Aepyornithidae: The Largest Maniraptors Of Madagascar

Aepyornis by Ville Sinkkonen. This picture is the one that best illustrates the absurdly large (by palaeognath standards) skull of these ratites.

Elephant birds, or, as they are known in Malagasy, Vorompatra (“marsh bird”) are iconic giant ratites from the island subcontinent of Madagascar. While they are very commonly present in prehistory books, very little is actually presented of these birds; their eggs, the largest among birds and in fact the largest dinosaur eggs ever found until the discovery of even larger eggs in China, attributed to sauropods and oviraptorids, are usually the focus when they are mentioned, and if you’re lucky they might also reference how they were heavier than their taller New Zealand relatives, the moas.

In truth, while admittedly hardly charismatic even to some ornithologists, are rather interesting because they heavily hint at how Madagascar’s fauna evolved during the Cenozoic, and further illustrate the way palaeognath diversity was established.

Overview

Aepyornis skull. Much like in cassowaries and moas, aepyornithids fused the nares, anteorbital frenestrae and eye sockets in a single opening, although in a more extreme way, almost resembling azhdarchoid pterosaurs in a way. This was likely to facilitate air passage, allowing the animal to cool the head in the tropical climate of Madagascar.

All aepyornithids are known from the Pleistocene/Holocene, a given due to the nigh-absence of earlier Cenozoic Malagasy fossils (the exception being a few sea cow fossils from the Eocene, Miocene and Pliocene). They are represented by two genera: the famous Aepyornis and the extremely obscure Mullerornis. The number of species is not certain; four species of Aepyornis and three of Mullerornis are recognized, but it has been suggested that many so called “species” might represent animals at different growth stages. For the sake of convenience, I will focus more on the genera as a whole and not on the supposed individual species.

As to be expected from flightless birds, aepyornithids suffered several anatomical modifications. The notarium was lost, as was most of the forelimbs with the exception of the minuscule humerus, which was probably located internally, rendering the bird completely wingless. As to be expected from a ratite, the sternum was small and flat, no longer exhibiting a recognizable keel. The skeleton in general is very robust; although many bones remained pneumatic as means to control body temperature as in other dinosaurs, being free from the pressures of powered flight meant that marrow production could become more extensive, and as such the hind limbs and pelvis were nothing short of massive. In life, the largest Aepyornis weighted over 400 kg, and were considered the biggest Neornithes of all time (the largest moas and terror birds were taller, but much less heavy), until later research gave that title to australian dromornithids, which managed to be both heavier and taller.

The skulls of Aepyornis were unusually large for ratite standards; while not proportionally the largest skulls among birds, in sheer size they were among the biggest, apparently only surpassed by the terror bird Kelenken. Palaeognaths, due to their lack of an ossified palate, are generally noted for having small skulls in comparison to other birds; even long billed forms like kiwis have very shallow beaks. This seems to be refuted by the very deep rostrums of aepyornithids, which superficially vaguely resembled those of azhdarchoid pterosaurs, particularly chaoyangopterids. The size of the skull was presumably an adaptation for the hot climate of Madagascar; the nares, anteorbital frenestrae and the eye sockets were fused into one large cavity, allowing the passage of air in other to keep the head cool.

Despite the large beaks, the animals probably had a weak bite force, due to the lack of a bony palate, although, given the strong gastric acids of most birds, this probably did not impair the animal much. Aepyornithids are thought to have been high browsers, occupying on Madagascar the same ecological niche that giraffids occupy on mainland Africa. Many Malagasy rainforest tree species have fruits with thick, highly sculptured endocarps, often dark blue or purple in color, much like those consumed by modern cassowaries, so aepyornithids might have played important roles as frugivores, dispersing the seeds of the species they fed on. In the presence of the also browsing giant lemurs, aepyornithids might have had a more flexible diet, feeding on small animals in addition to leaves like modern cassowaries and rheas, but this is not certain. While they were almost certainly present in rainforests, most aepyornithid remains were found in Madagascar’s wetlands; it’s not certain if this was a preferred environment or if was just where the fossils were best preserved.

Not much is known about aepyornithid social behavior; probably it was fairly loose, likely tending towards being solitary but without the aggressive territory creation that cassowaries and kiwis engage on. The male was almost certainly the one responsible for incubating the eggs and raising the young like in most modern ratites; it’s not clear if they formed harems like most modern ratites or if they only raised one or two eggs laid by a single female. The chicks were certainly precocial; the presence of more predators perhaps indicates that were guarded by their parents like in most modern ratites, unlike modern kiwis and maybe the extinct moas, which are essentially superprecocial. Regardless, the period of parental protection was likely short, as aepyornithid growth rates are slow like those of moas and kiwis, with the birds reaching sexual maturity after several years.

Grandma, What Big Eggs And Bones You Have!

Aepyornis eggs. The biggest among neornithes, their size probably is an evolutionary response to predation.

Aepyornithids are generally dismissed as the product of an environment without macropredators, much like practically every flightless bird in existence.

However, this view is erroneous; while many birds lost flight in the absence of predators, we now know that flight is more expendable than that, and in fact many flightless avifaunas evolved in environments ruled by many predators, such as the Cretaceous hesperornithes and patagopterygids. Even ostriches and rheas likely evolved in the company of predators; while their ancestry goes back to a time where predatory mammals were rare, sebecian and pristichampsid crocodillians ruled the ancient forests of the Eocene and were soon joined by avian bathornithids and mammalian “creodonts”, and forms like Palaeotis and Diogenornis were already cursorial.

Did aepyornithids evolve in a world without predators? A look at Malagasy Holocene fauna indicates the presence of three macropredators; the giant osteolamine crocodile Voay robustus and the giant fossa Cryptoprocta spelea likely posed a threat to the juveniles, probably even the adults of Mullerornis in Voay’s case. However, all aepyornithids probably feared the remaining Malagasy macropredator, Stephanoaetus mahery, the Malagasy Crowned Eagle, also known as Mahery. The similar Harpagornis moorei from New Zealand was a moa specialist, capable of dealing with even the larger species, so it is likely that the Mahery, with the ability to fly and thus strike at the vulnerable neck and head, was a threat to even the largest Aepyornis.

For obvious reasons, its not clear if aepyornithids have been under the influence of similar predators across the Cenozoic, and if they evolved flightlessness in a time when Madagascar had no predators. However, it seems clear that modern aepyornithids do have some adaptations that can be interpreted as defenses against the contemporary predators; the sheer robust built of these birds in comparison to other ratites, specially to the also insular moas, seems to suggest that these creatures became so massive in order to defend themselves. The only other birds that are equally as robust are gastornithids and dromornithids, which also evolved in environments with terrestrial predators. In fact, these three groups evolved in the company of large crocodillians, with pristichampsids co-existing with gastornithids, mekosuchines with dromornithids and Voay with the aepyornithids, so this might suggest that the robust built of these birds might be related to fending off crocodillians specialized in killing terrestrial prey.

While Voay might not had been the predator that influenced aepyornithid evolution, similar crocodiles might had been present earlier, when the birds evolved.

Similarly, the eggs of aepyornithids are unusually large. While ratites in general lay very large eggs, the only ones with such proportionally large eggs are kiwis, which are superprecocial. While recent genetic studies might suggest that this is simply a trait acquired between the last common ancestor between kiwis and elephant birds (see below), It is also possible that aepyornithid eggs simply became that large in other to decrease predation on the young; no known Malagasy carnivore can break the shell, and the young would have been born big enough to be only threatened by the larger carnivores. This too seems indicative that aepyornithids evolved to cope with the native predators.

Like moas, aepyornithids are clearly not specialized runners. However, the metatarsals (like in all neornithes, they are fused) appear to be proportionally slightly longer than in moas, and the hallux is absent. This seems to suggest that aepyornithids were more efficient runners than moas, presumably relying on speed to escape, although fully grown Aepyornis probably didn’t not had to run.

The Origins Of The Vorompatra

Ratite dispersal diagram by Daniel Foidl. Made way back in 2007, it more or less predicts ratite dispersal rates as dictated by posterior genetic samples.

Historically, the closest relatives of the elephant birds have been considered to be the ostriches, a rather logical conclusion given that ostriches live in Africa and aepyornithids live in Madagascar; since both landmasses were part of the supercontinent Gondwanna, both bird clades would had evolved from an ancestor that became isolated in Africa and Madagascar.

In reality, things are not as simple. Ratite diversity took place in the earliest Cenozoic, long after Gondwanna was largely split apart; Africa was already an island continent in the early Cretaceous, long before neornithes evolved. Indeed, no african palaeognaths have been recognized so far with the possible exception of Eremopezus, and Paleocene and Eocene ratites thought to be related to ostriches, like Remiornis, occur in Europe. Ostriches and aepyornithids could evolved from a common ancestor when India and Madagascar were a single landmass, with both groups evolving independently once India broke apart and moved northwards towards Eurasia.

However, genetic studies revealed that aepyornithids were not a sister clade with ostriches, but were surprisingly more closely related to emus, cassowaries and kiwis, the ratites of Oceania. More impressively, their closest ancestors are none other than kiwis, endemic to New Zealand.

Proapteryx micromeros by Dylan Bajda, a stem-kiwi from the Miocene of Saint Bathans that could probably still fly. The last common ancestor between elephant birds and kiwis would have looked something like this.

Thus, as fitting our understanding of early palaeognaths like lithornithids, the ancestors of elephant birds and kiwis were widely widespread and competent flyers, to the point that some members of this clade remained volant well into the Miocene, after the palaeognath heyday was over (i.e. kiwis; the Saint Bathans proto-kiwi Proapteryx retains features associated with flying birds, meaning it was either volant or recently flightless).

The the prevalence of the closely related Casuariiformes in Australia and the fact that moas reached New Zealand through a trans-Antarctic route, we have two scenarios:

- The aepyornithid + kiwi last common ancestor lived in Australasia, with the ancestors of elephant birds being blown into Madagascar. There is a lot of precedent: many bird species in Madagascar and the Mascarenes evolved from asian or australian ancestors, most notably the dodos and solitaires, which evolved from Papuan pigeons.

- The aepyornithid + kiwi last common ancestor lived in Antarctica and simply migrated northwards. Antarctica was in fact a ratite hotspot in the early Cenozoic, with the tinamou + moa clade being yet another example that flying palaeognaths occurred here and migrated either way.

In either case, the process of becoming flightless took widely different turns. Elephant birds must have lost their ability to fly by the Eocene, being massive, specialized herbivores by the Holocene with almost no wings, while kiwis clearly remained volant until the Miocene and indeed are currently smaller and have somewhat more developed wings. The proportionally massive eggs are unique among ratites, and could suggest that they either evolved in the last common ancestor between elephant birds and kiwis, or that they evolved independently in response to a need for superprecociality.

Eggs attributed to aepyornithids are known from the Canary Islands, precisely on the opposite side of Africa, as well as mainland African and Indian sites from the Eocene to Pliocene. Needless to say, in the absence of known aepyornithid fossils from mainland Africa and Asia, they are thought to belong to other birds instead, such as the albatross-like pelagornithids or even ostriches and less well known ratites.

Extinction

Mullerornis by Daniel Foidl. More gracile than Aepyornis, and likely a better runner, it was still a rather robust bird. The last individuals lived as recently as 1260 BP, well after humans reached Madagascar.

Aepyornithids, like the rest of the Holocene megafauna, were brought to extinction due to anthropogenic influence. The humans that colonized Madagascar likely hunted aepyornithids, but apparently not to the extent that they hunted moas; for some reason, vorompatras were apparently considered sacred, and accordingly there’s relatively few specimens that indicate death by humans; notably, nearly all of these specimens belonged to Mullerornis, and not to the larger Aepyornis. The eggs, however, were not regarded to the same standard, and they are much more common in archeological sites.

Other possible causes of extinction were the introduction of diseases transmitted by chickens brought by the human colonizers. Being of Indonesian ancestry, the early colonizers of Madagascar brought with them junglefowl, that likely carried pathogens that affected the native birds of Madagascar. For obvious reasons, this hypothesis has not been tested yet.

In spite of these factors (in part thanks to their sacred status), aepyornithids might have outlived the other members of the Malagasy megafauna by several hundreds of years. Mullerornis is known to have lived until at least the end of the first millenium, and Aepyornis might have lived to see Europeans arrive to the island. Indeed, the Androy region of Madagascar might have been one of the last places where these birds still dealt; Étienne de Flacourt described the giant birds of the Ampatres. The name “elephant bird” was attributed due to the legend of the Roc, a bird of arabian lore capable of carrying elephants, and due to the neotenous appearance of ratites, it would had been easy to see the vorompatras as chicks of a gigantic bird. It is possible that folk memories of the Mahery helped as well.

Conclusion

Aepyornis by Brian Choo.

As familiar as they are alien, vorompatras are one of those seriously underestimated prehistoric animals that nonetheless make it into the broader conscious, as vaguely as that happens. They do remind me of giraffes, in a way: always there, in the scenery, rarely in the foreground.

Hopefully, I’ve inspired to take a closer look at Madagascar’s avian giants.

References

Mitchell, Kieren J.; et al. 2014. “Ancient DNA reveals elephant birds and kiwi are sister taxa and clarifies ratite bird evolution”. Science, vol. 344, no. 6186, pp. 898–900; doi: 10.1126/science.1251981

Buffetaut, E.; Angst, D. (November 2014). “Stratigraphic distribution of large flightless birds in the Palaeogene of Europe and its palaeobiological and palaeogeographical implications”. Earth-Science Reviews. 138: 394–408. doi:10.1016/j.earscirev.2014.07.001.

Cheke, Anthony S.; Hume, Julian Pender (2008). Lost Land of the Dodo: an Ecological History of Mauritius, Réunion & Rodrigues. New Haven and London: T. & A. D. Poyser. ISBN 978–0–7136–6544–4.

Yonezawa, T.; Segawa, T.; Mori, H.; Campos, P. F.; Hongoh, Y.; Endo, H.; Akiyoshi, A.; Kohno, N.; Nishida, S.; Wu, J.; Jin, H.; Adachi, J.; Kishino, H.; Kurokawa, K.; Nogi, Y.; Tanabe, H.; Mukoyama, H.; Yoshida, K.; Rasoamiaramanana, A.; Yamagishi, S.; Hayashi, Y.; Yoshida, A.; Koike, H.; Akishinonomiya, F.; Willerslev, E.; Hasegawa, M. (2016–12–15). “Phylogenomics and Morphology of Extinct Paleognaths Reveal the Origin and Evolution of the Ratites”. Current Biology. 27 (1): 68–77. PMID 27989673. doi:10.1016/j.cub.2016.10.029.