Spotlight: Citizen Science and Rusty Collars in Ruffs

by Deborah Buehler originally published in Wader Study 128(1)

Some birds love their fashion.

Even waders – known for more practical, muted colours and ‘outfits’ that camouflage – have species amongst them that love to show off their plumage.

Ruffs Calidris pugnax have famously extravagant plumage. They’re even named for the typical male’s feathery neck ruffle resembling the exaggerated ruffs fashionable from the mid-sixteenth to mid-seventeenth centuries. In this issue of Wader Study, Verkuil, Jukema and colleagues report on what might seem like an accessory to Ruffs’ already flamboyant fashion – some Ruff individuals have a more understated collar, a rusty-brown ring around the neck or nape.¹

As with many things in science, the rusty neck rings (hereafter collars) were first discovered through close observation. Humans have been catching waders in Friesland, the Northern Netherlands, for a long time. For centuries, this activity centred around hunting birds for food. The trappers, known as wilsterflappers, used wind-driven nets, decoys and perfect timing to capture flocks of birds in midair. In the late 1970s, when commercial hunting was prohibited, some of them turned their unique skills to science. Joop Jukema, a retired potato farmer, and one of the study’s co-authors, has been trapping waders with scientists since the early 1980s. He and his fellow wilsterflappers (see the study’s Acknowledgements section) are classic citizen scientists. They are not scientifically trained, but they collect information for scientific study and their deep understanding of the birds was instrumental in discovering the rusty collars.

Once the rusty collars had been discovered, Verkuil, Jukema and colleagues set out to gather more information about them. They scored the presence or absence of the collars through field work conducted over many years and sites: Most of the birds, over 2,000 males and females, were captured and scored when migrating through the northern Netherlands between 1996 and 2019. In 1996 a single female was checked at the Willem Barents field station at Medusa Bay in Russia during breeding. In 2017, the researchers captured and checked 49 females in Finland during the breeding season. In 2018, they checked skins in the Moscow Zoological Museum from 73 females caught in Russia during breeding between 1903 and 2004.

Reliably seeing the collars was no small feat. In fact, the existence of the rusty neck collar was often scored as ‘unknown’, especially in two of the three male types: the independent and satellite males. Ruffs have one of the weirdest sexual systems in the world with three distinct types of male: territorial, ‘independent’ males with predominantly dark ornamental ruffs; non-territorial ‘satellite’ males, with predominantly white ruffs; and rare female-mimicking males (called faeders), with no ruffs and oversized testicles. These faeders were also first discovered in the northern Netherlands. Joop Jukema noticed that he was catching large ‘females’ (note that the testicles are inside the body in birds) and he started to doubt that they were what they seemed. ² The discovery and subsequent introduction of faeders to the scientific community triggered intense study into the sex lives of Ruffs. We now know that the female-mimicking faeders exist because a large chunk of chromosome 11 (~ 100 genes) flipped upside-down about 3.8 million years ago. More recently, about 500,000 years ago, part of the upside-down chunk flipped back forming the satellite male type. ³

So why were the rusty collars so hard to see in the independent and satellite males? Because in spring they ‘change their outfits’. All birds moult (shed old feathers to make way for new growth) and some species, including Ruffs, have complex annual moult cycles. ⁴ Independent and satellite males migrating through the Netherlands in spring shed all their neck feathers to make way for their ornamental ruffs and the feathers that would have had the rusty neck collar are simply gone.

This is why the existence of the rusty neck collar was so often scored as ‘unknown’ in males as spring progressed. It is also why the researchers decided to exclude males entirely from their analysis during the breeding period. During breeding, they scored only females (and very rare faeders) where the collar was clearly present or not. In females and faeders some feathers are replaced in spring, but the moult is less drastic and so it was still possible to detect the rusty neck collars.

The researchers also wanted to determine the origin of the colour in the rusty collars. They hypothesized two alternatives: Perhaps the collars were due to genetic plumage polymorphism (ancient differences in feather colouration). Some closely related plover species have similar collars, suggesting that this may have been the recurrence of an ancestral trait (atavism). On the other hand, maybe the collars were not a fixed trait at all, but rather an acquired trait. The feathers could simply be stained. Rusty stained feathers can occur when birds feed in water or mud that contains high levels of iron oxide. To test this, the authors collected a total of nine feather samples from the rusty-brown neck collars from birds migrating through the Netherlands in 2011 and 2019. To test if the feathers contained iron oxide, they performed a simple experiment. They took photos of the feathers, then soaked them for 24 hours in 5% hydrochloric acid (HCl), then photographed them again. The idea was that if the colour washed off and the wash then tested positive for iron oxide, the researchers could safely state that the colour was due to recently acquired staining rather than ancestral genetics.

Verkuil, Jukema and colleagues found that the rusty-brown neck collar occurred fairly commonly in Ruffs migrating through The Netherlands in spring. They detected collars in 14% of females, 20% of independent males and 40% of satellite males. The neck collars appeared rarer in faeders at 3.5%, but faeders themselves make up only 1% of the staging Ruff population studied and so the sample size was low (only 28 scored across all years). Overall, of the 2,098 Ruffs scored in The Netherlands between March and May 2006–2019, 395 birds (18.8%) had a neck collar. In the spring, males seem to have collars more often than females, and satellite males more often than all other sexes. However, it is easier to detect a rusty coloured ring on a background of white in satellite males, thus, this difference might be due to detection bias.

In contrast to spring in the Netherlands, the collars were uncommon during the breeding season elsewhere. Although the single female checked from Medusa Bay in Russia in 1996 had a brown neck ring, no rusty-brown neck collars were observed among any of the 49 females from the breeding population in Finland in 2017. Similarly, no rusty collars were found in the 73 females checked from the collection in the Moscow Zoological Museum.

One clear outcome of the study was the likely cause of the neck collars. Through their experiment, the researchers determined that the rusty colour washed off in 5% hydrochloric acid. Furthermore, all collar feathers tested positive for iron. Therefore, the likely cause of the neck collar is recently acquired staining by iron oxide and not ancestral genetic polymorphism.

Exactly where and how the feathers ended up stained, remains a mystery. Ruffs feed along the receding water line, where they often submerge their heads in water with a film of iron-rich bacteria. Iron containing surface water occurs in the floodplains in West Africa where a large proportion of Ruffs spend the winter, at stopover sites in southern Spain, and in many grassland areas in northern Europe. This study was not able to detect whether the staining was related to a particular wintering or staging area.

The study also wasn’t set up to answer the question of whether the collars mean anything for Ruff fashion. Iron oxide staining has been used by bird species for cosmetic colouration, ⁵ but we don’t yet know if this staining plays a role in sexual selection for Ruffs. Much more remains to be discovered and the authors also published this study as a call to field researchers to pay attention to this newly described plumage characteristic. Hopefully, this heightened awareness will contribute to more knowledge about the phenomenon in the future.

That’s the beauty of science. Each study gives us new information while raising more questions. Though Ruffs might love to show off their plumage and their rusty collars might be akin to ‘fast fashion’, at its core, this study highlights something slower and longer lasting. It highlights the power of sustained observation, year after year, and the labour (often unpaid) of the scientists and citizen scientists who have broadened our understanding of waders and their perils. ⁶

 

1. Verkuil, Y., J. Jukema, P. S. Tomkovich, N. Rönkä, J. C. E. W Hooijmeijer & T.Piersma. 2021. Striking rusty-brown neck collars in Ruffs: plumage polymorphism or staining? Wader Study 128(1): 36-43.

 

2. L. E. Ogden. 2014. In the world of ruffs, a male bird that’s sneaky … and well endowed. Earthtouch News Network. Blog post accessed 9 March 2021 at https://www.earthtouchnews.com/natural-world/animal-behaviour/in-the-world-of-ruffs-a-male-bird-thats-sneaky-and-well-endowed/

 

3. Küpper, C., M. Stocks, J.E. Risse, N. dos Remedios, L.L. Farrell, S.B. McRae, T.C. Morgan, N. Karlionova, P. Pinchuk, Y.I. Verkuil, A.S. Kitaysky, J.C. Wingfield, T. Piersma, K. Zeng, J. Slate, M. Blaxter, D.B. Lank & T. Burke. 2016. A supergene determines highly divergent male reproductive morphs in the Ruff. Nature Genetics 48: 79–83.

 

4. Pyle, P. 2019. Sunset Sanderlings: Digital photography leads to novel insights about the presupplemental molt of the Sanderling. Birding Magazine August 2019: 30–40.

 

5. Delhey, K., A. Peters & B. Kempenaers. 2007. Cosmetic coloration in birds: occurrence, function, and evolution. American Naturalist 169: S145–S158.

 

6. Piersma, T. 2018. Behind the Paper: The Natural History of Our Changing Planet. Nature Portfolio Ecology & Evolution Community. Blog post accessed 9 March 2021 at https://natureecoevocommunity.nature.com/posts/39860-the-natural-history-of-our-changing-planet?channel_id=521-behind-the-paper