Madeleine F. Scriba

Linking melanism to brain development: expression of a melanism-related gene in barn owl feather follicles covaries with sleep ontogeny

BackgroundIntra-specific variation in melanocyte pigmentation, common in the animal kingdom, has caught the eye of naturalists and biologists for centuries. In vertebrates, dark, eumelanin pigmentation is often genetically determined and associated with various behavioral and physiological traits, suggesting that the genes involved in melanism have far reaching pleiotropic effects. The mechanisms linking these traits remain poorly understood, and the potential involvement of developmental processes occurring in the brain early in life has not been investigated. We examined the ontogeny of rapid eye movement (REM) sleep, a state involved in brain development, in a wild population of barn owls (Tyto alba) exhibiting inter-individual variation in melanism and covarying traits. In addition to sleep, we measured melanistic feather spots and the expression of a gene in the feather follicles implicated in melanism (PCSK2).ResultsAs in mammals, REM sleep declined with age across a period of brain development in owlets. In addition, inter-individual variation in REM sleep around this developmental trajectory was predicted by variation in PCSK2 expression in the feather follicles, with individuals expressing higher levels exhibiting a more precocial pattern characterized by less REM sleep. Finally, PCSK2 expression was positively correlated with feather spotting.ConclusionsWe demonstrate that the pace of brain development, as reflected in age-related changes in REM sleep, covaries with the peripheral activation of the melanocortin system. Given its role in brain development, variation in nestling REM sleep may lead to variation in adult brain organization, and thereby contribute to the behavioral and physiological differences observed between adults expressing different degrees of melanism.

Did tool-use evolve with enhanced physical cognitive abilities?

The use and manufacture of tools have been considered to be cognitively demanding and thus a possible driving factor in the evolution of intelligence. In this study, we tested the hypothesis that enhanced physical cognitive abilities evolved in conjunction with the use of tools, by comparing the performance of naturally tool-using and non-tool-using species in a suite of physical and general learning tasks. We predicted that the habitually tool-using species, New Caledonian crows and Galápagos woodpecker finches, should outperform their non-tool-using relatives, the small tree finches and the carrion crows in a physical problem but not in general learning tasks. We only found a divergence in the predicted direction for corvids. That only one of our comparisons supports the predictions under this hypothesis might be attributable to different complexities of tool-use in the two tool-using species. A critical evaluation is offered of the conceptual and methodological problems inherent in comparative studies on tool-related cognitive abilities.

Ecology and Neurophysiology of Sleep in Two Wild Sloth Species

STUDY OBJECTIVES Interspecific variation in sleep measured in captivity correlates with various physiological and environmental factors, including estimates of predation risk in the wild. However, it remains unclear whether prior comparative studies have been confounded by the captive recording environment. Herein we examine the effect of predation pressure on sleep in sloths living in the wild. DESIGN Comparison of two closely related sloth species, one exposed to predation and one free from predation. SETTING Panamanian mainland rainforest (predators present) and island mangrove (predators absent). PARTICIPANTS Mainland (Bradypus variegatus, five males and four females) and island (Bradypus pygmaeus, six males) sloths. INTERVENTIONS None. MEASUREMENTS AND RESULTS Electroencephalographic (EEG) and electromyographic (EMG) activity was recorded using a miniature data logger. Although both species spent between 9 and 10 h per day sleeping, the mainland sloths showed a preference for sleeping at night, whereas island sloths showed no preference for sleeping during the day or night. Standardized EEG activity during nonrapid eye movement (NREM) sleep showed lower low-frequency power, and increased spindle and higher frequency power in island sloths when compared to mainland sloths. CONCLUSIONS In sloths sleeping in the wild, predation pressure influenced the timing of sleep, but not the amount of time spent asleep. The preference for sleeping at night in mainland sloths may be a strategy to avoid detection by nocturnal cats. The pronounced differences in the NREM sleep EEG spectrum remain unexplained, but might be related to genetic or environmental factors.

Sleep research goes wild: New methods and approaches to investigate the ecology, evolution and functions of sleep

Despite being a prominent aspect of animal life, sleep and its functions remain poorly understood. As with any biological process, the functions of sleep can only be fully understood when examined in the ecological context in which they evolved. Owing to technological constraints, until recently, sleep has primarily been examined in the artificial laboratory environment. However, new tools are enabling researchers to study sleep behaviour and neurophysiology in the wild. Here, we summarize the various methods that have enabled sleep researchers to go wild, their strengths and weaknesses, and the discoveries resulting from these first steps outside the laboratory. The initial studies to ‘go wild’ have revealed a wealth of interindividual variation in sleep, and shown that sleep duration is not even fixed within an individual, but instead varies in response to an assortment of ecological demands. Determining the costs and benefits of this inter- and intraindividual variation in sleep may reveal clues to the functions of sleep. Perhaps the greatest surprise from these initial studies is that the reduction in neurobehavioural performance resulting from sleep loss demonstrated in the laboratory is not an obligatory outcome of reduced sleep in the wild. This article is part of the themed issue ‘Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals’.

Sleep and vigilance linked to melanism in wild barn owls

Understanding the function of variation in sleep requires studies in the natural ecological conditions in which sleep evolved. Sleep has an impact on individual performance and hence may integrate the costs and benefits of investing in processes that are sensitive to sleep, such as immunity or coping with stress. Because dark and pale melanic animals differentially regulate energy homeostasis, immunity and stress hormone levels, the amount and/or organization of sleep may covary with melanin‐based colour. We show here that wild, cross‐fostered nestling barn owls (Tyto alba) born from mothers displaying more black spots had shorter non‐REM (rapid eye movement) sleep bouts, a shorter latency until the occurrence of REM sleep after a bout of wakefulness and more wakefulness bouts. In male nestlings, the same sleep traits also correlated with their own level of spotting. Because heavily spotted male nestlings and the offspring of heavily spotted biological mothers switched sleep–wakefulness states more frequently, we propose the hypothesis that they could be also behaviourally more vigilant. Accordingly, nestlings from mothers displaying many black spots looked more often towards the nest entrance where their parents bring food and towards their sibling against whom they compete. Owlets from heavily spotted mothers might invest more in vigilance, thereby possibly increasing associated costs due to sleep fragmentation. We conclude that different strategies of the regulation of brain activity have evolved and are correlated with melanin‐based coloration.

A bird's eye view of sleep

In the News Focus story “Simple sleepers” (18 July, p. [334][1]), E. Youngsteadt highlights recent advances, derived from genetic research in fruit flies and other “simple” animal models, in our understanding of sleep. The power of this genetic approach is undeniable, but the simplicity that

Nocturnal, diurnal and bimodal patterns of locomotion, sibling interactions and sleep in nestling Barn Owls

AbstractTemporal variation in physical activity is mainly determined by the day–night cycle. While this may be true for diurnal species whose vision at night is often poor, the situation might be more complex in nocturnal animals as many such species can see both in the dark and in the daylight. We examined in Barn Owl (Tyto alba) nestlings whether temporal variation of behavioural activities and sleep is shaped by parental feeding visits occurring during the first part of the night and the extent to which they also occur during daylight hours. We measured several behaviours in 280 individuals from 90 broods recorded in 4 years. Parental feeding visits progressively declined in frequency from the beginning to the end of the night, and a number of offspring behaviours followed the same pattern of activity (feeding, vocalization and self-preening). Surprisingly, nestlings were awake not only at sunset, but also at sunrise. Several behaviours (locomotion, wing flapping and sibling interactions, such as pecking and allopreening among nestlings) showed peaks of activity at sunset and sunrise, suggesting that they were performed for other reasons than to interact with parents. Allopreening was performed more often during the day than at night. We conclude that although adult Barn Owls are nocturnal, nestlings display a complex temporal pattern of activity that is governed not only by feeding but also by other unknown factors.ZusammenfassungNächtliche, tägliche und bimodale Muster der Lokomotion, der Interaktionen mit Geschwistern und des Schlafs bei Schleiereulennestlingen Der zeitliche Verlauf der körperlichen Aktivität wird hauptsächlich vom Tag-Nacht-Rhythmus bestimmt. Besonders tagaktive Arten sind oft nicht in der Lage nachts zu sehen, während nachtaktive Arten sowohl am Tag als auch nachts sehen können. Wir untersuchten an Schleiereulennestlingen (Tyto alba), ob zeitliche Variation von Verhalten und Gehirnaktivität von den elterlichen Besuchen in der ersten Hälfte der Nacht abhängen und ob Aktivitäten während des Tages ausgeführt werden. Wir bestimmten Verhaltensweisen von 280 Individuen aus 90 Bruten über vier Jahre. Elterliche Fütterungsbesuche nahmen über die Nacht stetig in der Frequenz ab, und einige der Verhaltensweisen der Nestlinge folgten diesem Muster (Fressen, Rufen und Putzen). Erstaunlicherweise waren Nestlinge nicht nur bei Sonnenuntergang wach, sondern auch bei Sonnenaufgang. Einige Verhaltensweisen (Lokomotion, Flügel schlagen und Interaktionen mit Geschwistern wie Picken und gegenseitiges Putzen) zeigten hohe Aktivität bei Sonnenuntergang und –aufgang, was darauf hindeutet, dass sie aus anderen Gründen ausgeführt wurden als mit den Eltern zu interagieren. Gegenseitiges Putzen wurde tagsüber öfter durchgeführt als nachts. Zusammenfassend ist zu sagen, dass Schleiereulen zwar nachtaktiv sind, Nestlinge aber ein komplexes Aktivitätsmuster zeigen, das durch die elterliche Fütterung vorgegeben ist, aber auch durch weitere, noch unbekannte Faktoren bestimmt ist.

Melanism is related to behavioural lateralization in nestling barn owls

Behavioural laterality is a commonly observed phenomenon in many species suggesting there might be an advantage of using dominantly one side over the other for certain tasks. Indeed, lateralized individuals were often shown to be more successful in cognitive tasks compared to non-lateralized conspecifics. However, stressed individuals are also often, but not always, more strongly lateralized. Because barn owl (Tyto alba) females displaying larger black spots on the tip of their ventral feathers produce offspring that are more resistant to a variety of environmental stressful factors, we examined whether laterality is associated with melanin-based coloration. We recorded whether nestlings use more often the right or left foot to scratch their body and whether they preen more often one side of the body or the other using their bills. We found that the strength of lateralization of preening and scratching was less pronounced in individuals born from heavily spotted mothers. This result might be explained by plumage-related variation in the ability to resist stressful rearing conditions.

The effect of food quality during growth on spatial memory consolidation in adult pigeons

ABSTRACT Poor environmental conditions experienced during early development can have negative long-term consequences on fitness. Animals can compensate for negative developmental effects through phenotypic plasticity by diverting resources from non-vital to vital traits such as spatial memory to enhance foraging efficiency. We tested in young feral pigeons (Columba livia) how diets of different nutritional value during development affect the capacity to retrieve food hidden in a spatially complex environment, a process we refer to as ‘spatial memory’. Parents were fed with either high- or low-quality food from egg laying until young fledged, after which all young pigeons received the same high-quality diet until memory performance was tested at 6 months of age. The pigeons were trained to learn a food location out of 18 possible locations in one session, and then their memory of this location was tested 24 h later. Birds reared with the low-quality diet made fewer errors in the memory test. These results demonstrate that food quality during development has long-lasting effects on memory, with a moderate nutritional deficit improving spatial memory performance in a foraging context. It might be that under poor feeding conditions resources are redirected from non-vital to vital traits, or pigeons raised with low-quality food might be better in using environmental cues such as the position of the sun to find where food was hidden. Summary: Food quality during development had long-lasting effects on memory in pigeons, with a moderate nutritional deficit improving spatial memory performance in a foraging context.

Ultradian Rhythmicity in Sleep-Wakefulness Is Related to Color in Nestling Barn Owls:

The possession of a rhythm is usually described as an important adaptation to regular changing environmental conditions such as the light-dark cycle. However, recent studies have suggested plasticity in the expression of a rhythm depending on life history and environmental factors. Barn owl (Tyto alba) nestlings show variations in behavior and physiology in relation to the size of black feather spots, a trait associated with many behavioral and physiological phenotypes including the circadian expression of corticosterone and the regulation of body mass. This raises the possibility that individual spottiness could be associated with rhythmicity in sleep-wakefulness. Owlets showed ultradian rhythms in sleep-wakefulness, with a period length of 4.5 to 4.9 h. The period length of wakefulness and non-REM sleep was shorter in heavily compared to lightly spotted female nestlings, whereas in males, the opposite result was found. Furthermore, male and female nestlings displaying small black spots showed strong rhythmicity levels in wakefulness and REM sleep. This might be an advantage in a stable environment with predictable periodic changes in light, temperature, or social interactions. Heavily spotted nestlings displayed weak rhythms in wakefulness and REM sleep, which might enable them to be more flexible in reactions to unexpected events such as predation or might be a mechanism to save energy. These findings are consistent with previous findings showing that large-spotted nestlings switch more frequently between wakefulness and sleep, resulting in higher levels of vigilance compared to small-spotted conspecifics. Thus, nestlings with larger black feather spots might differently handle the trade-off between wakefulness and sleep, attention, and social interactions compared to nestlings with smaller black spots.