Saturday, August 31, 2019

Shining a Light on Nightbird Evolution: My First First-author Paper!

As I previously mentioned on this blog, I'd been hoping to have the first part of my PhD research submitted to a journal by the time I had reason to blog about it again. I'm pleased to report that my research has now not only been submitted, but published! Diversity (the journal I submitted to) processed the article unbelievably quickly, having it reviewed, edited, accepted, and published in less than a month! I was also fortunate in that the reviewers didn't request any major changes. I certainly don't expect to go through such a painless submission experience again anytime soon.

For this study, my coauthors and I looked at the phylogenetic relationships of a remarkable group of theropods, Strisores. Many strisoreans* are well-camouflaged birds that are active at night or twilight; these include the nightjars, oilbirds, potoos, frogmouths, and owlet-nightjars. However, the diurnal swifts and hummingbirds are also members of Strisores. Most strisoreans (including the predominantly nectar-feeding hummingbirds) eat insects, but the oilbird (Steatornis caripensis) feeds exclusively on fruit.

*I used this new paper as an opportunity to make the case that "strisorean" should be the vernacular form for Strisores, for much the same reasons that I now use "enantiornithean" instead of "enantiornithine". Time will tell whether anyone else follows this...

A cartoon depiction of the major strisorean subgroups and their inferred phylogenetic relationships based on our new study.

Traditionally, the nocturnal strisoreans have been classified as one group, but recent studies have presented strong evidence that the owlet-nightjars are more closely related to swifts and hummingbirds than to the rest. (The group uniting owlet-nightjars, swifts, and hummingbirds has been named Daedalornithes.) When it comes to the phylogenetic relationships among the remaining groups, however, little consensus exists. In fact, up until recently, no two phylogenetic datasets aimed at resolving their relationships found the exact same results!

We approached this problem by combining the largest genetic and anatomical datasets that have been assembled for Strisores so far. The genetic dataset was originally put together for a different study by my coauthors Noor White and Mike Braun (accepted at Molecular Phylogenetics and Evolution but not yet published online at the time of writing) and the anatomical dataset came from a 2013 study by Dan Ksepka and colleagues.

The results of selected previous studies on strisorean phylogeny. Up until White and Braun (2019) found an identical topology to Prum et al. (2015), no two datasets produced the same result!

When we analyzed our combined dataset, we found that nightjars were best supported as the most distantly related group to other living strisoreans. The oilbird and potoos were united in one group, which was in turn closely related to a clade containing the frogmouths and daedalornitheans. This result was not only identical to what we found when we analyzed our genetic dataset on its own, but also to the findings of a previous genetic study by Richard Prum and colleagues. Although it is never wise to unilaterally declare a case closed in science, the fact that two large datasets independently recovered the same results suggests to me that this is indeed the most likely phylogenetic tree for Strisores.

In fact, we felt that the support for a group including all strisoreans except nightjars was strong enough that we chose to give it a name: Vanescaves. This name translates to "vanishing birds", partly a nod to the Emily Dickinson poem "A Route of Evanescence", which describes a hummingbird flying near some flowers. The name also references the fact that many vanescavian subgroups currently have geographically restricted ranges (oilbirds and potoos in the Neotropics, frogmouths in Australia and Southeast Asia, and hummingbirds in the Americas), but are known from the fossil record to have once lived in other regions, such as Europe. In contrast, nightjars are distributed almost globally today, but have very little of a documented fossil record.

One of the resulting phylogenetic trees we recovered in our study, scaled to geologic time. (The divergence times are largely bare minima necessary to accommodate known fossil ages and should not be taken literally.)

Speaking of fossils, one of the main benefits of combining genetic and anatomical data in our study was that it allowed us to place fossil species in the context of our phylogenetic results. Despite their small body size and delicate, sometimes literally paper-thin bones, a diverse range of fossil strisoreans have been identified in Eocene fossil deposits (33.9-56 million years old). In general, most fossil strisoreans included in our study fell out in parts of the tree that we expected them to based on previous research, but we did find a few surprises.

For example, we found that the oilbird may be the closest living relative to Fluvioviridavis, a 52-million-year-old strisorean from Wyoming, unlike previous phylogenetic analyses which found Fluvioviridavis as a close relative of frogmouths. This is a notable result given that paleornithologist Gerald Mayr previously noted features in Fluvioviridavis that are more similar to oilbirds than to frogmouths.

The holotype of Fluvioviridavis, from Nesbitt et al. (2011), under CC BY 2.5.

We also discovered that Hassiavis, a 47-million-year-old strisorean from Germany that had not been previously subjected to phylogenetic analysis, was potentially an early member of the owlet-nightjar lineage, which would make it the oldest known stem-owlet-nightjar and the first one known from outside of Australasia, identifying owlet-nightjars as yet another vanescavian group with a formerly much broader distribution. (However, it should be noted that not all of our analyses recovered Hassiavis as a stem-owlet-nightjar. In any case, we found that it was most likely a daedalornithean.)

Our research additionally allowed us to make new inferences about the evolution of strisorean anatomy. Previous studies that considered only anatomical data tended to recover nightjars, potoos, and daedalornitheans as a group. These strisoreans are often specialized for snapping up insects in flight, in contrast to the fruit-eating oilbird and the big-beaked frogmouths (which instead more commonly pounce on prey on the ground). According to previous morphology-based hypotheses, this would imply that aerial insectivory originated relatively late in strisorean evolution. However, the phylogeny we found has the oilbird and frogmouths nested among the insect-hawking groups, suggesting that they descended from ancestors that similarly hunted insects on the wing.

Nightjars and other insect-hawking strisoreans have such specialized-looking anatomy that it may seem counterintuitive that they represent the ancestral state for Strisores. However, there may be a parallel example in other flying vertebrates: bats likely also started out as aerial insectivores, and they too evolved into fruit-eaters, vertebrate predators, and nectar-feeders. Furthermore, our phylogenetic results really only imply two losses of aerial insectivory (once in the oilbird and once in frogmouths), which does not come across as an unbelievably high number to me.

The skull of a common potoo (Nyctibius griseus), viewed from the right. The giant eyes and broad palate, among other things, make this a very bizarre skull!

Is there any support for this in the fossil record? Maybe! We found that Protocypselomorphus, a small strisorean from the Eocene of Germany that was likely an aerial insectivore, may have been more closely related to the oilbird than to any other living strisorean. If this is correct, it would provide evidence that the oilbird had insect-hawking ancestors. Indeed, the often-prescient Gerald Mayr had already pointed out that Protocypselomorphus shares certain features in common with the oilbird. That being said, the majority of fossil strisoreans in our study were already very anatomically similar to their closest living relatives, so a clearer picture of what the ancestral strisorean looked like may depend on the discovery of even older fossils.

One question I've frequently received when discussing this research is whether hummingbirds and swifts evolved from nocturnal ancestors. We did not focus on this interesting topic for this study, but I personally think that we do not yet have enough information to answer this question conclusively. If one assumes that gaining and losing nocturnality are equally likely, it's true that the most straightforward interpretation is that strisoreans were ancestrally nocturnal and then became diurnal on the line leading to hummingbirds and swifts. However, it is not clear that such an assumption is correct. Furthermore, there is evidence that different groups of nocturnal strisoreans have adapted to darkness in different ways: the eyes of nightjars and potoos have a reflective layer that helps them capture more light at night, whereas other strisoreans appear to lack this feature. Thus, the notion that nocturnality originated several times in strisoreans may also be plausible.

If you've seen me present this study at conferences, you may remember that I also intended to perform divergence time estimation on Strisores. We ultimately decided to forgo that part of the study, because the massive size of our genetic dataset made divergence time estimation very computationally expensive and time consuming. However, I may still attempt such an analysis on a smaller dataset for a future manuscript. Stay tuned...

Reference: Chen, A., N.D. White, R.B.J. Benson, M.J. Braun, and D.J. Field. 2019. Total-evidence framework reveals complex morphological evolution in nightbirds (Strisores). Diversity 11: 143. doi: 10.3390/d11090143

Tuesday, July 30, 2019

Chester Zoo

Having heard many good things about the Chester Zoo, it was only a matter of time before I planned a trip there. I was very impressed by both the exhibit design and collection of rarely-seen species. I took more than enough photos to split this trip report into several separate posts, but I unfortunately don't have time to write more than one at the moment, so a highlights reel will have to do.

It's not every zoo where you get to see an Indian rhinoceros right off the bat.

A nearby aviary houses several bird species, including northern bald ibises. This is such a large aviary that unless the birds are standing right next to the viewing area, it can be difficult to see them clearly without binoculars! (Luckily, I almost always carry a pair with me.)

Cinereous vultures also live in this aviary. (This one was cooperatively standing near the mesh.)

I spent a good amount of time in the Tropical Realm building, which houses numerous species of free-flying tropical birds. If this hadn't been my first trip to the zoo, I probably could have been persuaded to spend most of my day there just looking for all the species. (I did end up seeing most of them.) Here is a Palawan peacock pheasant.

A Madagascar fody taking a bath while a Java sparrow and a red-billed leiothrix look on.

A sunbittern on a light fixture.

In addition to the free-flying birds, lining the walls of the Tropical Realm are separate aviaries housing even more species. Here is a pink pigeon. In 1991, only ten individuals of this Mauritian bird were left and it was considered critically endangered. Thanks to successful conservation efforts, its conservation status has been downlisted to vulnerable.

A great hornbill, one of the largest hornbills. Chester Zoo has a great collection of hornbills; I counted at least five species on my visit (great, Visayan, wrinkled, rhinoceros, and red-billed).

Not a hornbill, but a toucan. A green aracari, to be specific.

Two blue-naped mousebirds. Picking favorite birds is always difficult for me, but mousebirds have to be high on the list for their distinctiveness and their rich Paleogene fossil record.

A Congo peafowl, a species that wasn't scientifically described until the 20th Century.

A superb fruit dove.

A blue-necked tanager.

A pair of collared trogons.

The Tropical Realm also contains exhibits for amphibians, such as this false tomato frog.

There are non-avian reptiles as well, like this Graham's anole.

The species I'd most wanted to see at Chester though was the tuatara, and I'm happy to report that my wish was granted! I've now seen the world's only extant rhynchocephalian.

I also saw bush dogs for what I think is the first time. These small South American canids are very social, allowing them to prey on animals larger than themselves. They are housed in a different tropics-themed exhibit, the Spirit of the Jaguar.

In general, I liked the exhibit signage at the Chester Zoo (as we shall see), but one of the accompanying signs for the bush dogs did contain a glaring error. (Coatis are not rodents.) (Update: Surprisingly, the outreach team at the zoo responded to my tweet about this and has said they're working on fixing this. Huzzah!)

Yet another tropics-themed exhibit is the Realm of the Red Ape, a two-story building that allows visitors to view orangutans and gibbons high above ground. It was quite impressive, but I was more distracted by the blue-crowned hanging parrots, and can you blame me?

Upon exiting the Realm of the Red Ape, the zoo suggests several animal-themed recipes that make use of products with sustainable palm oil.

A babirusa showing off its unusual upwards-curving tusks.

This red forest duiker is exhibited alongside okapis. No doubt it gets regularly mistaken for a juvenile okapi by visitors.

Dragons in Danger is another indoor exhibit, this time named after its Komodo dragons. However, it also houses a variety of other animals, including many Southeast Asian birds. Due to the dense vegetation and dim lighting, the birds were quite hard to spot, but I did see this (very loud) Asian fairy bluebird.

Nearby is a surprisingly large exhibit for giant Hispaniolan galliwasps (shared with mountain chickens, a type of frog).

Islands is a relatively new exhibition area at Chester (having opened in 2015), and it features animals from Southeast Asian islands and New Guinea, such as this southern cassowary.

Islands also includes a walkthrough aviary for even more Southeast Asian birds, including the critically endangered Bali myna. Unfortunately, one of the other major exhibits at Islands, the Monsoon Forest, was partially destroyed by a fire in December 2018. Most of the inhabitants were rescued and relocated to other parts of the zoo, but a number of smaller animals did not make it.

A large chunk of the Chester Zoo is devoted to African animals. Here is a black stork, part of a large wetland aviary.

A black crowned crane (with a wild magpie in the background that I hadn't noticed until after I took the picture).

Nearby are these wattled cranes, the largest cranes in Africa.

Some African wild dogs.

Rock hyraxes (with babies)!

Despite the gaffe with coatis shown earlier, I liked how informative many of Chester's exhibit signs were. I especially appreciated this sign at the hyrax exhibit.

Naturally, there is a walkthrough aviary in this part of the zoo as well. Here, a village weaver works on its nest.

A snowy-crowned robin chat, a skilled vocal mimic of other birds.

A hamerkop, a wading bird known for building massive nests that can be more than one meter across. Some of these nests were evident in the exhibit.

Africa is home to several spectacular starlings, including this aptly-named superb starling.

A blacksmith lapwing.

Some crested guineafowl (as opposed to the more commonly kept helmeted guineafowl).

Although the African aviary isn't especially large or densely-planted, many birds remained surprisingly well hidden. Fortunately, some keepers passed through while I was there and scattered some mealworms on the ground, which drew out a few of the shier birds. One of the birds that emerged to check out the commotion was this red-winged starling.

This lilac-breasted roller also showed up, to my delight.

Saturday, June 22, 2019

What's the Deal with Enantiornithean Tails?

You are drawing a scene set in the Cretaceous and you need some birds in the picture, maybe as a way to show off the size of some much larger, more charismatic dinosaur. The setting is not oceanic enough to use something vaguely Ichthyornis-like, so what do you do? You draw in a few enantiornitheans, of course.

That's a good choice. Enantiornitheans, or "opposite birds", were probably the most diverse and abundant bird-like dinosaurs during the Cretaceous. They would have looked quite similar to modern birds and were probably doing many of the same things that modern birds do. However, recent findings have also given us insights into how enantiornitheans differed from modern birds, not only in the details of their skeletons but also in their external appearance and behavior. This means that scientifically rigorous depictions of enantiornitheans should not show them simply as modern birds transplanted into a different time period. And probably the most noticeable difference between most enantiornitheans and modern birds would have been the feathering on their tail.

(You might have noticed that I've switched to using "enantiornitheans" instead of the more commonly used "enantiornithines". As has been noted by Harris et al., 2006 and Matt Martyniuk, the suffix "-ine" is more typically used for the vernacular names of clades that end in "-inae", and Enantiornithes is not one of those clades. Seeing as Harris et al. suggested using "enantiornitheans", that's what I'm going with for now.)

Restoration of the enantiornithean Dapingfangornis, by Jack Wood (used with permission).

Unlike most other dinosaurs, the bony part of a modern bird's tail is very short, even in birds that have long tail feathers. Despite this, the tail serves important functions in most birds. The last few tail vertebrae are fused together into a structure called the pygostyle, which supports a pair of muscular bulbs in which the flight feathers on the tail are embedded. These bulbs are known as rectricial bulbs, and they are responsible for the ability to spread the tail feathers out like a fan. This allows the tail feathers to act as an additional lift-generating surface, which among other things grants finer control during low-speed flight, such as while landing.

A white-necked jacobin showing off its spread tail fan, photographed by Paul Tavares, under CC BY-NC 4.0.

Like modern birds, enantiornitheans had short tails with a pygostyle. As a result, they have traditionally been depicted with tail fans similar to those of modern birds. In fact, several early papers about enantiornitheans outright suggested that they likely had tail fans based on their possession of a pygostyle. However, by the mid-2000s, a good number of enantiornithean fossils had been described from the Jehol Group in China, famous for its preservation of soft tissue structures, including feathers.

How many of these enantiornitheans have been found with tail fans? None.

Julia Clarke and colleagues pointed this out in a 2006 paper describing the anatomy of Yixianornis, an Early Cretaceous avialan from the Jehol that was more closely related to modern birds than enantiornitheans were. Whereas the holotype of Yixianornis was preserved with a tail fan similar to those of modern birds, all enantiornitheans preserved with tail feathering that had been described up to that point either lacked large tail feathers entirely (leaving only a fuzzy stump of a tail) or had just a single pair of long tail feathers that wouldn't have provided much of a lift-generating surface.

Clarke et al. also highlighted the fact that (as had been noted by previous researchers) the pygostyle of enantiornitheans differed from those of Yixianornis and modern birds. Enantiornitheans had a longer, more rod-like pygostyle, whereas Yixianornis and modern birds have a shorter, more tab-like one. Thus, Clarke et al. suggested that the presence of a pygostyle alone does not indicate tail feathering similar to that of modern birds. Instead, it is specifically the short, tab-like pygostyle that correlates with a tail fan.

Comparison of the last few tail vertebrae among different maniraptor groups, mapped onto their phylogenetic relationships, from Wang and O'Connor (2017). In most long-tailed maniraptors (e.g.: Archaeopteryx, dromaeosaurids), the vertebrae are not fused into a pygostyle, but some oviraptorosaurs and therizinosaurs have evolved fused tail vertebrae independently of short-tailed avialans. Note that members of Ornithuromorpha (a group that includes modern birds) have a short, tab-shaped pygostyle.

If we had only a few fossils to base these conclusions on, these observations might not mean much. Even the Jehol Group rarely preserves a complete record of plumage in any individual specimen. However, dozens if not hundreds of feather-preserving Mesozoic avialan fossils have now been studied, and for most part, the pattern observed by Clarke et al. has held up under subsequent discoveries. So far, all Mesozoic avialans confirmed to have had a modern-style tail fan are species more closely related to modern birds than enantiornitheans were, with short, stumpy pygostyles.

Among enantiornitheans, on the other hand, the most commonly seen condition is the absence of any large tail feathers, which has been documented in Eoenantiornis, Longipteryx, Cruralispennia, and Avimaia. Enantiornithean genera that have been found with a single pair of long tail feathers include Protopteryx, Dapingfangornis, Bohaiornis, Parapengornis, Eopengornis, Cratoavis, Junornis, and Orienantius. Longirostravis was described as preserving these long tail feathers as well, though Mesozoic avialan specialist Jingmai O'Connor is reportedly doubtful of this interpretation. There are even very small juvenile enantiornithean specimens that apparently show a pair of tail feathers that had begun to grow, as seen in one of the amber-preserved enantiornitheans. (Yeah, we have amber-preserved enantiornitheans.)

Two enantiornithean specimens preserved with feathers, from O'Connor et al. (2012). Protopteryx (A) preserves a single pair of streamer-like tail feathers, whereas Eoenantiornis (B) preserves no large tail feathers at all. (C) shows isolated body feathers of Protopteryx, which are not especially relevant to this post.

These forms of tail plumage are similar to that of confuciusornithiforms, which were more distant relatives of modern birds compared to enantiornitheans. It's perhaps no accident that, like enantiornitheans, confuciusornithiforms had rod-shaped pygostyles. Currently, we don't have enough specimens described of any enantiornithean to determine whether long tail feathers were only present in some individuals of the same species, as has been documented in Confuciusornis and Eoconfuciusornis. At least in the case of confuciusornithiforms, it appears likely that the individuals with the long tail feathers were males.

The long tail feathers in enantiornitheans and confuciusornithiforms have been described as being ribbon-like or streamer-like. They are known by the technical names Rachis-Dominated Feathers (RDFs) or Proximally Ribbon-like Pennaceous Feathers (PRPFs). Recent findings of such feathers preserved in amber have been very informative regarding their detailed structure, which had been difficult to interpret from flattened Jehol-style fossils. It turns out that the central shaft of RDFs is an extremely thin sheet that is less than 50 micrometers thick. The underside of the shaft is open such that it forms an arch, unlike the enclosed tube seen in typical feathers.

Examples of RDFs preserved in amber, from Xing et al. (2018). (D) is a schematic showing the structure of RDFs, as inferred from these specimens.

Several groups of modern birds, from hummingbirds to parrots, have evolved superficially similar, streamer-like feathers, but none of these plumes exhibits the same type of structure seen in RDFs. It appears that RDFs are an entirely extinct form of feather that modern birds have "forgotten" how to make. Like most other types of feathers, RDFs have barbs coming off the central shaft. In some enantiornitheans, such as Eopengornis and Parapengornis, the barbs are present along almost the entire length of the tail feather, but in many others the barbs are restricted towards the feather tip.

So enantiornitheans either lacked flight feathers on the tail or had a single pair of ribbon-like feathers not found in any modern bird. Simple, right? Yet, as happens so often in science, some new discoveries have arisen that complicate the picture. For starters, we now also know of enantiornitheans that had two pairs of RDFs on the tail, as first discovered in Paraprotopteryx.

Furthermore, a few enantiornitheans described since 2006 have been purported to challenge the notion that enantiornitheans lacked tail fans. The first of these was Shanweiniao, described in 2009 by O'Connor and colleagues. Shanweiniao was found with at least four (possibly six) tail feathers closely aligned with one another, as though forming a tail fan. It was even named for this feature, Shanweiniao meaning "fan-tailed bird" in Chinese.

However, these feathers were not very well preserved, so their structure and arrangement are difficult to confirm. In a 2016 paper describing another enantiornithean, Chiappeavis (which will factor into this story shortly), O'Connor et al. reevaluated the evidence for a tail fan in Shanweiniao. They noted that there were narrow gaps between its tail feathers, unlike what was preserved in avialans with more definite tail fans. Therefore, they concluded, it was more likely that the tail feathering of Shanweiniao consisted of at least two pairs of RDFs, similar to Paraprotopteryx. Shanweiniao may have had more tail feathers than the average enantiornithean, but there is little reason to think that it had a modern-style tail fan.

The tail feathers of Shanweiniao, from O'Connor et al. (2009).

The next new find that seemed to question the dearth of enantiornithean tail fans was Feitianius, described in 2016. Feitianius was found with not just two or even four large tail feathers, but many. It had a single pair of RDFs, but it was also preserved with 5-7 shorter feathers that appear to have been barbed for only about half their length, as well as at least 5 more tail feathers that were shorter still. In addition, an organic mass preserved around the pygostyle was interpreted as the remnants of the soft tissues that include rectricial bulbs.

In 2017, Wang Wei and O'Connor put forth a more detailed study on the relationship between pygostyle form, tail musculature, and tail feathers. They found that it was unlikely for any enantiornithean pygostyle to have supported well-developed rectricial bulbs. However, they did find features of the pygostyle in enantiornitheans (and confuciusornithiforms) that correlate with strong muscles for raising the tail, and suggested that the soft tissues surrounding the pygostyle in Feitianius may instead include these muscles instead of rectricial bulbs. Thus, Feitianius was likely well adapted to raising its elaborate set of tail feathers (perhaps in display), but not for spreading them apart as a true tail fan.

The tail of Feitianius with preserved soft tissues, from O'Connor et al. (2016a).

Only a day after the paper naming Feitianius was posted online, along came the aforementioned description of Chiappeavis. The preserved tail feathers of Chiappeavis really do resemble a tail fan. There are no visible gaps between the feathers as in Shanweiniao, and though their detailed structure is poorly preserved, they appear to have been standard flight feathers instead of RDFs.

When O'Connor et al. presented a more detailed study* on the anatomy of Chiappeavis in 2017, they also estimated the aerodynamic qualities of its supposed tail fan. They found that its lift-generating capabilities were very limited compared to those of tail fans in modern birds and their close relatives. Wang and O'Connor (2017), which was published a few months later, also found no features that made Chiappeavis any more likely to have had rectricial bulbs than other enantiornitheans. So even though the tail feathers of Chiappeavis were arranged in a similar manner to a tail fan, they probably didn't function like the spreading tail fan of modern birds.

*Interestingly, O'Connor et al. did not exclude the possibility that enantiornitheans had rectricial bulbs in this study, claiming that some modern birds also lack the pygostyle features that typically support rectricial bulbs. They cite the Wang and O'Connor study (in-prep at the time) for this, but the final version of Wang and O'Connor (2017) does not repeat the claim, instead concluding that rectricial bulbs were most likely absent in enantiornitheans.

The tail of Chiappeavis with preserved feathers, from O'Connor et al. (2016b).

In the end, Feitianius and Chiappeavis demonstrate that enantiornithean tail feather arrangements came in more varieties than the two that Clarke et al. (2006) originally identified. Given the great diversity of enantiornitheans, it's not unlikely that more will be found in the future. However, after so much back and forth, it appears that Clarke et al.'s central contention that a true tail fan is found only in avialans more closely related to modern birds remains valid.

So if enantiornitheans weren't using their tail feathers like modern birds do, what were their tail feathers for? In many cases, the most obvious possibility is some form of visual signalling. That would certainly be consistent with the evidence for well-developed tail-raising muscles, as previously noted with respect to Feitianius. In addition, modern birds that have superficially similar, streamer-like feathers tend to use them in display.

That being said, a few other possibilities have been put forth. The abundance of isolated RDFs found in amber has been suggested as evidence that these feathers detached easily, which may have allowed them to misdirect attacks from predators (much like the detachable tails of many lizards). A variety of modern birds certainly have tail and rump feathers that shed readily if grabbed by a predator. However, as with the feathers of these modern birds, I suspect that distracting predators was not the primary function of RDFs.

The RDFs of Parapengornis in particular have been proposed to have functioned as props, similar to the tail feathers of some modern climbing birds such as woodpeckers. This idea was purportedly backed up by pygostyle anatomy, but Wang and O'Connor (2017) later determined that the pygostyle of Parapengornis wasn't especially similar to that of woodpeckers after all.

Restoration of Feitianius showing it using its tail feathers for display, by Scott Reid (used with permission).

How would the absence of a lift-generating tail fan impact the flight of enantiornitheans? That a tail fan is not a requirement for avian flight is evident from observations of modern birds. Individual birds that have lost their tail feathers can usually still adapt to flying without them. There are even flying birds today that naturally lack tail fans, namely grebes (though their large, lobed feet perform some of the functions that a tail fan normally would).

Even so, I wonder if enantiornitheans were generally clumsier fliers compared to similarly-sized modern birds, or perhaps needed to expend more energy to perform equivalent aerial maneuvers. Martyniuk has speculated that enantiornitheans may have preferred to land on large surfaces such as tree trunks before climbing to desired perches, instead of trying to precisely target small twigs and branches from the get-go. Given that many enantiornitheans appear to have been small, forest-dwelling animals, they might not have needed much endurance or agility if most of their flight involved flitting from tree to tree in this manner. Some recent research has focused on inferring the likely flight behavior of Mesozoic avialans from their wing shape and body mass. It would be interesting for future studies to compare the effects of different types of tail feathering on flight ability.

Restoration of the enantiornithean Alethoalaornis in flight, by Scott Reid (used with permission).

One final subject I'll remark on here is the evolutionary history of enantiornithean tail feathers. The structure of RDFs suggests that they evolved from more typical shafted feathers. Most early avialans and other long-tailed maniraptors (including troodonts, dromaeosaurids, and oviraptorosaurs) certainly had large shafted feathers along the length of their tail. Such an array of tail feathers has often been called a "tail fan", but there is no evidence that long-tailed maniraptors had structures similar to rectricial bulbs that could fan out their tail feathers. As a result, I prefer to use Stephen Gatesy's term "tail frond" to distinguish this type of tail from the mobile tail fan of modern birds.

On the lineage leading to enantiornitheans (as well as modern birds), the bony part of the tail shortened. What would an immobile tail frond look like when retained on a shortened tail? Well, probably something similar to the immobile fan of Chiappeavis. (That this represents the ancestral state for short-tailed avialans is potentially supported by the fact that a similar fan is also known in Sapeornis, which was more distantly related to modern birds than enantiornitheans were.) A plausible evolutionary scenario may be that most enantiornithean lineages then lost the majority of their tail feathers, modifying the remainder into RDFs. In 2014, Wang Xiaoli and colleagues further suggested that the fully barbed RDFs seen in Eopengornis might represent a precursor to RDFs that had a mostly naked shaft.

Comparison of tail plumage in different Mesozoic avialans, from Wang et al. (2014). (A) shows the "tail fan" of Sapeornis, (B) shows the RDFs of Dapingfangornis (which only have barbs near their tip), (C) shows the true tail fan of Hongshanornis, and (E) shows the fully barbed RDFs of Eopengornis. ("D" featured the forked tail of Schizooura, which I cropped out as it is not directly relevant to this post.)

However, there's a wrinkle to this tale. Phylogenetic analyses that include Chiappeavis find it to be more closely related to Eopengornis and Parapengornis (which had fully barbed RDFs) than to other enantiornitheans. If these relationships are correct, they may imply that the RDFs of Eopengornis and Parapengornis evolved independently from those of other enantiornitheans, instead of representing an ancestral state for RDFs. An alternative possibility is that Chiappeavis evolved its "tail fan" from an ancestor that had RDFs and is uninformative about the ancestral state of tail plumage in enantiornitheans. Or perhaps our current understanding of enantiornithean phylogeny is wrong. Given that enantiornitheans have some of the most poorly resolved interrelationships among all Mesozoic dinosaurs, that wouldn't surprise me. At present, I don't think we have enough information to rule out any of these possibilities.

Long story short, enantiornithean tail plumage came in a wide variety of forms, all of which were different from that of most modern birds. We still have some ways to go when it comes to understanding their function and evolution, and it's likely that they will continue to surprise us in years to come.