack sexual dimorphism. We compared body weights of captive and wild Callithrix jacchus obtained by repeatedly weighing subjects from two populations in Brazil. We obtained captive data by routinely weighing 138 individuals from the Universidade Federal do Rio Grande do Norte colony and wild data via regular trapping of 243 individuals in 15 free-ranging groups from IBAMA's field site in Nísia Floresta. We assigned all subjects to one of four age classes—infant, juvenile, subadult, and adult—according to their birth dates or size, reproductive status, and dental development. There is no significant difference between males and females in any of the four age classes, but captive subjects were heavier than wild ones in all age classes but infant. Reproductive and nonreproductive adult females showed no statistical difference in weight. These results accord with previous reports of lack of body size sexual dimorphism in common marmosets and suggest that differences between wild and captive common marmosets are not constitutional, but are instead a consequence of diet and physical activity. The absence of weight difference between reproductive and nonreproductive females suggests that any possible advantage from high rank is outweighed by the costs of reproduction in common marmosets.     

Circadian and Ultradian Periodicities of Grooming Behavior in Family Groups of Common Marmosets (Callithrix jacchus) in Captivity

Three families' groups of common marmosets were observed to describe the characteristics of their grooming rhythmicity, as the duration of the episodes of self- and social grooming made and received by the animals, in captivity under natural environmental conditions. Data were collected by focal animal sampling, at 20 min hourly intervals during 16 non-consecutive days, from January to March in 1994 (sunrise: 05:24 h ± 2 min; sunset: 17:34 h ± 1 min). Time series were obtained for each individual and for each family through hourly duration of grooming. Family time serie was obtained through the mean of its individuals time series. Spectral analysis revealed statistically significant circadian rhythms for all families and individuals. Ultradian components were detected in 50% of the families and in 46.7% of the animals. Acrophases of self- and social grooming calculated by Single Cosinor took place between 9:21 h and 10:39 h, for the families. For individuals self- and social grooming made and received, acrophases occurred from 8:35 h to 12:43 h. The confidence limits of acrophases did not show differences between the families and the individuals within the families, irrespective of their sex, age and reproductive condition, suggesting that this behavior has a stronger temporal marking. Grooming has circadian and ultradian components of rhythmicity in captive families' groups of common marmosets, under natural environmental conditions. Since only some animals showed the ultradian component, it may be consequence of social or environmental masking, or yet phenotypic plasticity of temporal genotype. Further studies are needed to test these possibilities.     

Pineal Gland and Circadian Locomotor Activity Rhythm in the Lacertid Gallotia galloti eisentrauti: Pinealectomy Induces Arrhythmicity

In order to contribute to a comparative view on lacertids, the effect of pinealectomy on the freerunning activity displayed under constant darkness and temperature (27.5°C ± 0.5) has been studied in the lizard Gallotia galloti eisentrauti . Animals showed an entrained motor activity rhythm under an initial light-dark (12:12 hours) routine and freerunning circadian periods ranging between 24.1 and 25.5 h during constant darkness (periodograms obtained by Sokolove & Bushell's method). After pinealectomy, most animals showed no significant circadian rhythm, their locomotor activity becoming diffuse throughout the whole 24 h period. Thus, the pineal gland seems to play an important role as a main pacemaker regulating the endogenous activity rhythm under constant conditions. This result contrasts with that found in Podarcis sicula where after pinealectomy only changes in length of the freerunning period were found.     

Behavioral and cardiophysiological responses of common marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>) to confrontations with opposite-sexed strangers

Common marmosets exhibit under captive conditions socially monogamous propensities. During confrontation with opposite-sexed stranger, in the presence of the pairmate, common marmosets often respond aggressively. However, in the absence of their mates, males actively solicit contact and even sexual interactions with strange females whereas mated females are indifferent to strange males. In the present study behavioral and cardiophysiological responses of pairmates of six established pairs of common marmosets were recorded during confrontation with an opposite-sexed stranger (1) in the presence or (2) in the absence of the familiar pairmate. Systolic and diastolic blood pressure, heart rate as well as locomotor activity were recorded telemetrically through peritoneally implanted transmitters. Behavioral responses were videotaped and in addition, urine samples from the female individuals were analyzed for their estrogen concentrations to monitor their ovarian cycles. The cardiophysiological values did not differ significantly between the two confrontation conditions. However, compared to baseline, heart rate values of both sexes and in males also blood pressure values, were significantly higher during confrontations. Hence, confrontations with an opposite-sexed conspecific clearly affect cardiophysiological parameters. Between confrontees affiliative behaviors could not been recorded but aggressive and sexual behaviors occurred.     

Behavioral and cardiophysiological responses of common marmosets (Callithrix jacchus) to social and environmental changes

Under captive conditions common marmosets (Callithrix jacchus) show socially monogamous propensities. Male and female form a social bond as characterized by signs of behavioral arousal during separation of the pairmates, high levels of affiliative interactions between pairmates and agonistic responses towards strange conspecifics. In the present study behavioral and cardiophysiological responses of mated individuals of common marmosets were recorded while the animals were in an unfamiliar environment (1) alone, (2) with the pairmate, or (3) with an opposite-sexed stranger. Pairmates of 6 established pairs were tested in 3 replicates yielding a total of 36 trials per experiment. A trial was divided into three 10-min segments (baseline; unfamiliar environment; reunion). Behavioral responses were videotaped with a remote controlled camera system installed within the cage. Systolic (SBP) and diastolic blood pressure (DBP), and heart rate (HR) as well as locomotor activity (ACT) were recorded telemtrically through peritoneally implanted transmitters. The individuals’ responses measured while in an unfamiliar environment was only reduced by the pairmate, but not by an opposite-sexed stranger. No affiliative behaviors occurred between strange conspecifics, whereas aggressive and sexual behaviors were observed. During reunion with the pairmate individuals recovered physiologically. The present study shows that an individualized pair bond exists between pairmates of common marmosets. Further, it becomes evident that establishing a social bond with the pairmate is important for maintaining physiological homeostasis.     

Unrearable litters and prenatal reduction of litter size in the common marmoset (Callithrix jacchus).

It is widely believed that common marmosets (Callithrx jacchus) typically give birth to twins under natural conditions. In captivity, however, births of triplets or even larger litters are common, although parents rarely succeed in rearing more than two offspring. The traditional interpretation is that captive conditions, notably the ready availability of food, have led to increased reproductive output, perhaps involving a higher ovulation rate. The present paper provides evidence, combined from ultrasound examinations between ovulation and birth and hysterotomies conducted during the late embryonic and early fetal phase, that the litter size can be progressively reduced during pregnancy without spontaneous abortion. There is an unusually long lag phase prior to the onset of embryonic growth in common marmosets; the fetal stage does not begin until day 80 of the 144-day pregnancy. Reduction in litter size occurs during embryonic stages (up to day 80), and continues into the fetal stages. These results indicate that the common marmoset is adapted for flexible modification of litter size between ovulation and birth. The high incidence of triplet births in captive colonies may therefore be an expression of an adapted natural developmental process under artificial circumstances.     

Seasonal changes of locomotor activity patterns in the desert isopod Hemilepistus reaumuri

The locomotor activity rhythm of the desert woodlouse Hemilepistus reaumurii was monitored as individuals over the four seasons, under entraining and constant darkness conditions. Results indicated that individuals exhibited an endogenous rhythm of locomotor activity with a circadian period longer in spring than the other seasons whatever the regimen. Due to the important inter-individual variability, no significant difference in period was found between seasons as well as between regimens. Periodogram analysis revealed also an ultradian period around 12 h. Activity was mostly confined to the hours of the photophase or to those of subjective day. The activity pattern showed two main peaks. This bimodal circadian rhythm persisted for as long as the experiments were run, and was clearer in summer and autumn than in winter. The most clearly defined rhythms were found in spring and summer recordings, respectively, under entraining and free running conditions. The variation of activity patterns according to the seasons will be discussed.     

Kinetics in metabolic control of time measurement in photoperiodism

Abstract

The period length of the locomotor activity rhythm of Drosophila melanogaster wild form is under conditions of continuous weak red light 23.38 h, whereas die eye mutants Ly3 with a 23.71 h mean period and JK 84 with 23.14 h differ significantly. This might be due to a changed perception of light and not the result of a change in the circadian pacemaker by the mutation.

The mutant sine oculis exhibits a normal activity rhythm if the complex eyes are not completely reduced. If this is the case, the activity pattern is either less rhythmic, composed of several rhythms with different periods or truely arrhythmic depending on the individual fly.

Since the mutation in sine oculis affects in addition to the complex eye the distal part of die medulla and the lamina of the optic lobe, it is suggested that the circadian pacemakers for the locomotor activity rhythm is localized in these parts.     

Locomotor Activity of the Fiddler Crab, Uca subcylindrica (Stimpson), under Artificial Illumination

Specimens of the fiddler crab Uca subcylindrica (Stimpson) were captured in south Texas (USA) for locomotor rhythm studies. Actographic data were analyzed using Tau™ sofware. Under constant illumination (LL) and darkness (DD), the semiterrestrial crabs express a circadian rhythm of locomotion. When exposed to illumination/darkness cycles (LD_12:12 or LD_14:10), their bouts of activity are entrained to the photoperiod. In LD, activity is generally bimodal with an initial burst about 0.5 h after illumination. A second burst of activity begins 1 to 2 h before the end of illumination. When transferred from LD to LL, a locomotor rhythm with an average period of 24.6 ± 1.0 h (n = 19) is expressed in 89 percent of the crabs. On the other hand, when placed in DD after LD (n = 8), the crabs are either arrythmic or weakly rhythmic (period = 23.8 ± 0.2 h; n = 2). If the onset of illumination is advanced by 6 h, a period of less than 24.0 h is detected in the actogram. If the onset of illumination is delayed by 6 h, a locomotor rhythm with a period greater than 24.0 h appears. The locomotor behavior of this species of fiddler crab, Uca subcylindrica, is not related to the tidal rhythmicities seen in other members of the genus Uca. Rather, it has strong circadian components.     

Circadian Rhythm in the Locomotor Activity of a Surface-Dwelling Millipede Syngalobolus sp.

Locomotor activity of the surface-dwelling millipede Syngalobolus sp. was recorded under laboratory conditions. Infra-red diodes were used to detect the locomotor activity in an oval shaped chamber, which was connected with an event recorder. The results of 11 individuals showed that the millipedes entrained to light/dark (LD12:12 h) conditions with negative phase angle difference (-83.2 ± 24.72 min). The millipedes showed a clear-cut free-running rhythm with a period (t) of 23.8 ± 1.0 h (n = 9) in constant darkness (DD). The period in continuous light (LL) was relatively greater (25.2 ± 0.1 h; n = 3) than that in DD.     

Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function

The cheetah (Acinonyx jubatus) is highly endangered because of loss of habitat in the wild and failure to thrive in captivity. Cheetahs in zoos reproduce poorly and have high prevalences of unusual diseases that cause morbidity and mortality. These diseases are rarely observed in free-ranging cheetahs but have been documented in cheetahs that have been captured and held in captive settings either temporarily or permanently. Because captivity may be stressful for this species and stress is suspected as contributing to poor health and reproduction, this study aimed to measure chronic stress by comparing baseline concentrations of fecal corticoid metabolites and adrenal gland morphology between captive and free-ranging cheetahs. Additionally, concentrations of estradiol and testosterone metabolites were quantified to determine whether concentrations of gonadal steroids correlated with corticoid concentration and to assure that corticosteroids in the free-ranging samples were not altered by environmental conditions. Concetntrations of fecal corticoids, estradiol, and testosterone were quantified by radioimmunoassay in 20 free-ranging and 20 captive cheetahs from samples collected between 1994 and 1999. Concentrations of baseline fecal corticoids were significantly higher (p = 0.005) in captive cheetahs (196.08 +/- 36.20 ng/g dry feces) than free-ranging cheetahs (71.40 +/- 14.35 ng/g dry feces). Testosterone concentrations were lower in captive male cheetahs (9.09 +/- 2.84 ng/g dry feces) than in free-ranging cheetahs (34.52 +/- 12.11 ng/g dry feces), which suggests suppression by elevated corticoids in the captive males. Evidence for similar sulppression of estradiol concentrations in females was not present. Adrenal corticomedullary ratios were determined on midsagittal sections of adrenal glands from 13 free-ranging and 13 captive cheetahs obtained between 1991 and 2002. The degree of vacuolation of cortical cells in the zona fasciculata was graded for each animal. Corticomedullary ratios were larger (p = 0.05) in captive cheetahs; however, there was no difference (p = 0.31) in the degree of corticocyte vacnolation between the two populations. These data proxile both mnorphologic and functional evidence suggestive of chronic stress in captive cheetahs. Further research into the role of hypercortisolemia in the pathogenesis of the reproductive abnormalities and unusual diseases of captive cheetahs is needed.