Flightlessness Is Harder Than You Think

Leptoptilos robustus reconstruction. Storks may fly better than fowl, but they did beat them at actually being flightless.

Flight is undoubtedly costly. It certainly modified the anatomy of birds to a large extent in terms of “weight saving”, and certainly is proven to be rather energetically demanding. That many birds discard flight whenever they are given the proper ecological opportunity to do so, such as being in a predator-less environment or finding themselves in a niche that does not require flight, is basic zoological common sense.

Yet, in spite of these groups of birds commonly cited as “poor flyers”, like fowl, woodpeckers and tinamous, do not have flightless members. Likewise, there are also no flightless members of other flying vertebrate clades, like pterosaurs, bats and volaticotheres, in spite of several also being rather terrestrial and found in insular environments where flightless birds prosper. Flight might even have been preserved among the juveniles of some large dromaeosaurs, as Deinonychus and Velociraptor demonstrate.

What gives, then?

Don’t Fix What Ain’t Broke

Vulcanops jennyworthyae by Gavin Mouldey. Mystacine bats became terrestrial in mainland Australia and exploded in diversity in New Zealand, but unlike contemporary ratites they retained flight.

Sometimes, giving up something even as it gets cumbersome ain’t worth it. For example, although the process of losing wings seems straightforward enough, you might A) not adjust to complete flightlessness fast enough and get stuck in a non-functional half-state, B) getting rid of the wings means simplifying other body parts that you might not want to remove.

Bats, pterosaurs and volaticotheres all are quadrupedal launchers with complex wing membranes. To birds, losing flight-appropriate wing feathers is a rather fast process that could hypothetically take less than a generation, but for these animals it would mean losing an extremely nuanced system of skin, fibers, muscles and digit bones. Losing an entire limb is not unheard off, as whales and snakes demonstrate, but no tetrapod animal has ever lost such a complex organ, and furthermore at least the wing finger play a role in terrestrial locomotion in pterosaurs (Witton 2013); combined with the well-developed state that terrestriality by itself implies, wing reduction in any capacity in these groups is therefore unthinkable.

True enough, even in situations where flightlessness would be expected these animals retained flight. The iconic mystacine bats of New Zealand, for example, have living in the landmass for over 17 million years and even co-existed with ancestors of modern flightless birds such as the proto-kiwi Proapteryx, but they have not lost the ability to fly in any capacity at all, to the point that modern Mystacina bats are as agile in the air as non-terrestrial bats (Arkins 1999). Meanwhile, the diverse pterosaur fauna of Hateg Island does not wield a single flightless species in spite of the fact that azhdarchids like Hatzegopteryx were its top predators. A specimen called “Dracula” might be flightless as a fully-grown adult, but anatomically it does not differ from flying pterosaurs, making it unlikely.

However, even in birds flightlessness may be something out of range for many groups. Crown-group Galliformes, for instance, do not have true flightless members in the wild; domestic chickens are often flightless, but due to artificial breeding allowing traits that could be fatal in the wild like non-asymmetrical feathers (or even no feather at all) or shorter wings, while adult snowcocks cannot launch from the ground, but are still capable of aerial locomotion if they can launch from a high place (Madge 2002). Same applies for other groups of traditional “poor flyers” like woodpeckers and tinamous.

In at least Galliformes, this might be connected to the development of flight muscles. In fowl, flight musculature develops very early on in comparison to other bird groups such as the closely related waterfowl, so much so that in taxa like megapodes the juveniles can even fly immediately after birth. Even the relatively non-extreme domestic chicken develops its flight muscles prior to birth (Biewener 2011), so unlike other birds getting rid of this equipment may be slightly harder. Whereas a duck can simply not develop complex flight musculature as it grows up, a chicken is born with it and would have to degenerate them at a latter stage of development.

Getting stuck with flight when it isn’t the most ideal situation can have some interesting results. Mystacine bats, for example, expanded ecologically in the rarity of other terrestrial mammals in New Zealand aside from the Saint Bathans mammal (Hand 2018), but are still small in size compared to the megafaunal birds in their environment, likely because they were constrained by size limits imposed by their flight capacities. Likewise New Zealand quails didn’t differ much from Australian ones, in contrast to indigenous flightless birds displaying a greater disparity from their mainland counterparts. Tinamous in South America are probably in the worst position, given that they are essentially inept at flying due to their small hearts (Altimiras 2017)… and also at running for that reason, so flight it is.

It Ain’t All That Bad

Turkeys launching. While typically thought off as “poor flyers”, fowl are actually highly specialised at a specific flight style, and retain strength at even large sizes.

Another caveat is that “poor flying” birds may not necessarily be so. Fowl, tinamous and woodpeckers are actually highly specialised to a specific type of flight, called “burst flight”, characterised by rapid launching and extensive, continuously flapping (Kaiser 2008). They have highly developed flight musculature and robust wing bones, allowing them to generate ridiculous amount of power to get off the ground as fast as possible. Ther wings are short and not not allow them to glide or soar, but do facilitate them to ascend quickly much like helicopters. The combination of short wings and sheer energy expended in launching means that they are rarely long distance flyers — a few species are actually migratory nonetheless (Kaiser 2008) — but they are capable of launching even at relatively large sizes, such as turkeys and peafowl.

In short, they might not win any marathons, but a speedy escape is all they need, and so flight is still immensely valuable to these birds. Burst flying also evolved in at least one pterosaur lineage, the dimorphodontids, which are more derived than “better flying” basal pterosaurs, further indicating the specialised status of this flight style (Witton 2013).

Specific lifestyles may also make flightlessness something more reluctantly lost. In raptors, for example, flight is often necessary for hunting and piercing prey from above, hence why there are no flightless eagles or hawks; insular owls and caracas did get around this by switching to mostly cursorial hunting, however. In pterosaurs, bats and volaticotheres, flight might be expensive, but quadrupedal launching makes the process of taking off less costly than in birds, probably further discouring full flightlessness.

Speculations

Lithornis vulturinus by Dylan Bajda. Unlike modern tinamous, lithornithids aside from Paracathartes were not burst flyers, which may suggest that tinamous are ironically less susceptible to becoming flightless than their better flying ancient cousins, which went on to spawn the decidedly flightless ratites.

Flightlessness in birds seems to develop mostly in groups that have terrestrial habits but also good flight capacities, allowing them to not only reach ideal ecosystems where flight is unnecessary but also the lack of developmental urgency at least fowl have, thus being able to simply not develop strong wing muscles when the time comes.

The groups that spawned the highest number of flightless species are waterfowl, Gruiformes and Cariamiformes:

  • In the former, excellent flight capacities are the norm: ducks and geese are specialised endurance flyers that can perform impressive migrations without ever needing to rest, while more basal screamers and magpie geese are soarers. Although the young are fairly precocial, in virtually all waterfowl the flight muscles develop relatively late, around moulting (Biewener 2011), so they can just not develop them. Waterfowl are also capable of occupying a vast variety of both terrestrial and aquatic niches, further augmenting the contexts in which flightlessness can evolve. Thus we have insular herbivores like moa-nalos, giant mainland herbivores like dromornithids, aquatic wing-powered divers like Bambolinetta, foot-propelled divers like the New Zealand merganser among others and even weird blind fossorial foragers like Talpanas. Like in snowcocks some individuals from flying species are flightless at large sizes, like mute swans and flying steamer ducks.
  • Flightless Gruiformes are present in both the crane and rail lines. While rails are not particularly agile aeronauts and some are in fact burst flyers, they are nonetheless usually highly endurant and can stay aloft for several miles. Unlike fowl they have extended parental care, hence most do not develop flight musculature until near adulthood (Biewener 2011). In crane-like forms flight capacities are usually much better, with cranes proper even being soarers and having proportionally large wings; this nonetheless did not prevent multiple instances of flightlessness, with ratite-like cranes such as geranoidids and eogruids flourishing in the northern continents and the Cuban crane being the tallest herbivore in the Caribbean.
  • Modern seriemas are poor flyers, though whereas they can be classed as burst flyers or not is debatable. Many extinct forms were good flyers, however (Mayr 2008, Mayr 2013), and likewise there is a high variety of extinct flightless species such as Strigogyps, bathornithids and phorusrhacids. Cariamiformes, like most other Australaves, have extensive parental care, further delaying the development of flight muscles.

Passerines such as New Zealand wrens and long-legged buntings, storks such as Leptoptilos robustus, Coraciiformes like the Saint Helena hoopoe, pigeons such as dodos and solitaires, parrots such as kakapos and several other taxa represent flightless members of groups that are typically considered effective flyers. Seabirds, which are generally some of the most aerial flying vertebrates, produced several waves of flightless divers such as penguins, plotopterids and Hesperornithes. Meanwhile, flight persists among basal maniraptors in at least juveniles, where megapode-like superprecociality is common (Fernández 2013, Parsons 2015, Mayr 2018).

By far the most interesting group to discuss in this regard are palaeognaths, the group that includes the most iconic flightless birds of all, ratites. While modern tinamous are burst flyers, as was the lithornithid Paracathartes (even compared functionally to turkeys[!]), most extinct flying palaeognaths were competent aeronauts, some lithornithids even comparable to soaring birds like storks and vultures (Houde 1988). In recent years the idea that palaeognaths dispersed by air across the continents instead of being gondwanan vicariants has been extensively supported by both genetic data and the survival of flying species until relatively recently like the proto-kiwi Proapteryx, suggesting that the ancestors of ratites were indeed good flyers.

Thus, the absurdly poor flight capacities of tinamous are not only an unique invention by the group, but also probably what prevented them from becoming flightless like their ratite cousins. Palaeognaths have developed flightlessness multiple times in mammal dominated environments, which combined with the sheer unnecessary expenses of tinamou flight makes their continued adherence to it all the more surreal. Rather than being functional relics, tinamous have probably remained volant because they can’t become flightless. Given that there are no ratites in North America, Paracathartes and its relatives must similarly have hit a proverbial boulder with their burst flying, allowing geranoidid cranes to become the local ratite-analogues.

The same also applies to fowl. Although modern fowl are burst flyers, some stem-fowl apparently had different flight styles (Mourer-Chaviré 2015), which might explain the otherwise odd anomalies that are sylviornithids, a bunch of flightless stem-fowl indigenous to Melanesian islands.

Conclusion

Dimorphodon macronyx by Mark Witton, a pterosaur burst flyer.

As always, “conventional wisdoms” must always be questioned in biology. In the post-All Yesterdays world we live in, we have undergone a renaissance in terms of understanding both extinct and living animals, and what might seem obvious at first may fall under harsh scrutiny at a closer glance.

Flight is no doubt a double-edged sword, but to what extent is clearly much murkier than previously thought.

References

Mark P. Witton (2013), Pterosaurs: Natural History, Evolution, Anatomy, Princeton University Press, ISBN 978–0–691–15061–1

Arkins, A. M., Winnington, A. P., Anderson, S. & Clout, M. N. 1999. Diet and nectarivorous foraging behaviour of the short-tailed bat (Mystacina tuberculata). Journal of Zoology 247, 183–187.

Madge, Steve; McGowan, J. K.; Kirwan, Guy M. (2002). Pheasants, Partridges and Grouse: A Guide to the Pheasants, Partridges, Quails, Grouse, Guineafowl, Buttonquails and Sandgrouse of the World. A. C. Black. pp. 174–180. ISBN 9780713639667.

Biewener, Andrew A., Muscle function in avian flight: achieving power and control, 2011 May 27; 366(1570): 1496–1506.

Hand, S. J.; Beck, R. M.; Archer, M.; Simmons, N. B.; Gunnell, G. F.; Scofield, R. P.; Tennyson, A. J. D.; De Pietri, V. L.; Salisbury, S. W.; Worthy, T. H. (2018). “A new, large-bodied omnivorous bat (Noctilionoidea: Mystacinidae) reveals lost morphological and ecological diversity since the Miocene in New Zealand”. Scientific Reports. 8 (1): 235. doi:10.1038/s41598–017–18403-w.

Jordi Altimiras, Isa Lindgren, Lina María Giraldo-Deck, Alberto Matthei & Álvaro Garitano-Zavala, Aerobic performance in tinamous is limited by their small heart. A novel hypothesis in the evolution of avian flight, Scientific Reports volume 7, Article number: 15964 (2017)

Kaiser, Gary W. , The Inner Bird: Anatomy and Evolution Paperback — 1 Feb 2008

Gerald Mayr & Cécile Mourer-Chauviré, The peculiar scapula of the late Eocene Elaphrocnemus phasianus Milne-Edwards, 1892 (Aves, Cariamae), December 2008, Volume 88, Issue 2, pp 195–198

Mayr, G.; Yang, J.; De Bast, E.; Li, C.-S.; Smith, T. (2013–06–25). “A Strigogyps-like bird from the middle Paleocene of China with an unusual grasping foot”. Journal of Vertebrate Paleontology. 33 (4): 895–901. doi:10.1080/02724634.2013.748059.

Fernández, Mariela S.; García, Rodolfo A.; Fiorelli, Lucas; Scolaro, Alejandro; Salvador, Rodrigo B.; Cotaro, Carlos N.; Kaiser, Gary W.; Dyke, Gareth J. (2013). “A Large Accumulation of Avian Eggs from the Late Cretaceous of Patagonia (Argentina) Reveals a Novel Nesting Strategy in Mesozoic Birds”. PLoS ONE. 8 (4): e61030. doi:10.1371/journal.pone.0061030. PMC 3629076 Freely accessible. PMID 23613776.

Parsons, William L.; Parsons, Kristen M. (2015). “Morphological Variations within the Ontogeny of Deinonychus antirrhopus (Theropoda, Dromaeosauridae)”. PLoS ONE. 10 (4): e0121476. Bibcode:2015PLoSO..1021476P. doi:10.1371/journal.pone.0121476. PMC 4398413 Freely accessible. PMID 25875499. e0121476.

D. C. Deeming; G. Mayr (2018). “Pelvis morphology suggests that early Mesozoic birds were too heavy to contact incubate their eggs”. Journal of Evolutionary Biology. in press. doi:10.1111/jeb.13256.

Houde, Peter W. (1988). “Paleognathous Birds from the Early Tertiary of the Northern Hemisphere”. Publications of the Nuttall Ornithological Club (Cambridge, MA) 22.

Mourer-Chauviré, C., M. Pickford. 2015. Stemp group galliform and stemp group psittaciform birds (Aves, Galliformes, Paraortygidae, and Psittaciformes, family incertae sedis) from the Middle Eocene of Namibia. Journal of Ornithology 156 (1): 275–286.