Macroecology

ongoing
Author

Kaspar Delhey, Mihai Valcu, Cristina Valcu

Published

September 1, 2012

1 Macroecology

2 Evolutionary ecology of bird colours

2.1 Climate and colour evolution

Ecogeographical rules link bird phenotypes to spatial variation in climate and other environmental variables. Prominent ecogeographical rules describe the effects of climatic variation on size (Bergmann’s rule), appendage size (Allen’s rule), or coloration. Ecogeographical rules that refer to animal coloration include Gloger’s rule - which predicts darker animals in wetter regions - and the thermal melanism hypothesis (Bogert’s rule) - which predicts darker animals in colder regions.

An illustration of the effect of rainfall on plumage coloration. The dark coloured Eastern Whipbird (Psophodes olivaceus, left) is an inhabitant of more humid coastal regions in Australia while the closely related Chirruping Wedgebill (Psophodes cristatus, right), with its lighter-coloured plumage, lives in the arid and semi-arid interior of the continent (photos: Kaspar Delhey).

An illustration of the effect of rainfall on plumage coloration. The dark coloured Eastern Whipbird (Psophodes olivaceus, left) is an inhabitant of more humid coastal regions in Australia while the closely related Chirruping Wedgebill (Psophodes cristatus, right), with its lighter-coloured plumage, lives in the arid and semi-arid interior of the continent (photos: Kaspar Delhey).

Our work revealed that both ecogeographical rules seem to apply to bird colours at a global scale (Delhey et al. 2019): birds are darker in regions that are wetter, and in colder regions. The most likely selection force behind the correlation between colour and temperature is thermoregulation: darker birds absorb more solar radiation, which is advantageous in cold environments, whereas lighter colours may be selected in warmer regions to avoid overheating. The selection mechanisms behind the effects of rainfall are less clear. Darker birds may be better camouflaged in darker, forested environments which are common in wet regions. Alternatively, selection may favour darker plumage because it makes feathers more resistant to abrasion and bacterial degradation, and these processes are more prevalent in humid and densely vegetated habitats.

Global distribution of plumage lightness across all passerine birds. Warmer colours indicate bird assemblages with lighter plumage colours.

Global distribution of plumage lightness across all passerine birds. Warmer colours indicate bird assemblages with lighter plumage colours.

We also found that the effects of rainfall on bird colours are much stronger than the effects of temperature. Depending on the geographic patterns of covariation between temperature and precipitation, climatic effects can work in concert and reinforce each other or work against each other. In the latter case, precipitation effects generally prevail over temperature effects, which explains why birds of the wet tropics are generally darker coloured. Correct interpretation of the ecogeographical rules of colour and how climatic effects interact is needed to predict potential effects of climate change. This led us to develop a framework to generate predictions associated with changes in temperature and precipitation (Delhey et al. 2020).

Currently, we are shifting our focus from variation in colour between species to variation within species, which should take us closer to the level at which selection is acting. We are using citizen science data on colour variation of European species (Common buzzard, Buteo buteo) and colour measurements of museum specimens of Australian birds to quantify the association between climatic factors and colour variation.

2.2 Migratory birds have lighter colours

One interesting spin-off of our work on climate and bird colour was inspired by recent research showing that long-distance migratory birds ascend rapidly after dawn and fly at higher altitudes during day than during night (doi.org/10.1016/j.cub.2021.05.047, doi.org/10.1126/science.abe7291). One explanation of this behaviour is that birds migrate at higher altitudes, where the air is colder, to reduce the risk of overheating during the day. We hypothesised that if overheating due to solar radiation was an important selection force affecting migratory birds, the thermal melanism hypothesis would predict lighter coloured plumage in migratory species. This was indeed the case: across all species we found that long distance migratory birds had on average lighter plumage colours than short-distance migrants which in turn were lighter coloured than resident species (Delhey et al. 2021).
Our research inspired a poem (see thepoetryofscience). A first for us!

(A) Plumage lightness increases with migratory behaviour across birds. (B) A flock of Sanderlings (Calidris alba), a long-distance migratory shorebird, which may benefit from being lighter coloured to avoid overheating during migration. Photo by Pablo F. Petracci.

(A) Plumage lightness increases with migratory behaviour across birds. (B) A flock of Sanderlings (Calidris alba), a long-distance migratory shorebird, which may benefit from being lighter coloured to avoid overheating during migration. Photo by Pablo F. Petracci.

2.3 The colours of all birds

Birds come in a large variety of colours. While we have made substantial advances in understanding why some species are more colourful than others and in why males and females differ in colouration, it still remains unclear what makes different species have different colours. We were interested in answering basic questions such as why are ravens black, swans white and parrots green. A substantial set of theories and hypotheses exists to explain such variation, but these have not yet been put to the test at a large scale (all birds). In an attempt to address this issue (Delhey et al. 2023), we used book plates to quantify the proportion of the body covered by each of 12 colour categories for most species of birds.

Computing colour variables. (A) We used handbook plates to quantify colour variation in human-visible CIELAB colour space, which has one achromatic axis of variation (L) and two chromatic axes (a, b). In (B), we show the same variation in 2-dimensions for ease of visualization (a and b chromatic coordinates, ignoring variation in L, the equivalent of looking at (A) from above), and overlay the position of the colours of two species (blue symbols: Blue Tit, Cyanistes caeruleus; red symbols: White-rumped Sandpiper, Calidris fuscicollis), chosen because their average colour coordinates (large blue and red circles in the centre) are similar despite having very different colours. Thus, computing the overall L, a, and b averages obscures the important differences in colour between these species. Instead, we computed the proportion of the pixels in each image that fall within specific sections of colour space (SI Appendix, Fig. S1 in (Delhey et al. 2023)) to obtain 12 colour variables per species. These values are depicted in (C) for both species (blue and red dots), overlaid on violin plots that represent the distribution of each colour variable across all images (horizontal line is the median, and fill colour the average colour of each category). Thus, despite similar overall average colours, Blue Tits score higher in blue and yellow, while White-rumped Sandpipers score higher for black and white. Bird figures ©Lynx Edicions /Cornell Lab of Ornithology/Birds of the World. Illustrated by Hilary Burn and Francesc Jutglar.

Computing colour variables. (A) We used handbook plates to quantify colour variation in human-visible CIELAB colour space, which has one achromatic axis of variation (L) and two chromatic axes (a, b). In (B), we show the same variation in 2-dimensions for ease of visualization (a and b chromatic coordinates, ignoring variation in L, the equivalent of looking at (A) from above), and overlay the position of the colours of two species (blue symbols: Blue Tit, Cyanistes caeruleus; red symbols: White-rumped Sandpiper, Calidris fuscicollis), chosen because their average colour coordinates (large blue and red circles in the centre) are similar despite having very different colours. Thus, computing the overall L, a, and b averages obscures the important differences in colour between these species. Instead, we computed the proportion of the pixels in each image that fall within specific sections of colour space (SI Appendix, Fig. S1 in (Delhey et al. 2023)) to obtain 12 colour variables per species. These values are depicted in (C) for both species (blue and red dots), overlaid on violin plots that represent the distribution of each colour variable across all images (horizontal line is the median, and fill colour the average colour of each category). Thus, despite similar overall average colours, Blue Tits score higher in blue and yellow, while White-rumped Sandpipers score higher for black and white. Bird figures ©Lynx Edicions /Cornell Lab of Ornithology/Birds of the World. Illustrated by Hilary Burn and Francesc Jutglar.

We found that the most common bird colours were black and white and shades of grey and brown. More saturated colours such as yellow, green, red, blue and purple were much rarer. Females were more likely to be coloured brown, light grey or yellow, while males had more black, blue, red, purple and green. In general colours that are more common in males are ornamental colours used to attract mates or repel rivals, while common female colours tend to be more cryptic. Such colours tended to be favoured by strong sexual selection on males (polygynous species).

We find strong support for the idea that vegetation structure affects colour evolution because variation in background colours and light conditions determine which colours are good signals or serve to camouflage. Colours that are optimally cryptic in dense vegetation (e.g. forests) are not the same as colours good for camouflage in a desert. On average, forests were more likely to harbour cryptic colours such as green, yellow or brown, and potentially signalling ones such as red or blue. White plumage was more common in species that live in open habitats.

Birds more vulnerable to predators (smaller species and species that nest near or on the ground) tend to be coloured with more cryptic colours such as browns, light grey, green or yellow, while less vulnerable species (larger species that nest in safe locations) were more often coloured black, red and blue. We also found general support for the effects of climate and migration (see above).

While we found support for many of the existing theories and predictions, large amounts of colour variation remain unexplained. Differences in colour between species may have evolved to avoid hybridization, something that was not captured in our analyses. We are currently working on evaluating this possibility.

3 The macroecology of life-history traits

3.1 Extra-pair paternity

Extra-pair paternity is a key aspect of the mating behaviour of birds. The frequency of extra-pair paternity varies not only among individuals (see The zebra finch and The Blue Tit study systems), but also among populations and species. We explored the geographical variation in the frequency of extra-pair paternity among populations, species and species assemblages.

At population level, the frequency of extra-pair paternity decreases with latitude and increases with the distance from the breeding range boundary within the species’ breeding range.

The predicted proportion of broods with extra-pair offspring across the breeding range of the Blue Tit (Cyanistes caeruleus). Populations for which EPP estimates are available are marked in red.

The predicted proportion of broods with extra-pair offspring across the breeding range of the Blue Tit (Cyanistes caeruleus). Populations for which EPP estimates are available are marked in red.

At species level, the frequency of extra-pair paternity is negatively associated with generation length and pair-bond duration among species. At assemblage level (all the species existing in a particular area), the frequency of extra-pair paternity has a strong geographical signature: the highest values are found in the Palearctic and Nearctic realms and the frequency of extra-pair paternity decreases with latitude within the zoogeographical realms.

Global distribution of the proportion of extra-pair broods at assemblage-level.

Global distribution of the proportion of extra-pair broods at assemblage-level.

Our study suggests that the frequency of extra-pair paternity is the product of influences of multiple environmental, ecological and life-history factors and therefore follows a complex pattern of geographical variation. The results support the hierarchical explanation for variation in extra-pair paternity (C.-M. Valcu, Valcu, and Kempenaers 2021).

Extra-pair paternity can increase the variance in male reproductive success, and may thus intensify sexual selection and drive sexual dimorphism. In a further study, we investigated the connection between extra-pair paternity and sexual dimorphism in wing length and plumage colouration. Size and colour dimorphism are predicted by different reproductive, social and life-history traits, but extra-pair paternity plays a role in the evolution of both forms of dimorphism. High extra-pair paternity levels are associated with sexual dichromatism, positively in species in which males are more colourful and negatively in those in which females are more colourful. However, high extra-pair paternity rates are associated with increased wing length dimorphism in species with both male- and female-biased dimorphism (M. Valcu, Valcu, and Kempenaers 2023).

Extra-pair paternity predicts sexual dimorphism in avian species.

Extra-pair paternity predicts sexual dimorphism in avian species.

Currently, we are investigating the link between extra-pair paternity and sexual dichromatism arising from different mechanisms of colour production and in different body parts.

3.2 Song frequency

Most birds use acoustic signals to communicate. The properties of these signals are both under strong natural selection, because the environment influences sound propagation, and sexual selection, because signal frequency correlates with body size and sounds with different frequencies are perceived differently. To test these hypotheses, we analysed variation in peak song frequency in passerine species.

Distribution of peak song frequency across passerines around the globe.

Distribution of peak song frequency across passerines around the globe.

Song frequency decreases with increasing body mass and with male-biased sexual size dimorphism. However, we found no association between habitat and sound frequency. Fig 2a. Associations between peak song frequency and body mass, sexual size dimorphism and tree cover across passerines. Our study suggests that the global variation in passerine song frequency is mostly driven by natural and sexual selection causing evolutionary shifts in body size rather than by habitat-related selection on sound propagation (Mikula et al. 2021).

3.3 Timing of activity

Species vary widely in their timing of activity. Species which are active outside of the time period typical for the taxonomic order to which they belong are referred to as ‘time-shifters’. The evolution of nocturnality and the existence of time-shifters has been linked to two forms of competition: (i) direct interference competition (defending resources, imposing harm on competitors) and (ii) indirect exploitation competition (competition for resources). We investigated the relative importance of these two forms of competition on the occurrence of time-shifting among avian predator species.

Global distribution of the number of species (i.e. species richness) for day-active avian predators.

Global distribution of the number of species (i.e. species richness) for day-active avian predators.

Despite phylogenetic constraints, avian predators partition their time of activity to minimize the costs of direct interactions with competitors. Body size, as a proxy for competitive ability, appears to influence this partitioning strategy. Our study highlights the importance of interference competition as an evolutionary driver of time-shifting and suggest a role of body size in mediating the mechanism of time partitioning (Pei, Valcu, and Kempenaers 2018).

3.4 Parental investment

Maternal investment (e.g. clutch size, egg size) varies among species with different mating systems, as well as within the breeding range of each species, depending on the environmental conditions of the breeding location. Meanwhile, previous research from our group indicates that breeding site fidelity and the opportunity for local adaptation vary among species with different mating systems (Kempenaers and Valcu 2017; Kwon et al. 2022). Based on these findings, we predict different degrees of inter-population differentiation of maternal investment in monogamous and polygamous species, respectively. We are currently investigating the relationship between maternal investment, and the mating environment and mating system in shorebirds, known for their wide range of mating and parental care systems (Bulla et al. 2016).

4 Resources

We developed rangeMapper (M. Valcu, Dale, and Kempenaers 2012), an open source front end R package for macroecological studies designed to serve as an interface between the spatial and the statistical tools offered through the R environment. We also developed and actively maintain a comprehensive database that links life-history traits of the world’s 10,000 bird species with environmental and ecological data.

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References

Bulla, Martin, Mihai Valcu, Adriaan M. Dokter, Alexei G. Dondua, András Kosztolányi, Anne L. Rutten, Barbara Helm, et al. 2016. “Unexpected Diversity in Socially Synchronized Rhythms of Shorebirds.” Nature 540 (7631): 109–13. https://doi.org/10.1038/nature20563.
Delhey, Kaspar, James Dale, Mihai Valcu, and Bart Kempenaers. 2019. “Reconciling Ecogeographical Rules: Rainfall and Temperature Predict Global Colour Variation in the Largest Bird Radiation.” Edited by Greg Grether. Ecology Letters 22 (4): 726–36. https://doi.org/10.1111/ele.13233.
———. 2020. “Why Climate Change Should Generally Lead to Lighter Coloured Animals.” Current Biology 30 (23): R1406–7. https://doi.org/10.1016/j.cub.2020.10.070.
———. 2021. “Migratory Birds Are Lighter Coloured.” Current Biology 31 (23): R1511–12. https://doi.org/10.1016/j.cub.2021.10.048.
Delhey, Kaspar, Mihai Valcu, Christina Muck, James Dale, and Bart Kempenaers. 2023. “Evolutionary Predictors of the Specific Colors of Birds.” Proceedings of the National Academy of Sciences 120 (34): e2217692120. https://doi.org/10.1073/pnas.2217692120.
Kempenaers, Bart, and Mihai Valcu. 2017. “Breeding Site Sampling Across the Arctic by Individual Males of a Polygynous Shorebird.” Nature 541 (7638): 528–31. https://doi.org/10.1038/nature20813.
Kwon, Eunbi, Mihai Valcu, Margherita Cragnolini, Martin Bulla, Bruce Lyon, and Bart Kempenaers. 2022. “Breeding Site Fidelity Is Lower in Polygamous Shorebirds and Male-Biased in Monogamous Species.” Edited by Michael D Jennions. Behavioral Ecology 33 (3): 592–605. https://doi.org/10.1093/beheco/arac014.
Mikula, Peter, Mihai Valcu, Henrik Brumm, Martin Bulla, Wolfgang Forstmeier, Tereza Petrusková, Bart Kempenaers, and Tomáš Albrecht. 2021. “A Global Analysis of Song Frequency in Passerines Provides No Support for the Acoustic Adaptation Hypothesis but Suggests a Role for Sexual Selection.” Edited by Greg Grether. Ecology Letters 24 (3): 477–86. https://doi.org/10.1111/ele.13662.
Pei, Yifan, Mihai Valcu, and Bart Kempenaers. 2018. “Interference Competition Pressure Predicts the Number of Avian Predators That Shifted Their Timing of Activity.” Proceedings of the Royal Society B: Biological Sciences 285 (1880): 20180744. https://doi.org/10.1098/rspb.2018.0744.
Valcu, Cristina-Maria, Mihai Valcu, and Bart Kempenaers. 2021. “The Macroecology of Extra-Pair Paternity in Birds.” Molecular Ecology 30 (19): 4884–98. https://doi.org/10.1111/mec.16081.
Valcu, Mihai, James Dale, and Bart Kempenaers. 2012. rangeMapper : A Platform for the Study of Macroecology of Life-History Traits.” Global Ecology and Biogeography 21 (9): 945–51. https://doi.org/10.1111/j.1466-8238.2011.00739.x.
Valcu, Mihai, Cristina Valcu, and Bart Kempenaers. 2023. “Extra-Pair Paternity and Sexual Dimorphism in Birds.” Journal of Evolutionary Biology 36 (5): 764–79. https://doi.org/10.1111/jeb.14172.