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Why do melanin ornaments signal individual quality? Insights from metal element analysis of barn owl feathers.

Melanin-based variation in colour patterns is under strong genetic control and not, or weakly, sensitive to the environment and body condition. Current signalling theory predicts that such traits may not signal honestly phenotypic quality because their production does not entail a significant fitness cost. However, recent studies revealed that in several bird species melanin-based traits covary with phenotypic attributes. In a first move to understand whether such covariations have a physiological basis, we quantified concentrations of five chemical elements in two pigmented plumage traits in the barn owl (Tyto alba). This bird shows continuous variation from immaculate to heavily marked with black spots (plumage spottiness) and from dark reddish-brown to white (plumage coloration), two traits that signal various aspects of individual quality. These two traits are sexually dimorphic with females being spottier and darker coloured than males. We found an enhancement in calcium and zinc concentration within black spots compared with the unspotted feather parts. The degree to which birds were spotted was positively correlated with calcium concentration within spots, whereas the unspotted feather parts of darker reddish-brown birds were more concentrated in zinc. This suggests that two different pigments are responsible for plumage spottiness and plumage coloration. We discuss the implications of our results in light of recent experimental field studies showing that female spottiness signals offspring humoral response towards an artificially administrated antigen, parasite resistance and fluctuating asymmetry of wing feathers.

Adaptation, Physiological↗

Ural owl sex allocation and parental investment under poor food conditions.

Parents are expected to overproduce the less costly sex under poor food conditions. The previously regular 3-year cycle in the abundance of voles, the main prey of the Ural owl, Strix uralensis, temporarily disappeared in 1999-2001. We studied Ural owls' parental feeding investment and sex allocation during these poor-quality years. We sexed hatchlings and embryos in unhatched eggs of all 131 broods produced during these years. Population wide, the owls produced significantly more males (56%). The parental food investment in the brood was estimated by sorting out the prey remains in the bottom of nest boxes. Food delivered to 83 broods without chick mortality showed no clear sex-specific investment. Nestling mortality was equal in both sexes. Thus, evidence for an investment-driven sex allocation is weak. Neither laying date, brood size nor the female's condition correlated with offspring sex ratios. In these poor years, parents provided less food per chick and the fledgling weight of daughters was reduced more than the weight of sons compared with years of high food abundance (1983 and 1986). We discuss, in relation to published studies, the possibility of a sex-allocation scenario where, under poor food conditions, a daughter's long-term fitness is reduced more than a son's.

Animals↗

Supplementary fed Ural owls increase their reproductive output with a one year time lag.

Life-history components may be food-limited. We supplemented food to 18 Ural owl, Strix uralensis, nests during the nestling period. Food supplementation led to a higher somatic condition in the female parent, but effects in males were moderate. Parents delivered less food to fed nests than to control nests. Offspring survival and fledging condition did not differ between control and fed nests. In the season following food supplementation, fed pairs bred 1 week earlier than control pairs and, coupled to this advance in laying date, fed pairs produced 0.6 eggs more than control pairs. This is the first evidence that food limitation in the current season may constrain next season's reproduction. Such carry-over effects of food-limitation may have important consequences for population dynamics.

Analysis of Variance↗

A test of multiple hypotheses for the species richness gradient of South American owls.

Many mechanisms have been proposed to explain broad scale spatial patterns in species richness. In this paper, we evaluate five explanations for geographic gradients in species richness, using South American owls as a model. We compared the explanatory power of contemporary climate, landcover diversity, spatial climatic heterogeneity, evolutionary history, and area. An important aspect of our analyses is that very different hypotheses, such as history and area, can be quantified at the same observation scale and, consequently can be incorporated into a single analytical framework. Both area effects and owl phylogenetic history were poorly associated with richness, whereas contemporary climate, climatic heterogeneity at the mesoscale and landcover diversity explained ca. 53% of the variation in species richness. We conclude that both climate and environmental heterogeneity should be retained as plausible explanations for the diversity gradient. Turnover rates and scaling effects, on the other hand, although perhaps useful for detecting faunal changes and beta diversity at local and regional scales, are not strong explanations for the owl diversity gradient.

Animals↗

Proximate basis of the covariation between a melanin-based female ornament and offspring quality.

In contradiction to sexual selection theory, several studies showed that although the expression of melanin-based ornaments is usually under strong genetic control and weakly sensitive to the environment and body condition, they can signal individual quality. Covariation between a melanin-based ornament and phenotypic quality may result from pleiotropic effects of genes involved in the production of melanin pigments. Two categories of genes responsible for variation in melanin production may be relevant, namely those that trigger melanin production (yes or no response) and those that determine the amount of pigments produced. To investigate which of these two hypotheses is the most likely, I reanalysed data collected from barn owls ( Tyto alba). The underparts of this bird vary from immaculate to heavily marked with black spots of varying size. Published cross-fostering experiments have shown that the proportion of the plumage surface covered with black spots, a eumelanin composite trait so-called "plumage spottiness", in females positively covaries with offspring humoral immunocompetence, and negatively with offspring parasite resistance (i.show $132#e. the ability to reduce fecundity of ectoparasites) and fluctuating asymmetry of wing feathers. However, it is unclear which component of plumage spottiness causes these relationships, namely genes responsible for variation in number of spots or in spot diameter. Number of spots reflects variation in the expression of genes triggering the switch from no eumelanin production to production, whereas spot diameter reflects variation in the expression of genes determining the amount of eumelanin produced per spot. In the present study, multiple regression analyses, performed on the same data sets, showed that humoral immunocompetence, parasite resistance and wing fluctuating asymmetry of cross-fostered offspring covary with spot diameter measured in their genetic mother, but not with number of spots. This suggests that genes responsible for variation in the quantity of eumelanin produced per spot are responsible for covariation between a melanin ornament and individual attributes. In contrast, genes responsible for variation in number of black spots may not play a significant role. Covariation between a eumelanin female trait and offspring quality may therefore be due to an indirect effect of melanin production.

Analysis of Variance↗

Hatching asynchrony in Burrowing Owls is influenced by clutch size and hatching success but not by food.

In most animals, siblings from a given reproductive event emerge over a very short period of time. In contrast, many species of birds hatch their young asynchronously over a period of days or weeks, handicapping last-hatched chicks with an age and size disadvantage. Numerous studies have examined the adaptive significance of this atypical hatching pattern, but few have attempted to explain the considerable intrapopulation variation that exists in hatching asynchrony. I explored proximate determinants of hatching asynchrony by monitoring 112 Burrowing Owl (Athene cunicularia) nests in the grasslands of southern Saskatchewan, Canada, over 4 years. Age disparities between first- and last-hatched siblings (i.e., hatching spans) varied considerably, ranging between 1 and 7 days (mode = 4 days). These hatching spans increased with increased hatching success. Hatching spans also increased with larger clutches, but the increase was less than predicted given the increased time required to lay more eggs. Hatching span was unrelated to number of prey cached in the nest during egg laying (an index of food availability), and was unaltered by a year of super-abundant prey. Furthermore, pairs given extra food during laying had hatching spans equal to those of unsupplemented control pairs. These results were inconsistent with both the energy constraint and facultative manipulation hypotheses, which predict that hatching asynchrony should vary with the level of food during laying, when incubation onset is determined. Burrowing Owls were apparently free of food limitation early in breeding, yet may not have been able to optimize hatching spans because food conditions during laying were largely unrelated to food conditions during brooding. Thus, one of the premises for facultative manipulation of hatching asynchrony-that laying females are able to forecast post-hatch food conditions-may not have been met for this population of Burrowing Owls.

Analysis of Variance↗

Demographic effects of extreme winter weather in the barn owl.

Extreme weather events can lead to immediate catastrophic mortality. Due to their rare occurrence, however, the long-term impacts of such events for ecological processes are unclear. We examined the effect of extreme winters on barn owl (Tyto alba) survival and reproduction in Switzerland over a 68-year period (approximately 20 generations). This long-term data set allowed us to compare events that occurred only once in several decades to more frequent events. Winter harshness explained 17 and 49% of the variance in juvenile and adult survival, respectively, and the two harshest winters were associated with major population crashes caused by simultaneous low juvenile and adult survival. These two winters increased the correlation between juvenile and adult survival from 0.63 to 0.69. Overall, survival decreased non-linearly with increasing winter harshness in adults, and linearly in juveniles. In contrast, brood size was not related to the harshness of the preceding winter. Our results thus reveal complex interactions between climate and demography. The relationship between weather and survival observed during regular years is likely to underestimate the importance of climate variation for population dynamics.

Adaptation, Physiological↗

Sources of variability in spotted owl population growth rate: testing predictions using long-term mark-recapture data.

For long-lived iteroparous vertebrates that annually produce few young, life history theory predicts that reproductive output (R) and juvenile survival should influence temporal variation in population growth rate (lambda) more than adult survival does. We examined this general prediction using 15 years of mark-recapture data from a population of California spotted owls (Strix occidentalis occidentalis). We found that survival of individuals > or =1 year old (phi) exhibited much less temporal variability (CV = 0.04), where CV is coefficient of variation, than R (CV = 0.83) and that R was strongly influenced by environmental stochasticity. Although lambda was most sensitive (ê; log-transformed sensitivity) to phi (ê = 0.77), and much less sensitive to either R (ê = 0.12) or juvenile survival (survival rate of owls from fledging to 1 year old; ê = 0.12), we estimated that R contributed as much as phi to the observed annual variability in lambda. The contribution of juvenile survival to variability in lambda was proportional to its ê. These results are consistent with the hypothesis that natural selection may have favored the evolution of longevity in spotted owls as a strategy to increase the probability of experiencing favorable years for reproduction. Our finding that annual weather patterns that most affected R (temperature and precipitation during incubation) and phi (conditions during winter related to the Southern Oscillation Index) were equally good at explaining temporal variability in lambda supports the conclusion that R and phi were equally responsible for variability in lambda. Although currently accepted conservation measures for spotted owl populations attempt to enhance survival, our results indicated that conservation measures that target R may be as successful, as long as actions do not reduce phi.

Animals↗

How owls structure visual information.

Recent studies on perceptual organization in humans claim that the ability to represent a visual scene as a set of coherent surfaces is of central importance for visual cognition. We examined whether this surface representation hypothesis generalizes to a non-mammalian species, the barn owl ( Tyto alba). Discrimination transfer combined with random-dot stimuli provided the appropriate means for a series of two behavioural experiments with the specific aims of (1) obtaining psychophysical measurements of figure-ground segmentation in the owl, and (2) determining the nature of the information involved. In experiment 1, two owls were trained to indicate the presence or absence of a central planar surface (figure) among a larger region of random dots (ground) based on differences in texture. Without additional training, the owls could make the same discrimination when figure and ground had reversed luminance, or were camouflaged by the use of uniformly textured random-dot stereograms. In the latter case, the figure stands out in depth from the ground when positional differences of the figure in two retinal images are combined (binocular disparity). In experiment 2, two new owls were trained to distinguish three-dimensional objects from holes using random-dot kinematograms. These birds could make the same discrimination when information on surface segmentation was unexpectedly switched from relative motion to half-occlusion. In the latter case, stereograms were used that provide the impression of stratified surfaces to humans by giving unpairable image features to the eyes. The ability to use image features such as texture, binocular disparity, relative motion, and half-occlusion interchangeably to determine figure-ground relationships suggests that in owls, as in humans, the structuring of the visual scene critically depends on how indirect image information (depth order, occlusion contours) is allocated between different surfaces.

Animals↗

Tonotopic projections of the auditory nerve to the cochlear nucleus angularis in the barn owl.

The nucleus angularis (NA), one of the two cochlear nuclei of birds, plays an important role in the processing of sound intensity. To begin investigating the NA in detail in the barn owl, which is a popular animal model for neural mechanisms of sound localization, a frequency map for this nucleus is presented here. Focal injections of horseradish peroxidase or neurobiotin were placed either in the NA or in the cochlear nucleus magnocellularis, labeling small groups of auditory nerve fibers of known characteristic frequency (CF) from 0.25 to 9.6 kHz. The courses of their axonal branches were used to construct a composite average map of the tonotopic frequency representation in the nucleus angularis. Nucleus angularis in the barn owl, as seen in frontal sections, resembles a sheet of cells bent approximately into an S shape. The lowest frequencies were found represented at the ventromedial extreme. The representation of increasingly higher frequencies then followed the S shape, with the highest frequencies located at the ventrolateral tip. Auditory nerve fibers of a given CF always entered the nucleus angularis within a well-restricted area and then traveled along their isofrequency band within the NA while branching off terminals. The isofrequency bands were typically slanted from caudo-ventro-medial to rostro-dorso-lateral. The basic tonotopic organization is comparable to that found in other birds, the major differences being the large size and unusual shape of the barn owl's nucleus angularis.

Animals↗

Sound-localization experiments with barn owls in virtual space: influence of interaural time difference on head-turning behavior.

Specific cues in a sound signal are naturally linked to certain parameters in acoustic space. In the barn owl, interaural time difference (ITD) varies mainly with azimuth, while interaural level difference (ILD) varies mainly with elevation. Previous data suggested that ITD is indeed the main cue for azimuthal sound localization in this species, while ILD is an important cue for elevational sound localization. The exact contributions of these parameters could be tested only indirectly because it was not possible to generate a stimulus that contained all relevant spatial information on the one hand, and allowed for a clean separation of these parameters on the other hand. Virtual auditory worlds offer this opportunity. Here we show that barn owls responded to azimuthal variations in virtual space in the same way as to variations in free-field stimuli. We interpret the increase of turning angle with sound-source azimuths (up to +/- 140 degrees) such that the owls did not experience front/back confusions with virtual stimuli. We then separated the influence of ITD from the influence of all other stimulus parameters by fixing the overall ITD in virtual stimuli to a constant value (+100 micros or +100 micros) while leaving all other sound characteristics unchanged. This manipulation influenced both azimuthal and elevational components of head arms. Since the owls' azimuthal head-turn amplitude always resembled the value signified by the ITD, these data demonstrated that azimuthal sound localization is influenced only by ITD both in the frontal hemisphere and in large parts of the rear hemisphere. ILDs did not have an influence on azimuthal components of head turns. While response latency to normal virtual stimuli was found to be largely independent of stimulus position, response delays of the head turns became longer if the ITD information pointed into a different hemisphere as the other cues of the sounds.

Animals↗

Detection of large interaural delays and its implication for models of binaural interaction.

The interaural time difference (ITD) is a major cue to sound localization along the horizontal plane. The maximum natural ITD occurs when a sound source is positioned opposite to one ear. We examined the ability of owls and humans to detect large ITDs in sounds presented through headphones. Stimuli consisted of either broad or narrow bands of Gaussian noise, 100 ms in duration. Using headphones allowed presentation of ITDs that are greater than the maximum natural ITD. Owls were able to discriminate a sound leading to the left ear from one leading to the right ear, for ITDs that are 5 times the maximum natural delay. Neural recordings from optic-tectum neurons, however, show that best ITDs are usually well within the natural range and are never as large as ITDs that are behaviorally discriminable. A model of binaural crosscorrelation with short delay lines is shown to explain behavioral detection of large ITDs. The model uses curved trajectories of a cross-correlation pattern as the basis for detection. These trajectories represent side peaks of neural ITD-tuning curves and successfully predict localization reversals by both owls and human subjects.

Animals↗

Some species of Centrorhynchus Lühe, 1911 (Acanthocephala: Centrorhynchidae) from the collection of the Natural History Museum, London.

Seven species of Centrorhynchus Lühe, 1911 are present in the Parasitic Worms Collection of The Natural History Museum, London: C. aluconis (Müller, 1780) Lühe, 1911 from Strix aluco Linnaeus in Great Britain; C. buteonis (Schrank, 1788) Kostylev, 1914 from Accipiter virgatus (Temminck) (new host record) in Sri Lanka (new geographical record); C. clitorideus (Meyer, 1931) Golvan, 1956 from Athene brama (Temminck) (new host record) in India; C. crotophagicola Schmidt and Neiland, 1966 (encysted juveniles in the stomach wall) from Anolis lineatopus Grey (new host record) and A. sagrei Duméril and Bibron (new host record) from Jamaica (new geographical record); C. falconis (Johnston and Best, 1943) Golvan, 1956 from Spilornis cheela (Latham) in Sri Lanka (new geographical record); C. globocaudatus (Zeder, 1800) Lühe, 1911 from Falco ardosiaceus Vieillot (new host record) in West Africa; and C. milvus Ward, 1956 from Milvus migrans (Boddaert) in India. The species are described and figured on the basis of this material.

Acanthocephala↗

Protean behavior under barn-owl attack: voles alternate between freezing and fleeing and spiny mice flee in alternating patterns.

When attacking a spiny mouse in an experimental arena, a barn owl launched a few attacks from distant perches, made repetitive short-distance swoops in each attack and remained in the vicinity of the prey while chasing it. The spiny mouse fled in response, and typically oriented to face the owl whenever it stopped. When attacking a vole, the barn owl performed a greater number of attacks from distant perches, and left the vicinity of the prey after a few short-distance chases or capture attempts. Voles responded to these attacks in unspecific combinations of freezing and fleeing, and did not turn to face the owl when they stopped. Four conclusions are drawn from these encounters. First, two strategies characterized these predator-prey interactions; in one, both predator and prey continuously maintained awareness of each other's location; whereas in the other they continuously attempted to avoid the attention of the other. Second, responses of spiny mice and voles were a manifestation of protean behavior, with spiny mice fleeing in an alternating pattern and voles alternating between running and freezing. Third, locomotor response to owl attack comprised behavior that is an augmentation of normal behavior, with voles clinging to the walls and spiny mice running with frequent and irregular changes in direction. Fourth, the different defensive responses accord with the motor capacities and habitat of each rodent species. All in all, these results demonstrate the dynamic and multidimensional nature of predator-prey interactions.

Animals↗

Auditory neuroscience: a time for coincidence?

Mammals and birds appear to encode timing differences between the ears, a major cue for auditory localization, in fundamentally different ways. It now appears that results from different species can be accommodated within a single general framework.

Animals↗

Heavy metal contamination in little owl (Athene noctua) and common buzzard (Buteo buteo) from northern Italy.

In this study, two raptor species, the common buzzard (Buteo buteo) and the little owl (Athene noctua), were investigated for lead and cadmium concentrations, using liver, kidneys, pectoral muscle, sternum bone, and feathers. All the collected birds died at the Centro Recupero Rapaci of Lega Italiana Protezione Uccelli in Sala Baganza (Parma, Italy). They arrived alive at the Centro between November 1998 and November 1999 but died or were put to death as a consequence of injuries or other ailments. The results of the investigation do not show an excessive exposure to cadmium, whereas some interesting data have emerged in the case of lead. The concentration of the latter in the liver and in the bone of two little owls seem to suggest the possibility of chronic exposure. The high values found in one common buzzard, on the other hand, suggest an acute exposure and, probably, a case of lead shot ingestion.

Animals↗

Brominated flame retardants and organochlorine pollutants in eggs of little owls (Athene noctua) from Belgium.

Residues of brominated diphenylethers (PBDEs), organochlorinated pesticides (OCPs) and polychlorinated biphenyls (PCBs) were measured in 40 eggs of little owls (Athene noctua), a terrestrial top predator from Belgium. The major organohalogens detected were PCBs (median 2,600 ng/g lipid, range 790-23 000 ng/g lipid). PCB 153,138/163, 170, 180 and 187 were the predominant congeners and constituted 71% of total sum PCBs. PBDEs were measurable in all samples, but their concentrations were much lower than for PCBs, with a range from 29-572 ng/g lipid (median 108 ng/g lipid). The most prevalent PBDE congeners in little owl egg samples were BDE 47, 99 and 153. This profile differs from the profile in marine bird species, for which BDE 47 was the dominant congener, indicating that terrestrial birds may be more exposed to higher brominated BDE congeners than marine birds. The fully brominated BDE 209 could be detected in one egg sample (17 ng/g lipid), suggesting that higher brominated BDEs may accumulate in terrestrial food chains. Brominated biphenyl (BB) 153 was determined in all egg samples, with levels ranging from 0.6 to 5.6 ng/g lipid (median 1.3 ng/g lipid). Additionally, hexabromocyclododecane (HBCD) could be identified and quantified in only two eggs at levels of 20 and 50 ng/g lipid. OCPs were present at low concentrations, suggesting a rather low contamination of the sampled environment with OCPs (median concentrations of sum DDTs: 826 ng/g lipid, sum chlordanes: 1,016 ng/g lipid, sum HCHs: 273 ng/g lipid). Hexachlorobenzene (HCB) and octachlorostyrene (OCS) were also found at low median levels of 134 and 3.4 ng/g lipid, respectively. Concentrations of most analytes were significantly higher in eggs collected from deserted nests in comparison to addled (unhatched) eggs, while eggshell thickness did not differ between deserted and addled eggs. No significant correlations were found between eggshell thickness and the analysed organohalogens.

Animals↗