The costs of becoming nocturnal: feeding efficiency in relation to light intensity in juvenile Atlantic Salmon

1. Most animals are active by day or by night, but not both; juvenile salmonids are unusual in that they switch from being predominantly diurnal for most of the year to being nocturnal in winter. They are visual foragers, and adaptations for high visual acuity at daytime light intensities are generally incompatible with sensitive night vision. Here we test whether juvenile Atlantic Salmon Salmo salar are able to maintain their efficiency of prey capture when switching between diurnal and nocturnal foraging.
2. By testing the ability of the fish to acquire drifting food items under a range of manipulated light intensities, we show that the foraging efficiency of juvenile salmon is high at light intensities down to those equivalent to dawn or dusk, but drops markedly at lower levels of illumination: even under the best night condition (full moon and clear sky), the feeding efficiency is only 35% of their diurnal efficiency, and fish will usually be feeding at less than 10% (whenever the moon is not full, skies are overcast or when in the shade of bankside trees). Fish were unable to feed on drifting prey when in complete darkness.
3. The ability of juvenile salmon to detect prey under different light intensities is similar to that of other planktivorous or drift-feeding species of fish; they thus appear to have no special adaptations for nocturnal foraging.
4. While winter drift abundance is slightly higher by night than by day, the difference is not enough to compensate for the loss in foraging efficiency. We suggest that juvenile salmon can nonetheless switch to nocturnal foraging in winter because their food requirements are low, many individuals adopting a strategy in which intake is suppressed to the minimum that ensures survival.     

Light masking in the field: an experiment with nocturnal and diurnal spiny mice under semi-natural field conditions

Light masking has been studied almost exclusively in the laboratory. The authors populated four field enclosures with locally coexisting nocturnal Acomys cahirinus and diurnal A. russatus, and monitored their body temperatures (T(b)) using implanted temperature-sensitive radio transmitters. A 3-h light pulse was initiated at the beginning of two consecutive nights; preceding nights were controls. A. cahirinus T(b) and calculated activity levels decreased significantly during the light pulse, demonstrating a negative light masking response (light effect on T(b): -0.32 °C?±?0.15 °C; average calculated activity records during the light pulse: 7?±?1.53, control: 9.8?±?1.62). Diurnal A. russatus did not respond to the light pulse. We conclude that light masking is not an artifact of laboratory conditions but represents a natural adaptive response in free-living populations.     

Do house mice modify their foraging behaviour in response to predator odours and habitat?

Predator odours and habitat structure are thought to influence the behaviour of small mammalian prey, which use them as cues to reduce risks of predation. We tested this general hypothesis for house mice, Mus domesticus, by manipulating fox odour density via addition of fox scats and habitat via patchy mowing of vegetation, for populations in 15 × 15-m field enclosures. Using giving-up densities (GUDs), the density of food remaining when an animal quits harvesting a patch, we measured foraging behaviours in response to these treatments. Mice consistently avoided open areas, leaving GUDs two to four times greater in these areas than in densely vegetated patches. However, mouse GUDs did not change in response to the addition of fox scats, even immediately after fresh scats were added. There was no interaction between fox odour and habitat use. We then tested whether habituation to fox odours had occurred, by comparing the individual responses to scats of eight mice born into enclosures with fox scats to those of eight mice born into scat-free enclosures and five wild mice. In smaller enclosures, GUDs of trays with scats did not differ from GUDs of trays without scats for any treatment. We conclude that exposure to high levels of fox odours did not alter the foraging behaviour of mice, but that mice did reduce foraging in areas where habitat was removed, perceiving predation risk to be greater in these areas than controls. We suggest further that studies using the ‘scat-at-trap’ technique, which have shown avoidance of predator odours by mice and other small mammals, may overestimate the general avoidance of predator odours by free-living prey, which must forage with a constant background of predator odours.     

Biophysical modeling of the temporal niche: from first principles to the evolution of activity patterns

Most mammals can be characterized as nocturnal or diurnal. However infrequently, species may overcome evolutionary constraints and alter their activity patterns. We modeled the fundamental temporal niche of a diurnal desert rodent, the golden spiny mouse, Acomys russatus. This species can shift into nocturnal activity in the absence of its congener, the common spiny mouse, Acomys cahirinus, suggesting that it was competitively driven into diurnality and that this shift in a small desert rodent may involve physiological costs. Therefore, we compared metabolic costs of diurnal versus nocturnal activity using a biophysical model to evaluate the preferred temporal niche of this species. The model predicted that energy expenditure during foraging is almost always lower during the day except during midday in summer at the less sheltered microhabitat. We also found that a shift in summer to foraging in less sheltered microhabitats in response to predation pressure and food availability involves a significant physiological cost moderated by midday reduction in activity. Thus, adaptation to diurnality may reflect the "ghost of competition past"; climate-driven diurnality is an alternative but less likely hypothesis. While climate is considered to play a major role in the physiology and evolution of mammals, this is the first study to model its potential to affect the evolution of activity patterns of mammals.     

Seasonal thermogenic acclimation of diurnally and nocturnally active desert spiny mice

Diurnally active golden spiny mice (Acomys russatus) and nocturnal common spiny mice (Acomys cahirinus) coexist in hot rocky deserts of Israel. Diurnal and nocturnal activities expose these species to different climatic conditions. Nonshivering thermogenesis (NST) capacity of individuals of both species immediately upon removal from the field exhibited seasonal changes, with no significant interspecific difference. Colony-reared mice of either species transferred in the laboratory from long to short photoperiod increased NST capacity, though to a lesser extent than observed in the seasonal acclimatization. The underlying biochemical mechanisms of short photoperiod acclimation differed between the species. In both Cytochrome-c oxidase (Cox) activity was higher in short as compared to long photoperiod. In short-photoperiod-acclimated A. cahirinus uncoupling protein (UCP) content in brown adipose tissue (BAT) was significantly higher than in long photoperiod, while in A. russatus there was no significant change. In A. russatus there was a significant increase in lipoprotein lipase (LPL) activity in BAT in short-photoperiod-acclimated individuals, while in A. cahirinus LPL activity was high under both acclimations. The low LPL activity in brown adipose tissue of desert-adapted A. russatus may facilitate lipid uptake in white adipose tissue, an advantage in desert conditions where food is scarce and irregularly distributed in space and time.     

Examining the Role of Cuticular Hydrocarbons in Firefly Species Recognition

During animal courtship, multiple signals transmitted in different sensory modalities may be used to recognize potential mates. In fireflies (Coleoptera: Lampyridae), nocturnally active species rely on long-range bioluminescent signals for species, sex, and mate recognition, while several diurnally active species rely on pheromonal signals. Although in many insects non-volatile cuticular hydrocarbons (CHC) also function in species and sex discrimination, little is known about the potential role of CHC in fireflies. Here, we used gas chromatography to characterize species and sex differences in the CHC profiles of several North American fireflies, including three nocturnal and two diurnal species. Additionally, we conducted behavioral bioassays to determine whether firefly males (the searching sex) were differentially attracted to extracts from conspecific vs. heterospecific females. Gas chromatography revealed that nocturnal Photinus fireflies had low or undetectable CHC levels in both sexes, while diurnal fireflies showed higher CHC levels. No major sex differences in CHC profiles were observed for any firefly species. Behavioral bioassays demonstrated that males of the diurnal firefly Ellychnia corrusca were preferentially attracted to chemical extracts from conspecific vs. heterospecific females, while males of the remaining species showed no discrimination. These results suggest that while CHC may function as species recognition signals for some diurnal fireflies, these compounds are unlikely to be important contact signals in nocturnal Photinus fireflies.     

Temporal partitioning among diurnally and nocturnally active desert spiny mice: energy and water turnover costs

Nocturnal Acomys cahirinus and diurnally active A. russatus coexist in hot rocky deserts. Diurnal and nocturnal activity exposes them to different climatic challenges. A doubly-labelled water field study revealed no significant differences in water turnover between the species at all seasons, reflecting the adaptations of A. russatus to water conservation. In summers the energy expenditure of A. russatus tended to be higher than that of A. cahirinus. Energy requirements of A. cahirinus in winter are double than that of A. russatus, and may reflect the cost of thermoregulating during cold nights.     

Daily scheduling of the golden spiny mouse under photoperiodic and social cues.

A most important function of the circadian system is to ensure that behaviors and metabolism are appropriately timed with respect to the light/dark cycle and photoperiod. Ecological constraints can perturb the daily schedules; would they also impair photoperiodic adaptations? A natural model exists in the golden spiny mouse (Acomys russatus), which is nocturnal, but driven into diurnal activity when sharing the habitat with its congener, A. cahirinus. We show here that the presence of A. cahirinus alters the diurnal rhythms of body temperature and urine volume, delays excretion of the major melatonin metabolite, 6-sulfatoxymelatonin (6-SMT), and increases 2-deoxyglucose uptake by the suprachiasmatic nuclei in A. russatus. Nevertheless, a clear photoperiod effect on urine volume and 6-SMT rhythms was observed. These results indicate that the circadian system can adapt to major changes in daily scheduling without impairing daylength measurement, and consequently seasonal adaptation.     

The Effect of Moonlight on Scopoli's Shearwater Calonectris diomedea Colony Attendance Patterns and Nocturnal Foraging: A Test of the Foraging Efficiency Hypothesis

Moonlight is known to affect the nocturnal behaviour and activity rhythms of many organisms. For instance, predators active at night may take advantage from increased visibility afforded by the moon, while prey might regulate their activity patterns to become less detectable. Many species of pelagic seabirds attend their colony only at night, in complete darkness, avoiding approaching their nest sites under moonlight. This behaviour has been most often interpreted as an antipredator adaptation (‘predation avoidance’ hypothesis). However, it may also reflect a lower foraging efficiency during moonlit nights (‘foraging efficiency’ hypothesis). Indeed, moonlight may reduce prey availability because preferred seabird prey is known to occur at higher depths in moonlit nights. Using high‐accuracy behavioural information from data loggers, we investigated the effect of moonlight on colony attendance and at‐sea nocturnal foraging in breeding Scopoli's shearwaters Calonectris diomedea. We found that birds departing for self‐feeding trips around the full moon performed longer trips than those departing around the new moon. On nights when the moon was present only partly, nest burrow entrances took place largely in the moonless portion of the night. Moreover, contrary to predictions from the ‘foraging efficiency’ hypothesis, nocturnal foraging activity increased according to moonlight intensity, suggesting that birds increased their foraging activity when prey became more detectable. This study strengthens the idea that colony attendance behaviour is strictly controlled by moonlight in shearwaters, which is possibly related to the perception of a predation risk.     

Temporal structure of an ant community in semi-arid Australia

The activity of five seed-harvesting and ten non-harvesting species of ants was examined over a 2-year period. The ant community appeared to be stable in the long term, but there was considerable variability in the numbers and species of ants active at any one time, both on a seasonal and diel basis. Only four species were active throughout the year, with activity reduced in winter. Two species were consistently nocturnal, nine were mainly diurnal, and the remaining four species switched from diurnal to more nocturnal activity with increasing temperatures. The changes in the diurnal pattern and intensity of foraging activity were shown to be controlled by several climatic and biotic variables. These were classed as either ‘stimulatory-inhibitory’ which determined whether activity would occur or not, or ‘regulatory’, which set the physical limits to activity and controlled foraging intensity. Factors such as forage availability and colony satiation were placed in the first category, and soil temperature, moisture stress and light intensity were placed in the second. There was no simple response to the combination of variables, and individual species responded differently to the various factors. The resulting temporal separation probably reduces competitive interactions between species.     

The relationship between the golden spiny mouse circadian system and its diurnal activity: an experimental field enclosures and laboratory study

Examples of animals that switch activity times between nocturnality and diurnality in nature are relatively infrequent. Furthermore, the mechanism for switching activity time is not clear: does a complete inversion of the circadian system occur in conjunction with activity pattern? Are there switching centers downstream from the internal clock that interpret the clock differently? Or does the switch reflect a masking effect? Answering these key questions may shed light on the mechanisms regulating activity patterns and their evolution. The golden spiny mouse (Acomys russatus) can switch between nocturnal and diurnal activity. This study investigated the relationship between its internal circadian clock and its diurnal activity pattern observed in the field. The goal is to understand the mechanisms underlying species rhythm shifts in order to gain insight into the evolution of activity patterns. All golden spiny mice had opposite activity patterns in the field than those under controlled continuous dark conditions in the laboratory. Activity and body temperature patterns in the field were diurnal, while in the laboratory all individuals immediately showed a free-running rhythm starting with a nocturnal pattern. No phase transients were found toward the preferred nocturnal activity pattern, as would be expected in the case of true entrainment. Moreover, the fact that the free-running activity patterns began from the individuals' subjective night suggests that golden spiny mice are nocturnal and that their diurnality in their natural habitat in the field results from a change that is downstream to the internal clock or reflects a masking effect.     

Linking foraging decisions to residential yard bird composition

Urban bird communities have higher densities but lower diversity compared with wildlands. However, recent studies show that residential urban yards with native plantings have higher native bird diversity compared with yards with exotic vegetation. Here we tested whether landscape designs also affect bird foraging behavior. We estimated foraging decisions by measuring the giving-up densities (GUD; amount of food resources remaining when the final forager quits foraging on an artificial food patch, i.e seed trays) in residential yards in Phoenix, AZ, USA. We assessed how two yard designs (mesic: lush, exotic vegetation; xeric: drought-tolerant and native vegetation) differed in foraging costs. Further, we developed a statistical model to calculate GUDs for every species visiting the seed tray. Birds foraging in mesic yards depleted seed trays to a lower level (i.e. had lower GUDs) compared to birds foraging in xeric yards. After accounting for bird densities, the lower GUDs in mesic yards appeared largely driven by invasive and synanthropic species. Furthermore, behavioral responses of individual species were affected by yard design. Species visiting trays in both yard designs had lower GUDs in mesic yards. Differences in resource abundance (i.e., alternative resources more abundant and of higher quality in xeric yards) contributed to our results, while predation costs associated with foraging did not. By enhancing the GUD, a common method for assessing the costs associated with foraging, our statistical model provided insights into how individual species and bird densities influenced the GUD. These differences we found in foraging behavior were indicative of differences in habitat quality, and thus our study lends additional support for native landscapes to help reverse the loss of urban bird diversity.     

Individual,social, and environmental factors affecting salivary and fecal cortisol levels in captive pied tamarins (Saguinus bicolor)

Pied tamarins (Saguinus bicolor) are endangered New World primates, and in captivity appear to be very susceptible to stress. We measured cortisol in 214 saliva samples from 36 tamarins and in 227 fecal samples from 27 tamarins, and investigated the effects of age, sex, pregnancy, rearing history, social status, weight, group composition, and enclosure type using generalized linear mixed models. There was no effect of age on either fecal or salivary cortisol levels. Female pied tamarins in late pregnancy had higher fecal cortisol levels than those in early pregnancy, or nonpregnant females, but there was no effect of pregnancy on salivary cortisol. Females had higher salivary cortisol levels than males, but there was no effect of rearing history. However, for fecal cortisol, there was an interaction between sex and rearing history. Hand‐reared tamarins overall had higher fecal cortisol levels, but while male parent‐reared tamarins had higher levels than females who were parent‐reared, the reverse was true for hand‐reared individuals. There was a trend towards lower fecal cortisol levels in subordinate individuals, but no effect of status on salivary cortisol. Fecal but not salivary cortisol levels declined with increasing weight. We found little effect of group composition on cortisol levels in either saliva or feces, suggesting that as long as tamarins are housed socially, the nature of the group is of less importance. However, animals in off‐show enclosures had higher salivary and fecal cortisol levels than individuals housed on‐show. We suggest that large on‐show enclosures with permanent access to off‐exhibit areas may compensate for the effects of visitor disturbance, and a larger number of tamarins of the same species housed close together may explain the higher cortisol levels found in tamarins living in off‐show accommodation, but further research is needed.     

Effect of dietary preformed water on energy and water budgets of two sympatric desert rodents, Acomys russatus and Acomys calzivinus

Golden spiny mice ( Acomys russatus ) and common spiny mice ( Acomys cahirinus ) are omnivorous rodents that are sympatric in many rocky areas in Israeli deserts. They are similar in body size and diet habits. They differ in that A. cahirinus are nocturnal whereas A. russatus are diurnal and A. russatus inhabit extremely arid areas where A. cahirinus are absent. These differences led us to hypothesix that A. russatus are more conservative in their water needs and thererore are ahle to consumc a drier diet than A. chairinus. To test this hypothesis we oikrcd both species a dry ration and different numbers of snails and measured their energy and water intakes and their body mass changes.
Acomys russatus were capable of maintaining body mass on a much drier diet than A. cahirinus and therefore our hypothesis was supported. In order to maintain body mass A. cahirinus required about 2·1 ml/day (or about 4·7% body mass) preformed water, about twice the volume required by A. russatus. They also required a diet that had a water content of 48·3%, of the fresh matter, which was about 20% higher than that of A. russatus. The main reason why A. russatus needed less water was that they losl less by evaporation than A. cahirinus did. We suggest that the lower preformed water needs of A. russatus and their ability to consume a drier diet allom them to tolerate higher air temperatures and to inhabit extreme deserts where A. cahirinus are absent.     

Cathemerality and lunar periodicity of activity rhythms in owl monkeys of the Argentinian Chaco

Although most South American owl monkeys are mainly nocturnal, Aotus azarai azarai of the Argentinean Chaco regularly shows diurnal activity. In this study we examined the strong influence of moonlight on its diurnal and nocturnal activity, as well as the interaction of moonlight effects with other exogenous factors. We analyzed long-term automated activity recordings obtained with accelerometer collars from 7 owl monkeys during 2003 and 2004. Our data show marked lunar periodic and seasonal modulations of the owl monkeys' activity pattern. On full moon days they were active throughout the whole night and displayed reduced activity during the day. With a new moon, activity decreased during the dark portion of the night, peaked during dawn and dusk and extended over the bright morning hours. Waxing and waning moons induced a significant increase in activity during the first and the second half of the night, respectively. During the cold winter months the monkeys displayed twice as much activity throughout the warmer bright part of the day than during the rest of the year. These findings indicate that A. a. azarai is mainly a dark-active species, but is still able to shift a considerable portion of activity into the bright part of the day if unfavourable lighting and/or temperature conditions prevail during the night.     

Simulation of migratory flight and stopover affects night levels of melatonin in a nocturnal migrant

Several species of diurnal birds are nocturnal migrants. The activation of nocturnal activity requires major physiological changes, which are essentially unknown. Previous work has shown that during migratory periods nocturnal migrants have reduced night-time levels of melatonin. Since this hormone is involved in the modulation of day-night rhythms, it is a good candidate regulator of nocturnal migratory activity. We studied whether melatonin levels change when nocturnally active blackcaps (Sylvia atricapilla) are experimentally transferred from a migratory to a non-migratory state. We simulated a long migratory flight by depriving birds of food for 2 days, and a refuelling stopover by subsequently re-administering food. Such a regimen is known to induce a reduction in migratory restlessness ('Zugunruhe') in the night following food reintroduction. The experiments were performed in both autumn and spring using blackcaps taken from their breeding grounds (Sweden) and their wintering areas (Kenya). In autumn, the food regimen induced a suppression of Zugunruhe and an increase in melatonin in the night following food reintroduction. In spring, the effects of the treatment were qualitatively similar but their extent depended on the amount of body-fat reserves. This work shows that the reduction of night-time melatonin during migratory periods is functionally related to nocturnal migration, and that fat reserves influence the response of the migratory programme to food deprivation.     

Effects of light and prey availability on nocturnal, lunar and seasonal activity of tropical nightjars

Nightjars and their allies represent the only major group of visually hunting aerial insectivores with a crepuscular and/or nocturnal lifestyle. Our purpose was to examine how both light regime and prey abundance in the tropics, where periods of twilight are extremely short, but nightjar diversity is high, affect activity across different temporal scales. We studied two nightjar species in West African bush savannah, standard‐winged nightjars Macrodipteryx longipennis Shaw and long‐tailed nightjars Caprimulgus climacurus Vieillot. We measured biomass of potential prey available using a vehicle mounted trap and found that it was highest at dusk and significantly lower at dawn and during the night. Based on direct observations, both nightjars exhibit the most intense foraging behaviour at dusk, less intense foraging at dawn and least at night, as predicted by both prey abundance and conditions for visual prey detection. Nocturnal foraging was positively correlated with lunar light levels and ceased below about 0.03 mW m^?2. Over the course of a lunar cycle, nocturnal light availability varied markedly, while prey abundance remained constant at dusk and at night was slightly higher at full moon. Both species increased twilight foraging activity during new moon periods, compensating for the shorter nocturnal foraging window at that time. Seasonally, the pattern of nocturnal light availability was similar throughout the year, while prey availability peaked shortly after onset of the wet season and then slowly decreased over the following four months. The courtship and breeding phenology of both species was timed to coincide with the peak in aerial insect abundance, suggesting that prey availability rather than direct abiotic factors act as constraints, at least at the seasonal level. Our findings illustrate the peculiar constraints on visually orienting aerial nocturnal insectivores in general and tropical nightjars in particular and highlight the resulting nocturnal, lunar and seasonal allocation of activities.     

Day–night fluctuations in floral scent and their effects on reproductive success in <Emphasis Type="Italic">Lilium auratum</Emphasis>

We examined the contribution of diurnal and nocturnal pollination to male and female reproductive success in Lilium auratum. Plants were bagged for either 12 h during the day or at night to allow either only nocturnal or only diurnal visitors to forage throughout the flowering period. We found that there was no significant difference in the seed:ovule ratio among diurnally pollinated, nocturnally pollinated, or control flowers. However, in terms of male reproductive success, it was more advantageous for the plants to be pollinated both diurnally and nocturnally: the numbers of pollen grains remaining in diurnally pollinated or nocturnally pollinated flowers were significantly greater than those in control flowers. The total amount of floral volatiles of L. auratum was significantly higher at night than during the day. The constituents of floral scent of all time series examined were mostly monoterpenoids, many of which serve as attractants for nocturnal hawkmoths. Such nocturnally biased floral scent emission of L. auratum might achieve male reproductive success by attracting nocturnal visitors, which may suggest that the relative contribution of floral scent in this species is biased towards male reproductive success.     

Visual fields in the Black-crowned Night Heron Nycticorax nycticorax: nocturnality does not result in owl-like features

Compared with diurnally active species, the eyes of nocturnally active herons (Ardeidae) are relatively larger and more widely separated. These features are found in comparisons between the nocturnally foraging Black-crowned Night Heron Nycticorax nycticorax and the diurnally active Cattle Egret Bubulcus ibis. Casual viewing of the Black-crowned Night Heron gives the impression of a somewhat owl-like appearance, with an apparently wide degree of binocular overlap. Visual fields and eye movements were determined in two alert, restrained Black-crowned Night Herons with the use of an ophthalmoscopic technique. A wide degree of binocular overlap was not confirmed, and the Black-crowned Night Heron's visual field closely resembles those of diurnally foraging herons (Western Reef Heron Egretta gularis schistacea , Squacco Heron Ardeola ralloides , Cattle Egret). The Black-crowned Night Heron's binocular field is vertically long and narrow (maximum width 22̀), with the bill placed approximately at the centre. Monocular and cyclopean field widths in the horizontal plane equal 171̀ and 320̀, respectively. Retinal binocular overlap can be abolished by eye movements. There is a blind sector (10–13̀ wide) at the margin of each eye's optical field, and this results in the functional retinal binocular field being much narrower than the optical binocular fields. It is these blind sectors which give rise to the appearance of a much wider binocular field. The visual field characteristics of this heron species may be best understood in relation to the foraging technique of capturing agile, evasive prey directly in the bill. The comparatively large size of the Black-crowned Night Herons' eyes may be associated with activity over a wide range of natural light levels but does not give rise to binocular fields larger than those of diurnal heron species.