ABSTRACT
Although diurnality is widespread across Lepidoptera and has evolved many times independently, its causes and ecological implications are yet poorly understood. The "Salient Aroma Hypothesis" (SAH) postulates that diurnal insect herbivores are overall more specialized in dietary breadth than species active at night. It is furthermore assumed that diurnality evolved more frequently in species that live in cooler environments. Using European geometrid moths as a model group, we tested whether diurnal activity in adults is associated with an increased larval dietary breadth as predicted by the SAH. We further investigated whether species that exclusively occur in colder regions or whose flight period is restricted to cool seasons are more likely to exhibit a diurnal flight activity. Contrary to expectation, we found no consistent differences in larval dietary breadth between diurnal and nocturnal species, and thus no support for the SAH. Diurnal activity occurred more frequently in species restricted to cold regions but not in species restricted to cool seasons. We conclude that diurnality could serve as an advantageous adaptation in cold environments, depending on further factors such as resource availability or predation pressure, but has no immediate consequences for larval dietary breadth.
Subject(s)
Diet , Larva , Moths , Animals , Moths/physiology , Larva/physiology , Circadian Rhythm , Flight, Animal , Seasons , Odorants/analysisABSTRACT
We used thermal imagining and heat balance modelling to examine the thermal ecology of wild mammals, using the diurnal marsupial numbat (Myrmecobius fasciatus) as a model. Body surface temperature was measured using infra-red thermography at environmental wet and dry bulb temperatures of 11.7-29°C and 16.4-49.3°C, respectively; surface temperature varied for different body parts and with environmental temperature. Radiative and convective heat exchange varied markedly with environmental conditions and for various body surfaces reflecting their shapes, surface areas and projected areas. Both the anterior and posterior dorsolateral body areas functioned as thermal windows. Numbats in the shade had lower rates of solar radiative heat gain but non-solar avenues for radiative heat gain were substantial. Radiative gain was higher for black and lower for white stripes, but overall, the stripes had no thermal role. Total heat gain was generally positive (<4 to >20 W) and often greatly exceeded metabolic heat production (3-6 W). Our heat balance model indicates that high environmental heat loads limit foraging in open areas to as little as 10 min and that climate change may extend periods of inactivity, with implications for future conservation and management. We conclude that non-invasive thermal imaging is informative for modelling heat balance of free-living mammals.
Subject(s)
Marsupialia , Animals , Marsupialia/metabolism , Body Temperature Regulation , Hot Temperature , Body Temperature , MammalsABSTRACT
Wolves have been the archetype of wildlife persecution by humans for centuries all over the world, and still are heavily persecuted in some regions. Facultative diurnal/nocturnal wild mammals are known to become more nocturnal when persecuted. Conversely, little is known regarding the possibility of wolves becoming more diurnal if not persecuted. We took advantage of a 9-year natural experiment of restricted human access to a restored coal mine debris dump to study the daily activity patterns of wolves under conditions of infrequent human presence. Results were compared with a paired control site with frequent human use. Circadian wolf activity was monitored using camera traps (3 years in human-restricted site; 2 years in control). Additionally, data from two GPS-GSM-collared wolves monitored in a second control site were also analyzed. In our control sites, wolves were nearly inactive during daylight hours. In contrast, in the human-restricted site wolves extended their activity toward noon, with a daily activity peak between 10:00 and 12:00, and showed some activity throughout the entire circadian 2-h interval cycle considered. Wolves clearly had higher diurnality in the human-restricted area with 78% greater incidence of capture with remote cameras during the day than in the control site. We suggest that the shift toward increased diurnality was related to the loss of fear of humans. Evidence in support of this hypothesis comes from flight initiation distance (FID) data. Wolves showed relatively short FIDs when faced with a human observer (range 70-183 m) in broad daylight at the human-restricted site, but were so afraid of humans in the control site that we were unable to conduct FID trials there. Based on these results, we suggest that wolves may increase their diurnality in those European countries with currently increasing movement of human populations from rural to urban areas and that do not conduct lethal control of wolves. This would represent a historical landmark for a species that has been persecuted for many centuries. However, such behavioral shifts could bring new human-wolf conflicts that would require new policies.
ABSTRACT
Patterns of diel activity-how animals allocate their activity throughout the 24-h daily cycle-play key roles in shaping the internal physiology of an animal and its relationship with the external environment.1,2,3,4,5 Although shifts in diel activity patterns have occurred numerous times over the course of vertebrate evolution,6 the genomic correlates of such transitions remain unknown. Here, we use the African striped mouse (Rhabdomys pumilio), a species that transitioned from the ancestrally nocturnal diel niche of its close relatives to a diurnal one,7,8,9,10,11 to define patterns of naturally occurring molecular variation in diel niche traits. First, to facilitate genomic analyses, we generate a chromosome-level genome assembly of the striped mouse. Next, using transcriptomics, we show that the switch to daytime activity in this species is associated with a realignment of daily rhythms in peripheral tissues with respect to the light:dark cycle and the central circadian clock. To uncover selection pressures associated with this temporal niche shift, we perform comparative genomic analyses with closely related rodent species and find evidence of relaxation of purifying selection on striped mouse genes in the rod phototransduction pathway. In agreement with this, electroretinogram measurements demonstrate that striped mice have functional differences in dim-light visual responses compared with nocturnal rodents. Taken together, our results show that striped mice have undergone a drastic change in circadian organization and provide evidence that the visual system has been a major target of selection as this species transitioned to a novel temporal niche.
Subject(s)
Circadian Clocks , Circadian Rhythm , Mice , Animals , Circadian Rhythm/genetics , Rodentia/genetics , Photoperiod , GenomicsABSTRACT
Several wild rodents, such as the subterranean tuco-tucos (Ctenomys famosus), switch their time of activity from diurnal to nocturnal when they are transferred from field to the laboratory. Nevertheless, in most studies, different methods to measure activity in each of these conditions were used, which raised the question of whether the detected change in activity timing could be an artifact. Because locomotor activity and body temperature (Tb) rhythms in rodents are tightly synchronized and because abdominal Tb loggers can provide continuous measurements across field and laboratory, we monitored Tb as a proxy of activity in tuco-tucos transferred from a semi-field enclosure to constant lab conditions. In the first stage of this study ("Tb-only group," 2012-2016), we verified high incidence (55%, n = 20) of arrhythmicity, with no consistent diurnal Tb rhythms in tuco-tucos maintained under semi-field conditions. Because these results were discrepant from subsequent findings using miniature accelerometers (portable activity loggers), which showed diurnal activity patterns in natural conditions (n = 10, "Activity-only group," 2016-2017), we also investigated, in the present study, whether the tight association between activity and Tb would be sustained outside the lab. To verify this, we measured activity and Tb simultaneously across laboratory and semi-field deploying both accelerometers and Tb loggers to each animal. These measurements (n = 11, "Tb + activity group," 2019-2022) confirmed diurnality of locomotor activity and revealed an unexpected loosening of the temporal association between Tb and activity rhythms in the field enclosures, which is otherwise robustly tight in the laboratory.
Subject(s)
Body Temperature , Circadian Rhythm , Animals , Rodentia , LocomotionABSTRACT
(1) Background: Bank voles (Clethrionomys glareolus) and Apodemus mice are of exceptional importance as prey for predators in temperate mixed forests. We hypothesized that overall prey availability would increase linearly with prey frequency, and that the daylight hours, which are considered particularly dangerous, would be used only during seasonal rodent population peaks and only in the twilight hours. (2) Methods: We conducted a two-year camera-trapping study in an inner alpine mixed forest and collected 19,138 1 min videos in 215 camera-trap nights. Prey availability was defined as the pseudo-replication-limited maximum number of the respective rodent taxon per 30 min period, summed per season. (3) Results: Overall prey availability increased with frequency, i.e., the maximum number of rodent individuals per camera-trap night. Seasonally, Apodemus mice were particularly available to predators in the summer and bank voles in the autumn after a tree mast year. In both cases, this was accompanied by a significant increase in diurnal availability. During the population peak of Apodemus mice, the nocturnal availability of bank voles decreased without a concurrent increase in absolute diurnal availability, even though the significant relative shift to diurnal activity superficially suggested this. Bank voles were active throughout the day, while Apodemus mice were nocturnal and (rarely) crepuscular. (4) Conclusions: Availability of rodents to predators, especially during daylight hours, was mainly dependent on their tree mast-induced increased frequencies. Bank voles likewise responded strongly to interspecific competition with the larger and aggressive Apodemus mice, which negatively affected availability to predators. At our seasonal level of evaluation, we conclude that nycthemeral availability of forest-dwelling rodents to generalist predators of temperate mixed forests is predominantly driven by bottom-up mechanisms.
ABSTRACT
Modern lifestyle reduces environmental rhythmicity and may lead to circadian desynchrony. We are exposed to poor day-time lighting indoors and excessive night-time artificial light. We use air-conditioning to reduce ambient temperature cycle, and food is regularly available at all times. These disruptions of daily rhythms may lead to type 2 diabetes mellitus (T2DM), obesity, cardiometabolic diseases (CMD), depression and anxiety, all of which impose major public health and economic burden on societies. Therefore, we need appropriate animal models to gain a better understanding of their etiologic mechanisms, prevention, and management.We argue that the fat sand rat (Psammomys obesus), a diurnal animal model, is most suitable for studying the effects of modern-life conditions. Numerous attributes make it an excellent model to study human health disorders including T2DM, CMD, depression and anxiety. Here we review a comprehensive series of studies we and others conducted, utilizing the fat sand rat to study the underlying interactions between biological rhythms and health. Understanding these interactions will help deciphering the biological basis of these diseases, which often occur concurrently. We found that when kept in the laboratory (compared with natural and semi-wild outdoors conditions where they are diurnal), fat sand rats show low amplitude, nocturnal or arrhythmic activity patterns, dampened daily glucose rhythm, glucose intolerance, obesity and decreased survival rates. Short photoperiod acclimation exacerbates these pathologies and further dampens behavioral and molecular daily rhythms, resulting in CMD, T2DM, obesity, adipocyte dysfunction, cataracts, depression and anxiety. Increasing environmental rhythmicity by morning bright light exposure or by access to running wheels strengthens daily rhythms, and results in higher peak-to-trough difference in activity, better rhythmicity in clock genes expression, lower blood glucose and insulin levels, improved glucose tolerance, lower body and heart weight, and lower anxiety and depression. In summary, we have demonstrated that fat sand rats living under the correspondent of "human modern lifestyle" conditions exhibit dampened behavioral and biological rhythms and develop circadian desynchrony, which leads to what we have named "The Circadian Syndrome". Environmental manipulations that increase rhythmicity result in improvement or prevention of these pathologies. Similar interventions in human subjects could have the same positive results and further research on this should be undertaken.
ABSTRACT
In both diurnal and nocturnal mammals, the timing of activity is regulated by the central circadian clock of the suprachiasmatic nucleus (SCN). The SCN is synchronized to the external light cycle via the retinohypothalamic tract (RHT). To investigate potential differences in light processing between nocturnal mice and the diurnal rodent Rhabdomys pumilio, we mimicked retinal input by stimulation of the RHT ex vivo. Using Ca2+ imaging, we observed excitations as well as inhibitions of SCN neurons in response to electrical RHT stimulation. In mice, the vast majority of responses were excitatory (85%), whereas in Rhabdomys, the proportion of excitatory and inhibitory responses was similar (51% excitatory, 49% inhibitory). Glutamate blockers AP5 and CNQX blocked the excitatory responses to RHT stimulation but did not abolish the inhibitory responses in mice or Rhabdomys, indicating that the inhibitions were monosynaptically transmitted via the RHT. Simultaneous application of glutamate blockers with the GABAA antagonist gabazine blocked all inhibitory responses in mice, but not in Rhabdomys. Collectively, our results indicate that in Rhabdomys, considerably more inhibitory responses to light are present and that these responses are driven directly by the RHT. We propose that this increased proportion of inhibitory input could reflect a difference in the entrainment mechanism employed by diurnal rodents.
Subject(s)
Circadian Clocks , Animals , Circadian Rhythm/physiology , Glutamates , Mice , Retina/physiology , Rodentia , Suprachiasmatic Nucleus/physiologyABSTRACT
Understanding the targets of selection associated with changes in behavioral traits represents an important challenge of current evolutionary research. Owls (Strigiformes) are a diverse group of birds, most of which are considered nocturnal raptors. However, a few owl species independently adopted a diurnal lifestyle in their recent evolutionary history. We searched for signals of accelerated rates of evolution associated with a diurnal lifestyle using a genome-wide comparative approach. We estimated substitution rates in coding and noncoding conserved regions of the genome of seven owl species, including three diurnal species. Substitution rates of the noncoding elements were more accelerated than those of protein-coding genes. We identified new, owl-specific conserved noncoding elements as candidates of parallel evolution during the emergence of diurnality in owls. Our results shed light on the molecular basis of adaptation to a new niche and highlight the importance of regulatory elements for evolutionary changes in behavior. These elements were often involved in the neuronal development of the brain.
Subject(s)
Strigiformes , Adaptation, Physiological/genetics , Animals , Genome , Genomics , Phenotype , Strigiformes/geneticsABSTRACT
The dromedary camel (Camelus dromedarius) is a large ungulate that copes well with the xeric environment of the desert. Its peculiar adaptation to heat and dehydration is well-known. However, its behavior and general activity is far from being completely understood. The present study was carried out to investigate the ecological effect of the various seasons on the locomotor activity (LA) rhythm and diurnal activity of this species. Six adult female camels were maintained under mesic semi-natural conditions of the environment during four periods of 10 days in each season: autumn, winter, spring and summer. In addition, three female camels were used to test the effect of rain on the LA rhythm during a period of 18 days during the winter. The animal's LA was recorded using the locomotion scoring method. Camels displayed a clear 24.0h LA rhythm throughout the four seasons. Activity was intense during Day-time (6-22 fold higher in comparison to night) and dropped or completely disappeared during nighttime. Mean daytime total activity was significantly higher in the summer as compared to winter. Regardless of the season, the active phase in camels coincided with the time of the photophase and thermophase. Furthermore, the daily duration of the time spent active was directly correlated to the seasonal changes of photoperiod. The diurnal activity remained unchanged over the four seasons. For each season, the start and the end of the active phase were synchronized with the onset of sunrise and sunset. At these time periods, temperature remained incredibly stable with a change ranging from 0.002 to 0.210°C; whereas, changes of light intensity were greater and faster with a change from 0.1 to 600 lux representing a variation of 3215-7192 fold in just 25-29 min. Rainfall affected the pattern of the LA rhythm with occurrence of abnormal nocturnal activity during nighttime disturbing nocturnal rest and sleep. Here we show that the dromedary camel exhibits significant seasonal changes of its activity within daylight hours. However, the diurnal pattern remains unchanged regardless of the season; whereas, abnormal nocturnal activity is observed during periods of rain. The activity onset and offset in this species seems to be primarily driven by the changes in light intensity at dusk and dawn.
Subject(s)
Camelus , Circadian Rhythm , Animals , Female , Locomotion , Photoperiod , SeasonsABSTRACT
Being active during the day requires a slow-closing ion channel that dampens the activity of neurons in a specific area of the brain.
Subject(s)
Circadian Rhythm , Suprachiasmatic Nucleus , Brain , NeuronsABSTRACT
Circadian rhythms in mammals are orchestrated by a central clock within the suprachiasmatic nuclei (SCN). Our understanding of the electrophysiological basis of SCN activity comes overwhelmingly from a small number of nocturnal rodent species, and the extent to which these are retained in day-active animals remains unclear. Here, we recorded the spontaneous and evoked electrical activity of single SCN neurons in the diurnal rodent Rhabdomys pumilio, and developed cutting-edge data assimilation and mathematical modeling approaches to uncover the underlying ionic mechanisms. As in nocturnal rodents, R. pumilio SCN neurons were more excited during daytime hours. By contrast, the evoked activity of R. pumilio neurons included a prominent suppressive response that is not present in the SCN of nocturnal rodents. Our modeling revealed and subsequent experiments confirmed transient subthreshold A-type potassium channels as the primary determinant of this response, and suggest a key role for this ionic mechanism in optimizing SCN function to accommodate R. pumilio's diurnal niche.
Subject(s)
Circadian Clocks/physiology , Muridae/physiology , Neurons/physiology , Suprachiasmatic Nucleus/physiology , AnimalsABSTRACT
BACKGROUND: Suicide is a public health problem, and the third major cause of death in Indian, black and mixed race groups. In whites suicide is the second cause of death. The patterns of suicide vary by time of day, day of the week, month of the year and seasons. As a result of limited and inaccurate data, these variations have not been fully examined in the developing world. This study investigated the diurnality and seasonality of suicide in peri-urban Pretoria, as opposed to studies conducted previously in the country's metropolitan. METHODS: A retrospective analysis of suicides recorded between 2007 and 2019 was undertaken. Data were extracted from the forensic pathology department's database (university mortuary). RESULTS: Of the 1515 cases of suicides examined, majority were black Africans (95.9%), male (83.9%), aged 21-40 years (50.5%). Hanging was the most common method of suicide irrespective of demographics (72.8%). Diurnal suicide variations were distinct for men and women, occurring at (16:00-20:00) and (08:00-12:00), respectively. Suicide peaked on days preceding and after the weekend (Mondays and Fridays) and in warmer seasons (summer and spring)Conclusion: The overall patterns of suicide in peri-urban Pretoria, mimic local and global trends with regard to methods, demographics and temporal characteristics. The underlying mechanism for these trends is unclear requiring in-depth investigation in order to develop appropriate interventions.
Subject(s)
Suicide , Female , Humans , Male , Racial Groups , Retrospective Studies , Seasons , South AfricaABSTRACT
In recent years, there has been an increase in the descriptions of members of the lizard genus Lepidophyma. Herein, we describe a new species of Lepidophyma from the Huasteca Potosina region of Mexico, previously confused with L. gaigeae, from which it differs in lacking parietal spot, among other characteristics. We inferred its phylogenetic position and provide information on its thermal and hydric physiology, as well as on some other aspects of natural history. Molecular and morphological data supported the independent taxonomic status of the new species, indicating its placement as the sister taxon of L. gaigeae and a wide morphological separation between these species. Lepidophyma lusca sp. nov. has a diurnal-crepuscular activity period and occurs at lower elevations than L. gaigeae. Also, the new species differ from its sister taxon in its physiology, as reflected by its tendency toward higher thermal parameters and water loss rates. With the description of L. lusca sp. nov., the number of species in the genus Lepidophyma rises to 21.
Subject(s)
Lizards , Animals , Lizards/genetics , Mexico , PhylogenyABSTRACT
Eye blinking is an essential maintenance behaviour for many terrestrial animals, but is also a risky behaviour as the animal is unable to scan the environment and detect hazards while its eyes are temporarily closed. It is therefore likely that the length of time that the eyes are closed and the length of the gap between blinks for a species may reflect aspects of the ecology of that species, such as its social or physical environment. An earlier published study conducted a comparative study linking blinking behaviour and ecology, and detailed a dataset describing the blinking behaviour of a large number of primate species that was collected from captive animals, but the analysis presented did not control for the nonindependence of the data due to common evolutionary history. In the present study, the dataset is reanalysed using phylogenetic comparative methods, after reconsideration of the parameters describing the physical and social environments of the species. I find that blink rate is best described by the locomotion mode of a species, where species moving through arboreal environments blink least, ground-living species blink most, and species that use both environments show intermediate rates. The duration of a blink was also related to locomotion mode, and positively correlated with both mean species group size and mean species body mass, although the increase in relation to group size is small. How a species moves through the environment therefore appears to be important for determining blinking behaviour, and suggests that complex arboreal environments may require less interruption to visual attention. Given that the data were collected with captive individuals, caution is recommended for interpreting the correlations found.
ABSTRACT
Several studies have reported activity patterns of various diurnal species from the order Rodentia, in which most of the species are nocturnal. Most of these studies have been performed under controlled laboratory conditions. These studies found that most of these species change their activity patterns when held under laboratory conditions, have a diverse masking response to light, and their activity pattern is influenced by the presence of a running wheel. Squirrels are reported to be strictly diurnal both in the field as well as in laboratory settings, and, therefore, form an interesting species to study to better understand the switch to diurnality. The aim of the current study is to characterize the masking response and temporal organization of wheel-running activity rhythms in the palm squirrel, Funambulus pennantii, under semi-natural (NLD) and controlled laboratory conditions using different lighting schedules. Squirrels were housed individually in a resting cage with running wheel under NLD (n = 10) and squared 12:12 h of light-dark cycle (LD) (n = 20). After stable entrainment under the LD condition, squirrels were divided into two groups. One group was housed under constant darkness (DD) (n = 10) and another group under constant light (LL) (n = 10). Following the stable free-running rhythm under DD and LL, the LD condition was reinforced. The kinetics of the endogenous pacemaker was studied following a 6 h phase advance or delay of LD cycle. Further, palm squirrels were subjected to a 3.5: 3.5 h LD cycle to evaluate the masking response to light and dark. Squirrels demonstrated stable, clear, robust, and strict diurnal activity rhythm during NLD and LD. In DD and LL, F. pennantii free-ran from the phase of the previous LD cycle, and the free-running period was longer in LL than in DD. The percentage of activity during the light phase was significantly higher in NLD and LD (above 96%) compared to activity during the subjective day in the DD and LL conditions (above 91%). The alpha/rho ratio was significantly higher in the LL compared to other lighting schedules. Further, all ten squirrels re-entrained to both 6 h advance and delay shifts within 11 days. In the ultradian cycle, significant positive masking of light was evident in nine of ten squirrels. These results suggest that the: (i) circadian system of F. pennantii is stable and functional under various lighting conditions; (ii) basic temporal organization in activity pattern remained unaltered even in the presence of a running wheel; (iii) diurnality is the inherent trait of F. pennantii, and (iv) behavioral activity rhythms are governed by both the circadian clock and external masking. Thus, palm squirrels can be used as a suitable diurnal model in circadian biology to study the underlying mechanisms of diurnality and effects of different light schedules, wavelengths, and non-photic cues on physiological and behavioral parameters.
Subject(s)
Circadian Clocks , Circadian Rhythm , Animals , Darkness , Motor Activity , Photoperiod , SciuridaeABSTRACT
An animal's temporal niche - the time of day at which it is active - is known to drive a variety of adaptations in the visual system. These include variations in the topography, spectral sensitivity and density of retinal photoreceptors, and changes in the eye's gross anatomy and spectral transmission characteristics. We have characterised visual spectral sensitivity in the murid rodent Rhabdomys pumilio (the four-striped grass mouse), which is in the same family as (nocturnal) mice and rats but exhibits a strong diurnal niche. As is common in diurnal species, the R. pumilio lens acts as a long-pass spectral filter, providing limited transmission of light <400â nm. Conversely, we found strong sequence homologies with the R. pumilio SWS and MWS opsins and those of related nocturnal species (mice and rats) whose SWS opsins are maximally sensitive in the near-UV. We continued to assess in vivo spectral sensitivity of cone vision using electroretinography and multi-channel recordings from the visual thalamus. These revealed that responses across the human visible range could be adequately described by those of a single pigment (assumed to be MWS opsin) maximally sensitive at â¼500â nm, but that sensitivity in the near-UV required inclusion of a second pigment whose peak sensitivity lay well into the UV range (λmax<400â nm, probably â¼360â nm). We therefore conclude that, despite the UV-filtering effects of the lens, R. pumilio retains an SWS pigment with a UV-A λmax In effect, this somewhat paradoxical combination of long-pass lens and UV-A λmax results in narrow-band sensitivity for SWS cone pathways in the UV-A range.
Subject(s)
Retinal Cone Photoreceptor Cells , Vision, Ocular , Animals , Mice , Opsins , Photoreceptor Cells, Vertebrate , Rats , Rod OpsinsABSTRACT
Humans, as super predators, can have strong effects on wildlife behaviour, including profound modifications of diel activity patterns. Subsequent to the return of large carnivores to human-modified ecosystems, many prey species have adjusted their spatial behaviour to the contrasting landscapes of fear generated by both their natural predators and anthropogenic pressures. The effects of predation risk on temporal shifts in diel activity of prey, however, remain largely unexplored in human-dominated landscapes. We investigated the influence of the density of lynx Lynx lynx, a nocturnal predator, on the diel activity patterns of their main prey, the roe deer Capreolus capreolus, across a gradient of human disturbance and hunting at the European scale. Based on 11 million activity records from 431 individually GPS-monitored roe deer in 12 populations within the EURODEER network (http://eurodeer.org), we investigated how lynx predation risk in combination with both lethal and non-lethal human activities affected the diurnality of deer. We demonstrated marked plasticity in roe deer diel activity patterns in response to spatio-temporal variations in risk, mostly due to human activities. In particular, roe deer decreased their level of diurnality by a factor of 1.37 when the background level of general human disturbance was high. Hunting exacerbated this effect, as during the hunting season deer switched most of their activity to night-time and, to a lesser extent, to dawn, although this pattern varied noticeably in relation to lynx density. Indeed, in the presence of lynx, their main natural predator, roe deer were relatively more diurnal. Overall, our results revealed a strong influence of human activities and the presence of lynx on diel shifts in roe deer activity. In the context of the recovery of large carnivores across Europe, we provide important insights about the effects of predators on the behavioural responses of their prey in human-dominated ecosystems. Modifications in the temporal partitioning of ungulate activity as a response to human activities may facilitate human-wildlife coexistence, but likely also have knock-on effects for predator-prey interactions, with cascading effects on ecosystem functioning.
Résumé Les humains, en tant que 'super-prédateurs', peuvent avoir des effets importants sur le comportement de la faune sauvage, y compris des modifications profondes de leurs rythmes circadiens d'activité. A la suite du retour des grands carnivores dans les écosystèmes anthropisés, de nombreuses espèces proies ont ajusté leur comportement spatial à ces paysages de la peur contrastés, générés à la fois par les pressions liées aux risques anthropiques et à la présence de leurs prédateurs naturels. Les effets du risque de prédation sur les modifications temporelles des rythmes circadiens d'activité des proies restent cependant largement inconnus dans les écosystèmes dominés par l'homme. Ici, nous avons étudié l'influence de la densité de lynx Lynx lynx, un prédateur nocturne, sur les rythmes circadiens d'activité de leur proie principale, le chevreuil Capreolus capreolus, à travers un gradient de pressions anthropiques à l'échelle Européenne. Sur la base de plus de 11 million de données d'activité issues de 431 suivis individuels de chevreuils équipés de colliers GPS provenant de 12 populations au sein du réseau EURODEER (http://eurodeer.org), nous avons analysé comment le risque de prédation par le lynx, associé aux risques létaux et non-létaux des activités humaines, influence la diurnalité des chevreuils. Nous avons démontré une forte plasticité des rythmes circadiens d'activité des chevreuils en réponse aux variations spatio-temporelles du risque, et notamment face aux activités humaines. Plus particulièrement, les chevreuils diminuent leur degré de diurnalité d'un facteur de 1.37 lorsque le dérangement humain est important. La chasse accentue cet effet, puisque durant la saison de chasse les chevreuils basculent la plupart de leur activité de nuit, et dans une moindre mesure, durant l'aube également, bien que ce patron soit essentiellement variable en fonction de la densité de lynx. En effet, en présence de lynx, leur principal prédateur, les chevreuils sont relativement plus diurnes. Globalement, nos résultats révèlent une forte influence des activités humaines et de la présence de lynx sur l'ajustement des rythmes circadiens d'activité des chevreuils. Dans le contexte du retour des grands carnivores en Europe, notre étude apporte de nouvelles connaissances sur les effets des prédateurs sur la réponse comportementale de leur proie dans des écosystèmes anthropisés. La modification de la répartition temporelle de l'activité des ongulés en réponse aux activités humaines pourrait être un facteur facilitant la coexistence homme-faune sauvage, avec toutefois des conséquences autres sur les interactions prédateurs-proies et leurs effets en cascade sur le fonctionnement des écosystèmes.
Subject(s)
Deer , Lynx , Animals , Ecosystem , Europe , Fear , Humans , Predatory BehaviorABSTRACT
The temporal niche that an animal occupies includes a coordinated suite of behavioral and physiological processes that set diurnal and nocturnal animals apart. The daily rhythms of the two chronotypes are regulated by both the circadian system and direct responses to light, a process called masking. Here we review the literature on circadian regulations and masking responses in diurnal mammals, focusing on our work using the diurnal Nile grass rat (Arvicanthis niloticus) and comparing our findings with those derived from other diurnal and nocturnal models. There are certainly similarities between the circadian systems of diurnal and nocturnal mammals, especially in the phase and functioning of the principal circadian oscillator within the hypothalamic suprachiasmatic nucleus (SCN). However, the downstream pathways, direct or indirect from the SCN, lead to drastic differences in the phase of extra-SCN oscillators, with most showing a complete reversal from the phase seen in nocturnal species. This reversal, however, is not universal and in some cases the phases of extra-SCN oscillators are only a few hours apart between diurnal and nocturnal species. The behavioral masking responses in general are opposite between diurnal and nocturnal species, and are matched by differential responses to light and dark in several retinorecipient sites in their brain. The available anatomical and functional data suggest that diurnal brains are not simply a phase-reversed version of nocturnal ones, and work with diurnal models contribute significantly to a better understanding of the circadian and photic modulation of daily rhythms in our own diurnal species.
Subject(s)
Circadian Rhythm , Suprachiasmatic Nucleus , Animals , Brain , Murinae , RatsABSTRACT
The circadian system regulates daily rhythms of physiology and behavior. Although extraordinary advances have been made to elucidate the brain mechanisms underlying the circadian system in nocturnal species, less is known in diurnal species. Recent studies have shown that retinorecipient brain areas such as the intergeniculate leaflet (IGL) and olivary pretectal nucleus (OPT) are critical for the display of normal patterns of daily activity in diurnal grass rats (Arvicanthis niloticus). Specifically, grass rats with IGL and OPT lesions respond to light in similar ways to intact nocturnal animals. Importantly, both the IGL and OPT project to one another in nocturnal species, and there is evidence that these 2 brain regions also project to the superior colliculus (SC). The SC receives direct retinal input, is involved in the triggering of rapid eye movement sleep in nocturnal rats, and is disproportionately large in the diurnal grass rat. The objective of the current study was to use diurnal grass rats to test the hypothesis that the SC is critical for the expression of diurnal behavior and physiology. We performed bilateral electrolytic lesions of the SC in female grass rats to examine behavioral patterns and acute responses to light. Most grass rats with SC lesions expressed significantly reduced activity in the presence of light. Exposing these grass rats to constant darkness reinstated activity levels during the subjective day, suggesting that light masks their ability to display a diurnal activity profile in 12:12 LD. Altogether, our data suggest that the SC is critical for maintaining normal responses to light in female grass rats.