Free-Running Locomotor Activity Rhythms in Cave-Dwelling Catfishes,Trichomycterus sp., from Brazil (Teleostei,Siluriformes)

Locomotor activity of troglobitic (cave restricted) catfishes, Trichomycterus sp., was recorded in the laboratory under constant darkness for ten consecutive days. Infra-red photocell beam crossings were totalled every thirty minutes and stored for later analysis. Spectral analysis of the data followed by a statistical test designed for the detection of significant components was then performed. The results of 14 individuals, seven pigmented and seven albino fishes, are reported here. In eight individuals, four pigmented and four albinos, we were not able to detect significant components in the circadian range, although ultradian and/or infradian significant components were found in all cases. Former studies on other two Brazilian cave catfishes, Pimelodella kronei and Imparfinis sp., showed similar results, suggesting a picture of gradual loss of circadian rhythmicity and persistence of ultradian and infradian rhythms in the locomotor activity of troglobitic populations. The proportion of specimens without significant circadian components was higher in Trichomycterus sp., supposedly less specialized to cave life than the other two species. This is tentatively correlated with a higher environmental stability during the time of evolutionary isolation in the subterranean biotope. These results provide strong arguments for the importance of external selection over circadian rhythmicity.     

Locomotor Activity Rhythms in Cave Catfishes, Genus Taunayia, from Eastern Brazil (Teleostei: Siluriformes: Heptapterinae)

We studied the locomotor rhythmicity in heptapterine catfishes, genus Taunayia, under free-running conditions (DD) and LD cycles (12:12). Taunayia sp., anophthalmic and depigmented undescribed species from a cave in northeastern Brazil, is the fourth Brazilian troglobitic catfish studied with focus on circadian rhythms. Weak free-running rhythmicity, with absence of significant circadian components, was observed for this species when compared to the epigean, eyed relatives. On the other hand, the studied troglobitic catfishes in general presented significant circadian rhythms under LD cycles, with activity peaks in the night phase probably corresponding to nocturnal activity pattern inherited from their epigean ancestors. However, no residual oscillations were observed after transition from LD to DD. This indicates masking of activity by light-dark cycles. Regression of circadian rhythmicity in the stable, permanently dark subterranean habitat was also observed for other cave fishes. Such regression corroborates the notion that circadian rhythmicity is mainly selected in the epigean environment by ecological factors, namely daily cycles of light and/or temperature.     

Locomotor Activity Rhythms in Cave Catfishes,Genus Taunayia,from Eastern Brazil (Teleostei: Siluriformes: Heptapterinae)

We studied the locomotor rhythmicity in heptapterine catfishes, genus Taunayia, under free-running conditions (DD) and LD cycles (12:12). Taunayia sp., anophthalmic and depigmented undescribed species from a cave in northeastern Brazil, is the fourth Brazilian troglobitic catfish studied with focus on circadian rhythms. Weak free-running rhythmicity, with absence of significant circadian components, was observed for this species when compared to the epigean, eyed relatives. On the other hand, the studied troglobitic catfishes in general presented significant circadian rhythms under LD cycles, with activity peaks in the night phase probably corresponding to nocturnal activity pattern inherited from their epigean ancestors. However, no residual oscillations were observed after transition from LD to DD. This indicates masking of activity by light-dark cycles. Regression of circadian rhythmicity in the stable, permanently dark subterranean habitat was also observed for other cave fishes. Such regression corroborates the notion that circadian rhythmicity is mainly selected in the epigean environment by ecological factors, namely daily cycles of light and/or temperature.     

Locomotor activity rhythms in cave fishes from Chapada Diamantina, northeastern Brazil (Teleostei: Siluriformes)

Previous studies on the locomotor activity of troglobitic (exclusively subterranean) species have shown that circadian rhythmicity may be reduced in populations evolving in the absence of zeitgebers such as daily cycles of light and temperature; therefore, circadian activity rhythms, although not infradian nor ultradian rhythms, seem to have been selected by external, ecological factors. We studied the locomotor activity of a highly specialized Heptapteridae catfish (undescribed genus and species) from Chapada Diamantina, NE Brazil, compared to another specialized Brazilian troglobitic heptapterid, Taunayia sp. Locomotor activity was continuously measured in the laboratory with an infra-red photocell system. Seven specimens of the new genus were tested, each one during 14 consecutive days according to the following schedule: three days in DD → seven days in LD (12:12 h) → four days in DD. Data were submitted both to fast Fourier transform periodogram followed by Siegel's test of significance and Lombs - Scargle periodogram techniques in order to identify spectral composition of the time series. In general, results were similar to those obtained for Taunayia sp.: (a) for most specimens, absence of significant circadian components in locomotor activity under DD; (b) for all specimens, significant circadian components under LD, with higher levels of activity during the dark phase, as expected for species belonging to nocturnal epigean taxa; (c) for most specimens, no residual oscillations recorded when free-running conditions were reinstalled. Circadian locomotor activity detected under LD may thus be interpreted as a direct, masking effect of the LD cycle. This suggests a pattern for highly specialized troglobitic species, isolated for a long time in the subterranean habitat, with a progressive reduction of circadian time-keeping mechanisms. Our studies also demonstrate the potential of subterranean organisms for investigation of the origin, evolution, functioning and genetics of circadian rhthmicity.     

Food and reproduction of Trichomycterus itacarambiensis, cave catfish from south-eastern Brazil

Trichomycterus itacarambiensis is a troglobitic (cave-restricted) catfish found in the Olhos ďÁgua Cave, Itacarambi Co., Minas Gerais, south-eastern Brazil. The cave is subject to a pronounced seasonality, and is flooded during part of the rainy season. The pigmentation degree is variable in T. itacarambiensis , a third of the population being true albinos; the eyes vary from normal to externally invisible. As expected for a cave-dwelling fish, T. itacarambiensis is a carnivorous generalist, which preys mainly on autochthonous insects and earthworms. It is a chemically oriented predator of bottom and surface animals, using foraging tactics also used by other cave catfishes, such as the pimelodids Pimelodella kronei and Imparfinis sp. However, bottom feeding seems to be more important for T. itacarambiensis than for the latter. There is a severe feeding stress during the dry season, when few individuals are able to get food. Reproduction is seasonal, with increased reproductive activity at the end of the rainy period, as recorded for Imparfinis sp., also a species living in a semi-arid region with a well-defined dry season. It is estimated that up to 50% of the female T. itacarambiensis can reproduce every year, a high proportion for a troglobitic fish species. At least during the study period, pigmented individuals reproduced more frequently than the albinos.     

Population ecology of Trichomycterus itacarambiensis, a cave catfish from eastern Brazil (Siluriformes, Trichomycteridae)

The population ecology of the trichomycterid catfish, Trichomycterus itacarambiensis, from the Olhos d'Àgua Cave, Itacarambi Co., Minas Gerais, eastern Brazil, was investigated by the mark-recapture method during the dry season of 1994 (April to October). The cave is subject to a pronounced seasonality, and is flooded during part of the rainy period. All individuals captured along the 5000 m long stream gallery (divided in 50 sections) were marked by tattooing, measured and examined for the degree of pigmentation reduction. About one third of the population is truly albinic; the remainder may exhibit partial depigmentation. After five bimestrial collections, 583 specimens have been marked, of which 150 were recaptured at least once. Estimated population size was 1500–2000 individuals longer than 20 mm SL. The total population size of T. itacarambiensis is considered small when compared to those of epigean trichomycterids and of other studied cavefishes as well. Mean population density was 0.15–0.20 individuals m^-2 throughout the dry season; it increased with the distance to the stream resurgence, probably due to the higher food availability upstream. This population density may be considered intermediate to those of other troglobitic fishes. Most recaptures (66%) were done in the same section as the previous capture. Active movements, both upstream and downstream, were recorded up to distances of 600 m; a few possibly passive, downstream movements covered distances from 900 to 1500 m. T. itacarambiensis catfishes move more frequently and for longer distances than the Brazilian blind pimelodids, Pimelodella kronei. Individual growth in T. itacarambiensis probably occurs in pulses, during the rainy seasons; interruption of growth in the dry season is attributed to the pronounced food shortage. The mean longevity was estimated as seven years. Differences between pigmented and albino individuals include a higher frequency of downstream movements and slightly higher growth rates in the latter.     

Cellular oscillators: rhythmic gene expression and metabolism

Many biological processes are driven by biological clocks that, depending on the frequency they generate, are classified into ultradian, circadian and infradian oscillators. In virtually all light-sensitive organisms from cyanobacteria to humans, a circadian timing system adapts cyclic physiology to geophysical time. Recent evidence suggests that even in mammals circadian oscillators function in a cell-autonomous manner. In yeast, an ultradian oscillator regulates cyclic respiratory activity and global gene expression. Circadian oscillators and the ultradian yeast respiratory clock share at least four properties: they follow limit-cycle kinetics, interweave with cellular metabolism, are temperature-compensated and influence the cell division clock.     

Changes in Body Temperature Rhythm after Traumatic Brain Injury

We performed this study to determine whether in head injured patients body temperature rhythmicity exists outside the usual spectrum. Temperature data of in total 22 patients with head injury were analyzed using the Regressive and Iterative Cosinor methods. We found that circadian rhythm often remained, and usually was combined with rhythms in ultradian or infradian ranges. Tau shifts over consecutive days were observed in three severely head injured patients (Glasgow Coma Scale score ≤ 8). To validate the results we used surrogate data. Detection of temperature rhythms in this study may serve to estimate the clinical importance of biological rhythms in head injury.     

Changes in Body Temperature Rhythm after Traumatic Brain Injury

We performed this study to determine whether in head injured patients body temperature rhythmicity exists outside the usual spectrum. Temperature data of in total 22 patients with head injury were analyzed using the Regressive and Iterative Cosinor methods. We found that circadian rhythm often remained, and usually was combined with rhythms in ultradian or infradian ranges. Tau shifts over consecutive days were observed in three severely head injured patients (Glasgow Coma Scale score ≤ 8). To validate the results we used surrogate data. Detection of temperature rhythms in this study may serve to estimate the clinical importance of biological rhythms in head injury.     

Epigean and subterranean ichthyofauna from the São Domingos karst area, Upper Tocantins River basin, Central Brazil

In a survey of epigean and cave streams in the São Domingos karst area, 38 species were present in the stream reaches, including 10 characiforms, 19 siluriforms, seven gymnotiforms and two perciforms. One species of Astyanax and the new armoured catfish species Parotocinclus were the most common epigean fishes in São Domingos. The most conspicuous non-troglomorphic cave fishes were Hoplerythrinus unitaeniatus , Astyanax sp., Brycon sp. and two species of Imparfinis , with I. hollandi being the most common fish in most caves. São Domingos karst area has the most diverse and abundant Brazilian cavefish fauna, not only in terms of troglobitic species but also in general fish richness, with 22 non-troglomorphic species recorded in caves in addition to five troglobitic ones. Most fishes examined for stomach contents had at least partially full stomachs. The studied fishes were carnivorous, feeding primarily on aquatic insects. Fishes with developed gonads recorded in caves were I. hollandi , Rhamdia quelen , Pseudocetopsis plumbeus , Hoplerythrinus unitaeniatus and Cichlasoma araguaiensis , indicating a potential for reproduction in the subterranean habitat.     

Differential elimination of circadian and ultradian rhythmicity by hypothalamic lesions in the common vole, Microtus arvalis

Effects of hypothalamic lesions on the ultradian and circadian organization of wheel running and feeding were studied in the common vole, Microtus arvalis. Circadian organization broke down within 30 days in continuous darkness in 24% of intact voles (n = 135). Ultradian rhythmicity of feeding (period 2-3 hr) persisted in constant conditions in all intact voles. Following lesions of the suprachiasmatic nuclei (SCN), circadian rhythmicity disappeared when lesions were complete (n = 8) or more extensive than 25% of the total SCN volume (n = 5). Absence of circadian rhythmicity was also found in animals with substantial lesions in the diencephalic paraventricular area (PVA) and in the retrochiasmatic area (RCA) and/or adjacent arcuate nucleus (Arc). Complete loss of ultradian and circadian organization occurred in eight voles with damage to the RCA and/or Arc. In three of these, the SCN was intact. The SCN is a likely candidate for a circadian pacemaker in voles (as in other rodents), while the loss of circadian rhythmicity following PVA and RCA/Arc lesions may be due to destruction of efferent pathways from the SCN. The RCA/Arc area is apparently necessary for the expression of ultradian rhythms. The intact SCN is neither necessary nor sufficient for the generation of ultradian rhythmicity.     

From Ultradian to Infradian Rhythms: LH Releases Patterns In Vitro

In the present study, we examined in vitro luteinizing hormone (LH) release patterns from pituitaries and from pituitary cell cultures (3 and 7 days in culture) to elucidate the endogenous period generated by the gonadotroph cell population and to evaluate the relationship between the basic period generated at the cellular level and the output pattern observed at the organ level. In addition, we examined the effect of photic environmental signals perceived by the animals on LH release patterns from pituitaries in vitro. When the animals were exposed to circadian photoperiodic signals, the in vitro LH release pattern from the pituitaries exhibited ultradian, circadian, and infra-dian frequencies. When the animals were exposed to continuous illumination, the in vitro patterns exhibited only ultradian and infradian frequencies. Furthermore, free running is a process, not a state. This process is driven by a change in the relative dominance of different frequencies that construct the pattern without changing the basic period length. Evaluation of the relative dominance of the different frequencies that construct the pattern indicates that, although infradian oscillators may take part in shaping the output pattern, the basic rhythm generated by the pituitary cells is in the ultradian domain. The results obtained from the examined system suggest that an endogenous oscillator is a cellular entity with ultradian periodicity, and that the rhythmic output of many biological variables is structured by various ultradian components that construct the circadian and infradian output rhythms.     

From Ultradian to Infradian Rhythms: LH Releases Patterns In Vitro

In the present study, we examined in vitro luteinizing hormone (LH) release patterns from pituitaries and from pituitary cell cultures (3 and 7 days in culture) to elucidate the endogenous period generated by the gonadotroph cell population and to evaluate the relationship between the basic period generated at the cellular level and the output pattern observed at the organ level. In addition, we examined the effect of photic environmental signals perceived by the animals on LH release patterns from pituitaries in vitro. When the animals were exposed to circadian photoperiodic signals, the in vitro LH release pattern from the pituitaries exhibited ultradian, circadian, and infra-dian frequencies. When the animals were exposed to continuous illumination, the in vitro patterns exhibited only ultradian and infradian frequencies. Furthermore, free running is a process, not a state. This process is driven by a change in the relative dominance of different frequencies that construct the pattern without changing the basic period length. Evaluation of the relative dominance of the different frequencies that construct the pattern indicates that, although infradian oscillators may take part in shaping the output pattern, the basic rhythm generated by the pituitary cells is in the ultradian domain. The results obtained from the examined system suggest that an endogenous oscillator is a cellular entity with ultradian periodicity, and that the rhythmic output of many biological variables is structured by various ultradian components that construct the circadian and infradian output rhythms.     

The end effector of circadian heart rate variation: the sinoatrial node pacemaker cell

Cardiovascular function is regulated by the rhythmicity of circadian, infradian and ultradian clocks. Specific time scales of different cell types drive their functions: circadian gene regulation at hours scale, activation-inactivation cycles of ion channels at millisecond scales, the heart''s beating rate at hundreds of millisecond scales, and low frequency autonomic signaling at cycles of tens of seconds. Heart rate and rhythm are modulated by a hierarchical clock system: autonomic signaling from the brain releases neurotransmitters from the vagus and sympathetic nerves to the heart’s pacemaker cells and activate receptors on the cell. These receptors activating ultradian clock functions embedded within pacemaker cells include sarcoplasmic reticulum rhythmic spontaneous Ca²⁺ cycling, rhythmic ion channel current activation and inactivation, and rhythmic oscillatory mitochondria ATP production. Here we summarize the evidence that intrinsic pacemaker cell mechanisms are the end effector of the hierarchical brain-heart circadian clock system. [BMB Reports 2015; 48(12): 677-684]     

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.     

Physiology and regulation of biological rhythms in laboratory animals: an overview

Biological rhythms have been observed in practically all groups of laboratory mammals and at every level of physiological and behavioural organization. Biological rhythms are classified according to their period as ultradian (less than 24 h), circadian (approximately 24 h), infradian (greater than 24 h), and seasonal or circannual rhythms (approximately 1 year). This review outlines what is known about the neurobiology of biological rhythms in mammals and describes the hierarchical order in which ultradian, circadian and infradian rhythms are related to each other. The article does not attempt to catalogue every physiological variable showing rhythmical fluctuations in laboratory mammals. Rather, it focuses on the basic concepts of circadian rhythms and recent advances made in our understanding of the physiology of the internal clock controlling circadian and other biological rhythms.     

Cave adaptation in the spider genus Anthrobia (Araneae, Linyphiidae, Erigoninae)

The genus Anthrobia Tellkampf, 1844 is revised and expanded to include two epigean species, Anthrobia acuminata ( Emerton, 1913 ) comb. nov., and A. whiteleyae sp. nov., and two troglobites, the type species A. monmouthia Tellkampf, 1844 , and A. coylei sp. nov. The female of A. acuminata is described for the first time. All four Anthrobia species were added to a phylogenetic analysis of erigonine genera. Analysis of this matrix results in a single most parsimonious tree (length = 915, CI = 0.23, RI = 0.58; uninformative characters excluded: length = 911, CI = 0.23), which places Anthrobia sister to Diplocentria Hull, 1911. Troglobitic Anthrobia and epigean Anthrobia are both monophyletic. In comparison to the epigean species, troglobitic Anthrobia exhibit the following putative adaptations to cave life: loss of eyes, elongation of the legs, and reduction of the tracheal system. The reliability of phylogenetic results indicating monophyly of cave Anthrobia are discussed in light of the fact that potentially cave adaptive synapomorphies support this relationship.     

Ultradian clocks in eukaryotic microbes: from behavioural observation to functional genomics

Period homeostasis is the defining characteristic of a biological clock. Strict period homeostasis is found for the ultradian clocks of eukaryotic microbes. In addition to being temperature-compensated, the period of these rhythms is unaffected by differences in nutrient composition or changes in other environmental variables. The best-studied examples of ultradian clocks are those of the ciliates Paramecium tetraurelia and Tetrahymena sp. and of the fission yeast, Schizosaccharomyces pombe. In these single cell eukaryotes, up to seven different parameters display ultradian rhythmicity with the same, species- and strain-specific period. In fission yeast, the molecular genetic analysis of ultradian clock mechanisms has begun with the systematic analysis of mutants in identified candidate genes. More than 40 "clock mutants" have already been identified, most of them affected in components of major regulatory and signalling pathways. These results indicate a high degree of complexity for a eukaryotic clock mechanism. BioEssays 22:16-22, 2000.     

Effect of geomagnetic activity on the rhythm of resistance of rats to hypoxia

The resistance of male Wistar rats to acute hypoxia was estimated from the lifetime at an "altitude" of 11.5 km above sea level from 13 to 21 p.m. and in different seasons of a year. Identical types of rhythms (circaseptan, circasemiseptan, infradian, circadian, and ultradian) of geomagnetic activity and lifetime were revealed. It was found that the periods of basal rhythms either coincide or are multiple. It was shown that the rhythms of geomagnetic activity (including nonbasal rhythms) affect lifetime rhythms (especially ultradian rhythms). As the periods of the rhythms decrease, the number of rhythms for both parameters increase (ultradian rhythms are most numerous), and relative differences in the values of periods (they are minimal for ultradian rhythms) and the amplitudes of rhythms decrease.     

A Four-Year Follow-Up Study of the Sleep-Wake Cycle of an Infant

The sleep-wake behavior of a boy was investigated from 5 weeks up to four years of age. The protocol consisted of recording waking and sleep states by direct observation by his mother and eventually by the housemaid. Data were divided in 7-day segments and these segments were then divided in 10-minute binary information about asleep or awake. Fast Fourier Transform (FFT) was applied to obtain the frequency spectrum for each 7-day epoch, and the results were submitted to statistical test for the identification of significant component frequencies. Data were also divided in 21-day epochs and 30-minute windows in order to detect infradian periodicities. Overall rhythmicity increased during the four years with the circadian component as the major contribution after the fifth week of life. The semicircadian and the 8-hour components had maximum contributions during the second and third years, and the 6-, 5- and 4-hour components during the first year. After the beginning of his attendance to school, the boy showed a decrease of the semicircadian component, explained by the absence of an afternoon nap and an increase of the circadian component. Infradian periodicities were not found during the whole four years.