Interspecific variation in the use of carotenoid-based coloration in birds: diet, life history and phylogeny

Birds show striking interspecific variation in their use of carotenoid-based coloration. Theory predicts that the use of carotenoids for coloration is closely associated with the availability of carotenoids in the diet but, although this prediction has been supported in single-species studies and those using small numbers of closely related species, there have been no broad-scale quantitative tests of the link between carotenoid coloration and diet. Here we test for such a link using modern comparative methods, a database on 140 families of birds and two alternative avian phylogenies. We show that carotenoid pigmentation is more common in the bare parts (legs, bill and skin) than in plumage, and that yellow coloration is more common than red. We also show that there is no simple, general association between the availability of carotenoids in the diet and the overall use of carotenoid-based coloration. However, when we look at plumage coloration separately from bare part coloration, we find there is a robust and significant association between diet and plumage coloration, but not between diet and bare part coloration. Similarly, when we look at yellow and red plumage colours separately, we find that the association between diet and coloration is typically stronger for red coloration than it is for yellow coloration. Finally, when we build multivariate models to explain variation in each type of carotenoid-based coloration we find that a variety of life history and ecological factors are associated with different aspects of coloration, with dietary carotenoids only being a consistent significant factor in the case of variation in plumage. All of these results remain qualitatively unchanged irrespective of the phylogeny used in the analyses, although in some cases the precise life history and ecological variables included in the multivariate models do vary. Taken together, these results indicate that the predicted link between carotenoid coloration and diet is idiosyncratic rather than general, being strongest with respect to plumage colours and weakest for bare part coloration. We therefore suggest that, although the carotenoid-based bird plumage may a good model for diet-mediated signalling, the use of carotenoids in bare part pigmentation may have a very different functional basis and may be more strongly influenced by genetic and physiological mechanisms, which currently remain relatively understudied.     

Latitude, elevation and body mass variation in Andean passerine birds

• 1 Relationships between body mass and latitude, and body mass and elevation are examined in the assemblage of Andean passerine birds.
• 2 Across species, body mass is positively correlated with the mid‐point of the species elevational distribution, but there is no significant relationship between body mass and latitudinal range mid‐point.
• 3 When the assemblage is separated into Andean endemic and non‐endemic species, the former group shows a significant positive relationship between body mass and elevation, and the latter a significant positive relationship between body mass and latitude (‘Bergmann’s rule’). Andean endemic species exhibit Bergmann’s rule once elevation is controlled for using multiple regression.
• 4 These relationships are not a consequence of the phylogenetic non‐independence of species. All the effects shown are very weak, with latitude and elevation explaining only a few per cent of the variation in body mass. Relationships are strongest when phylogenetically controlled analyses are performed just within genera.
• 5 The implications of these results for the mechanistic understanding of Bergmann’s rule are discussed.

     

Dispersal and the interspecific abundance-occupancy relationship in British birds

Aim To test the prediction that deviations of species from the positive interspecific relationship between abundance and occupancy (a measure of geographical range size) are related to differences in dispersal. Location Great Britain. Methods Quantitative data on the abundances, occupancy and dispersal distances of British birds are compared using phylogenetic comparative methods. Results Measures of natal and adult dispersal distance, and the intraspecific variance in these parameters, explain little variation in occupancy in addition to that accounted for by population size. Individual dispersal variables failed to explain significant variance when added individually to a model with population size as a predictor. Migrants and species using wet habitats tend to disperse further than residents and dry habitat species. Analysing these four groups separately revealed effects of dispersal only on the occupancy attained by dry habitat species. Conclusions The only consistent predictor of occupancy in these analyses was population size.     

Hues of a dragon's belly: morphological correlates of ventral coloration in water dragons

Sexual dichromatism is common in lizards, and may play an important role in sex recognition and mating systems. Nonetheless, relatively few published papers provide quantitative analyses of colour, deal with Australian taxa or are based on large-bodied species. Water dragons Physignathus lesueurii (Agamidae) from eastern Australia are very large (upto 1 m total length) and sexually dichromatic, with conspicuous red ventral coloration in adult males. We quantified coloration in three ventral regions (throat, chest and abdomen) of males and females using a spectroradiometer and looked for associations of colour with sex and with morphological traits predicted to correlate with fitness (body size, body condition, relative head size and asymmetry of femoral pores). Among adult males, larger individuals showed less red on the abdomen than did smaller animals, and males with relatively large heads had darker, less red abdomens than did males with smaller heads. Among adult females, larger animals had darker chests, and less red on the abdomen and chest, than did smaller females. The similarity in these trends between the sexes, and the location of the sexually dichromatic and size-sensitive colours in an area (under the abdomen) where they presumably are not visible to other lizards cast doubt on their utility as sexual or dominance signals. Hence, although we documented significant sex and body-size effects on ventral coloration, our results suggest that ventral colours in water dragons do not function in sex-specific displays.     

Processes generating macroevolutionary patterns of morphological variation in birds: a simulation study

Multivariate patterns of morphological variation in birds are analysed. In general, there are strong allometric patterns among characters such that most of the variation is confined to a major “size” axis. To analyse the possible evolutionary processes behind this pattern I employed a computer simulation of cladogenesis and anagenesis based on a genetic and a random walk model (drift). All runs started with one species and speciation occurred to generate 100 species. Three levels of correlations were allowed. The results from the simulations were compared with the pattern of variation in finches (Fringillidae). The simulations showed two things. First, the univariate drift model was inappropriate in terms of the level of variation; the observed level was lower than expected by drift. Univariate drift was also unable to create tight correlations among characters as observed in several taxa. Second, to create the pattern observed, either relatively strong genetic correlations (r_g ≈ 0.5), or alternatively strong correlated selection, was needed. This suggests that morphological change in birds in general consists of changes in growth such that species become larger or smaller than their ancestors but retain their ancestral shape. The results stress the importance of stabilising selection in shaping the macroevolutionary patterns of morphological variation in birds.     

Response of lamb plasma carotenoid concentration to a shift from a low to a high dietary carotenoid level

This study was conducted to investigate the pattern of plasma carotenoid concentration (PCC) in lambs switching from a low to a high dietary carotenoid level. A total of 12 Romane lambs were individually penned indoors and fed a low dietary carotenoid level for 23 days (period 1) and then a high dietary carotenoid level for 15 days (period 2). At the beginning of period 2, the lambs were 15 weeks old and weighed 29.9 kg (s.d. 2.7) on average. Lambs were fed daily (dry matter) 0.558 kg alfalfa pellets, 0.181 kg straw and 0.181 kg barley. Plasma content of total carotenoids was measured daily in period 2 by spectrophotometry. PCC (μg/l) varied with the animal (P < 0.001) and with time elapsed since the beginning of alfalfa distribution (P < 0.001). Mean PCC was 8 μg/l (s.d. 3.3) at the beginning of period 2, then increased curvilinearly with the time elapsed since the beginning of alfalfa distribution. As early as 24 h on the alfalfa diet, PCC was already higher than before the switch (P < 0.001). Mean PCC continued to increase until day 6 on average and reached a plateau thereafter. We propose a monomolecular function to model this pattern, the equation obtained on the mean data being: PCC = 97 (s.e. 2.2) × (1−exp^{(−0.3378 (s.e. 0.0282)×d)}), where r² = 0.997, r.s.d. = 4.47, n = 15 and d = day. The percentage of variance explained by the model ranged between 95.9% and 99.2%, depending on the animal. The parameters of the monomolecular function varied among animals, confirming the interindividual variability in animal response. Plateau for PCC was reached slightly earlier for the six lambs with the lowest values of the asymptote than for the six lambs with the highest values of the asymptote.     

Sociality,ecology and developmental constraints predict variation in brain size across birds

Conflicting theories have been proposed to explain variation in relative brain size across the animal kingdom. Ecological theories argue that the cognitive demands of seasonal or unpredictable environments have selected for increases in relative brain size, whereas the ‘social brain hypothesis’ argues that social complexity is the primary driver of brain size evolution. Here, we use a comparative approach to test the relative importance of ecology (diet, foraging niche and migration), sociality (social bond, cooperative breeding and territoriality) and developmental mode in shaping brain size across 1886 bird species. Across all birds, we find a highly significant effect of developmental mode and foraging niche on brain size, suggesting that developmental constraints and selection for complex motor skills whilst foraging generally imposes important selection on brain size in birds. We also find effects of social bonding and territoriality on brain size, but the direction of these effects do not support the social brain hypothesis. At the same time, we find extensive heterogeneity among major avian clades in the relative importance of different variables, implying that the significance of particular ecological and social factors for driving brain size evolution is often clade- and context-specific. Overall, our results reveal the important and complex ways in which ecological and social selection pressures and developmental constraints shape brain size evolution across birds.     

Differential rates of morphological divergence in birds

There are more small-bodied bird species than there are large-bodied, even on a logarithmic scale. In birds this pattern, which is also found in other higher taxa, appears not to be due to neutral evolution. It has often been suggested that the skew of body size frequency distributions is the result of a relationship between body size and the net rate of speciation, but phylogenetic analyses so far have rejected the hypothesis that small-bodied species are subject to higher net rates of speciation. On the contrary, we show that there exists a relationship between body size and its own evolutionary variability: avian families of small body size show less interspecific variation in body size than large-bodied families of similar age and species richness.     

Patterns of within-species body size variation of birds: strong evidence for Bergmann's rule

Aim The aim of this study is to test whether Bergmann's rule, a general intraspecific tendency towards larger body size in cooler areas and at higher latitudes, holds for birds throughout the world. Location This study includes information on species of birds from throughout the world. Methods I gathered data on body size variation from the literature and used two general meta‐analytical procedures to test the validity of Bergmann's rule in birds: a modified vote‐counting approach and calculation of overall effect sizes. Related species may show similar body size trends, thus I performed all analyses using nonphylogenetic and phylogenetic methods. I used tests of phylogenetic signal for each data set to decide which type of statistical analysis (nonphylogenetic or phylogenetic) was more appropriate. Results The majority of species of birds (76 of 100 species) are larger at higher latitudes, and in cooler areas (20 of 22 species). Birds show a grand mean correlation coefficient of +0.32 for body size and latitude, and ?0.81 for body size and temperature, both significant trends. Sedentary species show stronger body size trends in some, but not all, analyses. Neither males nor females consistently have stronger body size trends. Additionally, the strength of body size trends does not vary with latitude or body mass. Conclusions Bergmann's rule holds for birds throughout the world, regardless of whether temperature or latitude (as a proxy) is used. Previous studies have suggested that Bergmann's rule is stronger for sedentary than migratory species, males than females and temperate than tropical taxa. I did not find strong support for any of these as general themes for birds, although few studies of tropical taxa have been conducted. The processes responsible for Bergmann's rule remain somewhat of a black box; however, fasting endurance is probably a more important factor than the traditional hypothesis of heat conservation.     

Comparing phylogenetic signal in intraspecific and interspecific body size datasets

Phylogenetic comparative methods have become a standard statistical approach for analysing interspecific data, under the assumption that traits of species are more similar than expected by chance (i.e. phylogenetic signal is present). Here I test for phylogenetic signal in intraspecific body size datasets to evaluate whether intraspecific datasets may require phylogenetic analysis. I also compare amounts of phylogenetic signal in intraspecific and interspecific body size datasets. Some intraspecific body size datasets contain significant phylogenetic signal. Detection of significant phylogenetic signal was dependant upon the number of populations (n) and the amount of phylogenetic signal (K) for a given dataset. Amounts of phylogenetic signal do not differ between intraspecific and interspecific datasets. Further, relationships between significance of phylogenetic signal and sample size and amount of phylogenetic signal are similar for intraspecific and interspecific datasets. Thus, intraspecific body size datasets are similar to interspecific body size datasets with respect to phylogenetic signal. Whether these results are general for all characters requires further study.     

Ecological correlates of geographical range occupancy in North American birds

Aim  The degree to which a species is predictably encountered within its range varies tremendously across species. Understanding why some species occur less frequently within their range than others has important consequences for conservation and for analyses of ecological patterns based on range maps. We examined whether patterns in geographical range occupancy can be explained by species-level traits.
Location  North America.
Methods  We used survey data from 1993 to 2002 from the North American Breeding Bird Survey along with digital range maps produced by NatureServe to calculate range occupancy for 298 species of terrestrial birds. We tested whether species traits explained variation in range occupancy values using linear regression techniques.
Results  We found three species traits that together explained more than half of the variation in range occupancy. Population density and niche breadth were positively correlated with occupancy, while niche position was negatively correlated with occupancy.
Main conclusions  Our results suggest that high range occupancy will occur in species that are common at sites on which they occur, that tolerate a relatively wide range of ecological conditions and that tend to have ranges centred on areas with common environmental conditions. Furthermore, it appears that niche-based characteristics may explain patterns of distribution and abundance from local habitats up to the scale of geographical ranges.     

Phenotypic correlates of yolk and plasma carotenoid concentration in yellow-legged gull chicks

Abstract Carotenoids perform important biological actions in animal tissues, including contributing antioxidant protection. However, the function of transmission of maternal carotenoids to bird eggs is still largely unknown. We made a yolk biopsy of yellow-legged gull (Larus michahellis) eggs and found that the concentration of lutein declined with laying date and across the laying order and increased with egg mass. The concentration of all the main carotenoids (lutein, zeaxanthin, and dehydrolutein) pooled also declined with date and increased with egg mass. We also performed a partial reciprocal cross-fostering of eggs between clutches and investigated the covariation between morphology, T cell-mediated immunity, and plasma carotenoid concentrations of the chicks and carotenoid concentrations in their original eggs. Absolute plasma carotenoid concentrations did not covary with those in the yolk, whereas a positive covariation was found for relative concentrations. Yolk and absolute plasma carotenoid concentrations positively predicted chick body mass and size but not the intensity of the cell-mediated immune response. Thus, yolk carotenoid concentrations may affect chick carotenoid profile and growth, possibly mediating early maternal effects. However, rearing conditions also contributed to determining relative concentrations of circulating carotenoids. Since yolk or plasma antioxidant capacity did not correlate with carotenoid concentrations, future studies of maternal effects mediated by antioxidants should integrate information on carotenoids with information on other components of the antioxidant systems.     

Explanations for bird species range size: ecological correlates and phylogenetic effects in the Canary Islands

Aim To explore the determinants of island occupancy of 48 terrestrial bird species in an oceanic archipelago, accounting for ecological components while controlling for phylogenetic effects. Location The seven main islands of the Canary archipelago. Methods We obtained field data on population density, habitat breadth and landscape distribution in Tenerife, Fuerteventura and La Palma, aiming to sample all available habitats and the gradient of altitudes. In total, 1715 line transects of 0.5 km were carried out during the breeding season. We also reviewed the literature for data on occupancy, the distance between the Canary Islands and the nearest distribution border on the mainland, body size and endemicity of the 48 terrestrial bird species studied. Phylogenetic eigenvector regression was used to quantify (and to control for) the amount of phylogenetic signal. Results The two measurements of occupancy (number of occupied islands or 10 × 10 km UTM squares) were tightly correlated and produced very similar results. The occupancy of the terrestrial birds of the Canary Islands during the breeding season had a very low phylogenetic effect. Species with broader habitat breadth, stronger preferences for urban environments, smaller body size, and a lower degree of endemicity had a broader geographical distribution in the archipelago, occupying a larger number of islands and 10 × 10 UTM squares. Main conclusions The habitat‐generalist species with a tolerance for novel urban environments tend to be present on more islands and to occupy a greater area, whereas large‐sized species that are genetically differentiated within the islands are less widespread. Therefore, some properties of the ranges of these species are explicable from basic biological features. A positive relationship of range size with local abundance, previously shown in continental studies, was not found, probably because it relies on free dispersal on continuous landmasses, which may not be applicable on oceanic islands.     

Development of intraspecific size variation in black coucals,white-browed coucals and ruffs from hatching to fledging

Most studies on sexual size dimorphism address proximate and functional questions related to adults, but sexual size dimorphism usually develops during ontogeny and developmental trajectories of sexual size dimorphism are poorly understood. We studied three bird species with variation in adult sexual size dimorphism: black coucals (females 69% heavier than males), white-browed coucals (females 13% heavier than males) and ruffs (males 70% heavier than females). Using a flexible Bayesian generalized additive model framework (GAMM), we examined when and how sexual size dimorphism developed in body mass, tarsus length and bill length from hatching until fledging. In ruffs, we additionally examined the development of intrasexual size variation among three morphs (Independents, Satellites and Faeders), which creates another level of variation in adult size of males and females. We found that 27–100% of the adult inter- and intrasexual size variation developed until fledging although none of the species completed growth during the observational period. In general, the larger sex/morph grew more quickly and reached its maximal absolute growth rate later than the smaller sex/morph. However, when the daily increase in body mass was modelled as a proportion, growth patterns were synchronized between and within sexes. Growth broadly followed sigmoidal asymptotic models, however only with the flexible GAMM approach, residual distributions were homogeneous over the entire observation periods. These results provide a platform for future studies to relate variation in growth to selective pressures and proximate mechanisms in these three species, and they highlight the advantage of using a flexible model approach for examining growth variation during ontogeny.     

Exploring patterns of interspecific variation in quantitative traits using sequential phylogenetic eigenvector regressions

A number of metrics have been developed for estimating phylogenetic signal in data and to evaluate correlated evolution, inferring broad-scale evolutionary and ecological processes. Here, we proposed an approach called phylogenetic signal-representation (PSR) curve, built upon phylogenetic eigenvector regression (PVR). In PVR, selected eigenvectors extracted from a phylogenetic distance matrix are used to model interspecific variation. In the PSR curve, sequential PVR models are fitted after successively increasing the number of eigenvectors and plotting their R(2) against the accumulated eigenvalues. We used simulations to show that a linear PSR curve is expected under Brownian motion and that its shape changes under alternative evolutionary models. The PSR area, expressing deviations from Brownian motion, is strongly correlated (r= 0.873; P < 0.01) with Blomberg's K-statistics, so nonlinear PSR curves reveal if traits are evolving at a slower or higher rate than expected by Brownian motion. The PSR area is also correlated with phylogenetic half-life under an Ornstein-Uhlenbeck process, suggesting how both methods describe the shape of the relationship between interspecific variation and time since divergence among species. The PSR curve provides an elegant exploratory method to understand deviations from Brownian motion, in terms of acceleration or deceleration of evolutionary rates occurring at large or small phylogenetic distances.