A daily rhythm in mating behavior in a diurnal murid rodent Arvicanthis niloticus

The time of day at which mating occurs is dramatically different in diurnal compared to nocturnal rodents. We used a diurnal murid rodent, Arvicanthis niloticus, to determine if inverted rhythms in responsiveness to hormones contribute to this difference. Male and hormone-primed female grass rats were tested for mating behavior at four different times of day (ZT 5, 11, 17, 23; ZT 0=lights-on). In females, there was considerable inter-individual variability with respect to patterns of responsiveness to hormones. Overall, the lordosis quotient (LQ) was rhythmic with a single peak just before lights-on (ZT 23); however, while roughly half of the females (7/15) exhibited this clear daily rhythm, the remaining animals (8/15) had relatively high LQs that did not change as a function of time. Males had their shortest ejaculation latencies and their highest number of ejaculations at ZT 23. Rhythms in mount frequency and post-ejaculatory refractory period were bimodal, with peaks around lights-on and -off (ZT 23 and 11). This temporal pattern of mounting behavior closely parallels previously documented patterns of general activity, whereas rhythms in the more reflexive components of sex behavior (LQ and ejaculation) had more restricted peaks that coincided with just the onset of rhythms in general activity. These rhythms in sexual behavior are essentially reversed relative to those previously documented in lab rats.     

Nocturnal and diurnal rhythms in the unstriped Nile rat, Arvicanthis niloticus.

In a laboratory population of unstriped Nile grass rats, Arvicanthis niloticus, individuals with two distinctly different patterns of wheel-running exist. One is diurnal and the other is relatively nocturnal. In the first experiment, the authors found that these patterns are strongly influenced by parentage and by sex. Specifically, offspring of two nocturnal parents were significantly more likely to express a nocturnal pattern of wheel-running than were offspring of diurnal parents, and more females than males were nocturnal. In the second experiment, the authors found that diurnal and nocturnal wheel-runners were indistinguishable with respect to the timing of postpartum mating, which always occurred in the hours before lights-on. Here they also found that both juvenile and adult A. niloticus exhibited diurnal patterns of general activity when housed without a wheel, even if they exhibited nocturnal activity when housed with a wheel. In the third experiment, the authors discovered that adult female A. niloticus with nocturnal patterns of wheel-running were also nocturnal with respect to general activity and core body temperature when a running wheel was available, but they were diurnal when the running wheel was removed. Finally, a field study revealed that all A. niloticus were almost exclusively diurnal in their natural habitat. Together these results suggest that individuals of this species are fundamentally diurnal but that access to a running wheel shifts some individuals to a nocturnal pattern.     

Circadian regulation of gonadotropin-releasing hormone neurons and the preovulatory surge in luteinizing hormone in the diurnal rodent, Arvicanthis niloticus, and in a nocturnal rodent, Rattus norvegicus

Daily rhythms in the timing of the preovulatory surge and the display of reproductive behavior are reversed in diurnal and nocturnal rodents, but little is known about the neural mechanisms underlying these differences. We examined this issue by comparing a diurnal murid rodent, Arvicanthis niloticus (the grass rat), to a nocturnal one, Rattus norvegicus (the lab rat). In the first study, we established that sequential estradiol and progesterone treatment induces a proestrous-like rise in LH secretion and in the percentage of GnRH neurons that express Fos in grass rats, as is the case in lab rats. Next, we tested the hypothesis that differences in the timing of estrus-related events in diurnal and nocturnal species are caused by differences in rhythms in responsiveness to steroid hormones. We found rhythms in GnRH neuron activity, as indicated by Fos, that were 12 hours out of phase in grass rats and lab rats. These patterns persisted in both species when animals were housed in constant darkness for 5 days, suggesting that they are driven by an endogenous circadian mechanism. These results indicate that steroid-primed grass rats and lab rats are similar with respect to the temporal relationship among estrus-related events, but that the timing of these events relative to the light-dark cycle is dramatically different and that this difference is caused by endogenous circadian mechanisms.     

A morning surge in plasma luteinizing hormone coincides with elevated Fos expression in gonadotropin-releasing hormone-immunoreactive neurons in the diurnal rodent, Arvicanthis niloticus.

Arvicanthis niloticus is a diurnal murid rodent from sub-Saharan Africa. Here we report on processes associated with mating in this species in an attempt to elucidate how the neural mechanisms governing temporal organization differ in nocturnal and diurnal species. First, we systematically mapped the distribution of GnRH neurons in adult females. Second, we tested the hypothesis that Arvicanthis differ from nocturnal murid rodents with respect to the timing of the LH surge and the associated increase in Fos expression in GnRH-immunoreactive (IR) neurons. We examined these events around a postpartum estrus. When parturition occurred between zeitgeber time (ZT) 2 and 17 (lights on at ZT 0 and off at ZT 12; there are 24 ZT units a day, each equivalent to 1 standard hour), we collected blood and perfused females at ZT 17, 20, 23, or 2. A sharp peak in plasma LH occurred at ZT 20, and a 10-fold increase in the percentage of GnRH-IR neurons that expressed Fos-IR occurred between ZT 17 and 20. By contrast, this rise occurs in nocturnal rodents during the last few hours of the light period. This is the first indication of a difference between nocturnal and diurnal animals with respect to neural mechanisms associated with a precisely timed event of known significance.     

Acute Behavioral Responses to Light and Darkness in Nocturnal Mus musculus and Diurnal Arvicanthis niloticus

The term masking refers to immediate responses to stimuli that override the influence of the circadian timekeeping system on behavior and physiology. Masking by light and darkness plays an important role in shaping an organism's daily pattern of activity. Nocturnal animals generally become more active in response to darkness (positive masking) and less active in response to light (negative masking), and diurnal animals generally have opposite patterns of response. These responses can vary as a function of light intensity as well as time of day. Few studies have directly compared masking in diurnal and nocturnal species, and none have compared rhythms in masking behavior of diurnal and nocturnal species. Here, we assessed masking in nocturnal mice (Mus musculus) and diurnal grass rats (Arvicanthis niloticus). In the first experiment, animals were housed in a 12:12 light-dark (LD) cycle, with dark or light pulses presented at 6 Zeitgeber times (ZTs; with ZT0 = lights on). Light pulses during the dark phase produced negative masking in nocturnal mice but only at ZT14, whereas light pulses resulted in positive masking in diurnal grass rats across the dark phase. In both species, dark pulses had no effect on behavior. In the 2nd experiment, animals were kept in constant darkness or constant light and were presented with light or dark pulses, respectively, at 6 circadian times (CTs). CT0 corresponded to ZT0 of the preceding LD cycle. Rhythms in masking responses to light differed between species; responses were evident at all CTs in grass rats but only at CT14 in mice. Responses to darkness were observed only in mice, in which there was a significant increase in activity at CT 22. In the 3rd experiment, animals were kept on a 3.5:3.5-h LD cycle. Surprisingly, masking was evident only in grass rats. In mice, levels of activity during the light and dark phases of the 7-h cycle did not differ, even though the same animals had responded to discrete photic stimuli in the first 2 experiments. The results of the 3 experiments are discussed in terms of their methodological implications and for the insight they offer into the mechanisms and evolution of diurnality.     

Rhythms in Fos expression in brain areas related to the sleep-wake cycle in the diurnal Arvicanthis niloticus

Most mammals show daily rhythms in sleep and wakefulness controlled by the primary circadian pacemaker, the suprachiasmatic nucleus (SCN). Regardless of whether a species is diurnal or nocturnal, neural activity in the SCN and expression of the immediate-early gene product Fos increases during the light phase of the cycle. This study investigated daily patterns of Fos expression in brain areas outside the SCN in the diurnal rodent Arvicanthis niloticus. We specifically focused on regions related to sleep and arousal in animals kept on a 12:12-h light-dark cycle and killed at 1 and 5 h after both lights-on and lights-off. The ventrolateral preoptic area (VLPO), which contained cells immunopositive for galanin, showed a rhythm in Fos expression with a peak at zeitgeber time (ZT) 17 (with lights-on at ZT 0). Fos expression in the paraventricular thalamic nucleus (PVT) increased during the morning (ZT 1) but not the evening activity peak of these animals. No rhythm in Fos expression was found in the centromedial thalamic nucleus (CMT), but Fos expression in the CMT and PVT was positively correlated. A rhythm in Fos expression in the ventral tuberomammillary nucleus (VTM) was 180 degrees out of phase with the rhythm in the VLPO. Furthermore, Fos production in histamine-immunoreactive neurons of the VTM cells increased at the light-dark transitions when A. niloticus show peaks of activity. The difference in the timing of the sleep-wake cycle in diurnal and nocturnal mammals may be due to changes in the daily pattern of activity in brain regions important in sleep and wakefulness such as the VLPO and the VTM.     

Light pulses entrain the circadian activity rhythm of a diurnal rodent (Ammospermophilus leucurus)

Circadian rhythms of wheel-running activity of the antelope ground squirrel (Ammospermophilus leucurus) were entrained by light-dark cycles (LD: 100 1x vs total darkness) with periods (T) between ca 23.75 and 24.75 hr. Two 1-hr light pulses per cycle ('skeleton photoperiods') with T = 24.25 hr as well as one 1-hr light pulse per cycle with Ts of 23.75 and 24.25 hr were effective in entraining the circadian activity rhythms in at least 50% of the antelope ground squirrels. Phase and period responses to single 1-hr light pulses were measured which depend on the initial phase and period of the rhythm. It is concluded that discrete (phasic) light input contributes to the mechanism of entrainment to LD cycles in diurnal rodents.     

Chromosomal evidence for a polytypic structure of Arvicanthis niloticus (Rodentia, Muridae)

The analysis of R- and C-banding patterns of chromosomes of Arvicanthis niloticus from five localities of Africa (Egypt, Senegal, Burkina-Faso, Mali and Central African Republic) revealed the existence of three karyotypic forms labelled in the study as ANI-1, ANI-2 and ANI-3. These forms differ from each other by 6 to 8 chromosomal rearrangements such as reciprocal and Robertsonian translocations and pericentric inversions. Moreover, they possess different quantities of C-heterochromatin. The data indicate that these three forms are distinct species, cytogenetically isolated, and that a further taxonomic analysis of the genus Arvicanthis is needed.     

Functional and anatomical variations in retinorecipient brain areas in Arvicanthis niloticus and Rattus norvegicus: implications for the circadian and masking systems

ABSTRACT

Daily rhythms in light exposure influence the expression of behavior by entraining circadian rhythms and through its acute effects on behavior (i.e., masking). Importantly, these effects of light are dependent on the temporal niche of the organism; for diurnal organisms, light increases activity, whereas for nocturnal organisms, the opposite is true. Here we examined the functional and morphological differences between diurnal and nocturnal rodents in retinorecipient brain regions using Nile grass rats (Arvicanthis niloticus) and Sprague-Dawley (SD) rats (Rattus norvegicus), respectively. We established the presence of circadian rhythmicity in cFOS activation in retinorecipient brain regions in nocturnal and diurnal rodents housed in constant dark conditions to highlight different patterns between the temporal niches. We then assessed masking effects by comparing cFOS activation in constant darkness (DD) to that in a 12:12 light/dark (LD) cycle, confirming light responsiveness of these regions during times when masking occurs in nature. The intergeniculate leaflet (IGL) and olivary pretectal nucleus (OPN) exhibited significant variation among time points in DD of both species, but their expression profiles were not identical, as SD rats had very low expression levels for most timepoints. Light presentation in LD conditions induced clear rhythms in the IGL of SD rats but eliminated them in grass rats. Additionally, grass rats were the only species to demonstrate daily rhythms in LD for the habenula and showed a strong response to light in the superior colliculus. Structurally, we also analyzed the volumes of the visual brain regions using anatomical MRI, and we observed a significant increase in the relative size of several visual regions within diurnal grass rats, including the lateral geniculate nucleus, superior colliculus, and optic tract. Altogether, our results suggest that diurnal grass rats devote greater proportions of brain volume to visual regions than nocturnal rodents, and cFOS activation in these brain regions is dependent on temporal niche and lighting conditions.     

Circadian organization in a diurnal rodent, Arvicanthis ansorgei Thomas 1910: chronotypes, responses to constant lighting conditions, and photoperiodic changes

Little information is available on circadian organization in diurnal mammals. In the present study, the daily patterns of wheel-running activity were described in a diurnal rodent, Arvicanthis ansorgei Thomas 1910, as assessed by karyological analysis. Among 108 animals born in the colony and studied under a 12:12 light-dark cycle (lights on at 7:00 a.m.), the authors determined the timing of daily activity (i.e., mean onsets and offsets of pattern of locomotor activity) and the level of wheel-running activity performed during daytime versus nighttime. The activity pattern was essentially diurnal in 84% of individuals, 46% being active only during the light period +/- 1 h (activity onsets and offsets at 6:20 a.m. and 7:40 p.m., respectively) and 38% being diurnal with a period of nocturnal activity longer than 1 h (activity onsets and offsets at 5:40 a.m. and 9:30 p.m., respectively). Of the 108 animals, 16% expressed a nocturnal activity with diurnal overlaps no longer than 1 h. In 6 diurnal individuals first exposed to constant light and then to constant dim red light, the endogenous period was shortened from 24.6 +/- 0.1 to 24.0 +/- 0.1 h, respectively. The numbers of wheel revolutions per day and during the active period remained unchanged between the two lighting conditions. In response to different photoperiodic changes from 16:08 to 08:16 light-dark cycles, the phase angle of photic synchronization, estimated by the daily onset of wheel-running activity in 6 diurnal animals, showed marked changes, its timing occurring 2 h before and 0.5 h after the onset of light under short and long photoperiods, respectively. The numbers of wheel revolutions per 24 h and during the active period were modified similarly according to photoperiodic changes. Finally, in 5 diurnal animals exposed to a 12:12 light-dark cycle, the daily pattern of general locomotor activity, determined by telemetry, was not modified by wheel availability. The data indicate that A. ansorgei is an interesting experimental model to understand the regulation of the circadian timing system in day-active species.     

LD ratios and the entrainment of circadian activity in a nocturnal and a diurnal rodent

Summary The activity rhythms of 5 flying squirrels,Glaucomys volans, and 7 chipmunks,Tamias striatus, were examined under controlled conditions in the laboratory. Free-running, circadian rhythms were demonstrated using a total of 25 LL or DD experiments. With 46 LD schedules the limits of entrainment in a 24-hour day were determined, and the phase angle difference for each schedule measured.Glaucomys was able to synchronize to schedules ranging from 1 second of light per 24-hour day to at least 18 hours light per day with little or no change in the phase angle.Tamias showed an oscillatory type of entrainment when the photoperiod was less than 3 hours per 24-hour day or greater than 23 hours, but in the intervening region was capable of stable entrainment. A tendency was evident for the phase angle difference to become less positive as the LD ratio increased. InGlaucomys single, isolated light pulses of either one second or 24 hours duration were able to bring about relatively large shifts in the phase of the activity rhythm.Dedicated to Professor Jürgen Aschoff on the occasion of his 60th birthday.I wish to acknowledge the hospitality and assistance of the Zoology Department, University of Wisconsin, Madison, the Max-Planck Institute, Erling-Andechs, Germany, and the Belle W. Baruch Coastal Research Institute, University of South Carolina, Columbia. Special thanks are due Dr. John Emlen and Dr. William Reeder of Madison, Prof. J. Aschoff of Erling-Andechs, Dr. John Vernberg and Dr. Winona Vernberg of Columbia, and my husband, Dr. George DeCoursey, for their untiring encouragement and help with these experiments.     

Effect of tranquilizers on the total acetylcholine content and acetylcholinesterase activity in the brain tissue of Arvicanthis niloticus

The effect of reserpine and meprobamate on the total acetylcholine content and acetylcholinesterase activity in the brain tissue of the kusu rat, Arvicanthis niloticus, was studied. The total acetylcholine content and acetylcholinesterase activity were determined 1 hr after i.p. injection of different doses of reserpine (0.25, 0.5 and 1 mg/ml/100 g body wt) and meprobamate (6.25, 12.5 and 25 mg/ml/100 g body wt). The effect of different time intervals (1, 10, 30 min, 1, 2.5, 5, 8, 12, 24 and 48 hr) on the total acetylcholine content and acetylcholinesterase activity was investigated after i.p. injection of 0.5 mg of reserpine and 12.5 mg of meprobamate/ml/100 g body wt. Both reserpine and meprobamate caused an increase in the total ACh content in the brain tissue of Arvicanthis niloticus which was suggested to be due to a decrease in the release of ACh, since both reserpine and meprobamate inhibited AChE activity after some tested periods. The effect of meprobamate was observed to be stronger than that of reserpine.     

Histological study of Trichosomoides nasalis (Nematoda: Trichinelloidea) in the nasal cavities of the murid Arvicanthis niloticus, with associated pathology

Histological study of the nasal cavities and upper maxillae of Arvicanthis niloticus naturally infected with Trichosomoides nasalis shows that the female worms reside in the epithelial monolayer of the nasal mucosa of the posterior and median cavities. Eggs laid by T. nasalis were infiltrated between the female body wall and the epithelial lining. Small groups of eggs, mixed with mucus and polymorphonuclear cells, were found in the nasal lumen, freed by rupture of the stretched epithelium. Two females and a few eggs were also found in the connective tissues. One male was found in a female uterus and two were apparently in the lumen of the nasal cavity but the surrounding tissues were disrupted. No male was identified in the lamina propria of the mucosa. However, significant inflammatory lesions occurred in the lamina propria, similar to those induced by the males of Anatrichosoma spp. which live in this part of the mucosa. In rodents, the lesions resulted in rhinosinusitis characterised by a lymphocytic infiltration leading to nasal obstruction.     

Effects of photoperiod on the reproductive condition of Nile grass rats (Arvicanthis niloticus) from an equatorial population

We evaluated the effects of photoperiod on the reproductive condition of male and female Nile grass rats (Arvicanthis niloticus) descended from members of an equatorial population trapped 2°S of the equator. Study animals housed in 12:12 light:dark (LD) cycles were transferred either to short photoperiod (9:15) or long photoperiod (15:9) for 9 weeks (males) or 11 weeks (females), and various reproductive parameters were assessed. We observed no differences between short‐ and long‐day males with respect to plasma concentration of testosterone, testicular mass, seminal vesicle mass, or spermatogenesis. Similarly, we observed no differences between short‐ and long‐day females with respect to oestrous cycles, uterine mass, follicle size, or presence of corpora lutea. Reproductive parameters of male and female A. niloticus housed in short‐ and long photoperiods were similar to those typically observed among animals descended from the same equatorial population and housed in LD 12:12. Thus, photoperiod appears not to elicit changes in reproductive condition among A. niloticus from populations whose native habitat lies within 2° of the equator. These data contrast with the results of other studies indicating that photoperiod alters reproductive condition in A. niloticus populations living >10° from the equator.     

Mitochondrial and Nuclear Genes-Based Phylogeography of Arvicanthis niloticus (Murinae) and Sub-Saharan Open Habitats Pleistocene History

A phylogeographic study was conducted on the Nile grass rat, Arvicanthis niloticus, a rodent species that is tightly associated with open grasslands from the Sudano-Sahelian regions. Using one mitochondrial (cytochrome b) and one nuclear (intron 7 of Beta Fibrinogen) gene, robust patterns were retrieved that clearly show that (i) the species originated in East Africa concomitantly with expanding grasslands some 2 Ma, and (ii) four parapatric and genetically well-defined lineages differentiated essentially from East to West following Pleistocene bioclimatic cycles. This strongly points towards allopatric genetic divergence within savannah refuges during humid episodes, then dispersal during arid ones; secondary contact zones would have then stabilized around geographic barriers, namely, Niger River and Lake Chad basins. Our results pertinently add to those obtained for several other African rodent as well as non-rodent species that inhabit forests, humid zones, savannahs and deserts, all studies that now allow one to depict a more comprehensive picture of the Pleistocene history of the continent south of the Sahara. In particular, although their precise location remains to be determined, at least three Pleistocene refuges are identified within the West and Central African savannah biome.