Bucorvids: post-Cretaceous maniraptorans on the savannah
Yes I’ve been to Marwell zoo again (see What I saw at the zoo and More on what I saw at the zoo). Mark Witton and Graeme Elliott were in attendance: it was a sort of University of Portsmouth Palaeobiology Research Group Day Out. We were frustrated by anteaters, humbled by rhinos, awed by megabats, and salivated on by giraffes.
Ground hornbills are big birds, reaching 4 kg in weight and with a wingspan that can reach 2 m. They're entirely black except for their white primaries and for the bright red fleshy wattles that decorate their faces and throats (a second species in the genus Bucorvus [which means ‘big crow’], the Northern or Abyssinian ground hornbill B. abyssinicus, has red and blue facial skin in males and all-blue skin in females). Inhabiting the wooded savannahs of tropical southern African, Southern ground hornbills forage on the ground, picking up animal prey from among the grass or from low-growing vegetation, and grabbing everything from insects, snails, arachnids and worms to lizards, snakes, tortoises and even squirrels and hares. They may also excavate wasp and bee nests. Prey is grasped delicately with the forceps-like bill tips and snakes and other dangerous prey may be repeatedly squeezed at the jaw tips until dead. Prey is swallowed using a ‘throw and gulp’ action.
The jaws are laterally compressed and gently curved, and though the bill tips meet when the jaws are in occlusion, a gap is usually visible part way along the jaws, even when they’re closed. The size of the gap seems variable between individuals, and it’s much less pronounced than that seen in some other hornbills, like the red-billed and yellow-billed Tockus species. All hornbills share a heavily reinforced bill: the palatal surface forms a complete bony roof to the mouth, and all of the palatal bones are fused together. This is a modified version of the desmognathous condition and it presumably evolved to provide mechanical support for the bill: among so-called ‘higher landbirds’ it is present in birds that kill and consume active prey, as well as in forms that beat prey dead against a perch. Among this lot are motmots, bee-eaters and rollers. This isn’t the whole story behind the desmognathous palate incidentally, as it’s also present in waterfowl, ibises, spoonbills, pelicans and other groups (Huxley 1867).
Hornbills are also unusual in possessing a unique ligament – the quadratomandibular ligament – that connects the body of the quadrate with the inside surface of the lower jaw. In ground hornbills the anatomy of the quadratomandibular ligament makes it impossible for the upper jaw to be raised or lowered without an automatic lowering or raising of the lower jaw, and the ligament is so strong that the lower jaw stays connected to the skull even in dried skeletons (Burton 1984). The hornbill quadratomandibular ligament was only discovered in 1940, and as Walter Bock noted in 1964 it has been mostly overlooked and little studied. Oh, if all this talk of ‘raising or lowering the upper jaw’ confuses you, I should explain that a special hinge zone at the base of the bill allows hornbills (and other birds with the same sort of hinge zone) to raise and lower the entire upper jaw relative to the rest of the skull, an ability termed prokinesis.
Given the importance of the bill tips in handling prey, it would make sense if the birds could see the end of their own bill, and indeed work on the visual field perceived by the birds indicates that the bill tips do indeed intrude into the lower part of the hornbill’s binocular field. This is highly unusual among birds and it seems that the huge decurved bill and precision-grasping feeding technique that hornbills employ evolved in concert with their visual field (Martin & Coetzee 2004) [if you’re really interested in this particular subject do check out Graham Martin’s website]. Immense, stiff, flattened and widely spaced black eyelashes, the longest of which are 18 mm long, encircle the eye and overhang its upper part. The birds seem to use these as sunshades, deliberately positioning the head so that the cornea is shaded from bright light when appropriate (Martin & Coetzee 2004).
Several features of the hornbill head and neck seem specially suited to help support the big, heavy head. Ground hornbills have more cervical vertebrae than other hornbills (15 opposed to 14), but like other hornbills their atlas and axis (the two vertebrae closest to the skull) are fused together. This is unique among birds, with the exception of one-off freaks. While most birds have just one occipital condyle, hornbills have two, as there is an accessory one on the supraoccipital (the bone that forms the upper border to the foramen magnum). Some of their neck muscles have special accessory slips that insert further down the cervical column than is typical for birds, and presumably this assists in carrying and moving the large head (Burton 1984). What’s also odd about ground hornbill neck anatomy is that they have no cranial carotid arteries (Ottley 1879), and don’t ask me how that works.
What of course makes hornbills immediately distinct is the presence of the bony casque that sits on top of the bill. In ground hornbills this is a modest structure located dorsal to the proximal part of the bill, ramified internally by large spaces and sheathed in life by keratin (in the Northern ground hornbill the casque is much taller than that of the southern species). Basal hornbills, which probably include the ground hornbills (read on), have a small casque that is often little more than a mid-line dorsal ridge on the bill, but in more derived forms it is a large, mostly hollow structures supported internally by strut-like trabeculae (Kemp 1995): for images of sectioned casques go here. Casques probably function as identification devices as they differ in shape between species, sexes and growth stages, but an intriguing proposal is that they function as resonating devices used to amplify calls (Alexander et al. 1994). Those of you reading Bousfield & LeBlond’s (1995) Cadborosaurus monograph right now – you know who you are – will be amused to see Alexander et al.’s paper cited therein, I kid you not.
In terms of casque morphology, the most strongly modified hornbill is the Helmeted hornbill Rhinoplax vigil, a territorial fig specialist of SE Asia. The casque of this species is solid, looks like a block of ivory – it’s actually called hornbill ivory* – and, believe it or don’t, is employed in aerial jousting. During this behaviour flying males smack their casques together, the resulting CLACK being audible from at least 100 m away (Kinnaird et al. 2003). The blunt leading edge of the casque might actually result from this head-butting behaviour. If you want to know what a Rhinoplax casque looks like in section, visit the relevant page on Matt Wedel's site (here). Thanks to Matt for reminding me about this.
* It’s prized for carving by Chinese and Japanese artists, being used by the latter for netsuke sculptures.
Anyway, I digress. Compared to other hornbills, ground hornbills have elongate tarsometatarsi, and they also have short toes, though strangely with the hallux being the longest of the four (note that this is rarely depicted accurately in artwork). The scutes covering the tarsus look odd: large, non-imbricating scutes are scattered along the anterior surface like crazy paving, and not arranged in a row as is normally the case in birds with large tarsal scutes. Ground hornbills are reported to be able to run extremely quickly, apparently at speeds of up to 30 km/h, and though they do their foraging by striding around on the ground, they’re capable, though reluctant, fliers (see adjacent image, borrowed from Natural Encounters).
Their social behaviour is interesting in that non-breeding individuals, including immatures of both sexes and adult males, assist breeding pairs in raising their young. As many as 12 non-breeders may collaborate to assist a single breeding pair. All of these birds are related and know each other well, and they use intimidation, play, mutual grooming and other forms of interaction to cement social bonds. It is well known that hornbill females become walled into a cavity nest while they incubate their eggs and raise their chicks, but ground hornbills are unique among the group in not doing this. Natural cavities in rocks or trees are used, and of the 1-3 eggs laid only one chick ever survives. The ‘surplus’ chicks may perhaps be an insurance should the first-hatched chick die. Apparently no ground hornbill has ever been known to raise more than one chick, but if you look at the title of Kemp & Kemp (in press) below – a reference I borrowed from Alan Kemp’s website – you’ll see that some new data on this is soon to be published. Kemp is a leading expert on hornbills and has been involved in a long-term field study of ground hornbills.
Once chicks fledge, their mortality rates are low (31% survive to maturity), but they’re tremendously slow in maturing, taking about 6 years. In keeping with this, ground hornbills are very slow breeders, fledging on average one chick every 9 years. Pairs may go for as long as 18 years without breeding. Unsurprisingly, ground hornbills are highly vulnerable to human persecution and habitat loss, and because they rely on a few species of large trees for nesting, and even then require special trees that have natural cavities, the number of available nest sites may be a limiting factor on their distribution. As you would guess for all this K-strategy behaviour, they are long-lived: Kemp (1996) suggested that they might be among the longest-lived of birds, perhaps surviving into their fourth decade.
So in ground hornbills we seem to have slow-breeding, terrestrial, ground-feeding, carnivorous savannah-dwellers that belong to a clade of mostly arboreal, forest-dwelling frugivores. Kemp has noted that ground hornbills therefore seem to have followed a similar evolutionary path to us hominids (Kemp 1996). The complex social behaviour and apparent intelligence of the birds also makes them reminiscent of primates, though note that I don’t want to promote the horrible opinion that the only time non-mammals become interesting is when they somehow seem mammalian in their behaviour or biology.
Phylogenetic studies indicate that ground hornbills are most closely related to the SE Asian Buceros hornbills, all of which are arboreal inhabitants of tropical forests (Kemp 1995, 2001). It is also fairly well agreed nowadays that Murie (1873) was right in arguing that hornbills are close allies of hoopoes and wood-hoopoes, the Upupiformes (Burton 1984, Olson 1985, Mayr 2000, 2003, Mayr et al. 2003). In fact some workers now use the term Upupiformes for this hornbill + hoopoe + wood-hoopoe clade (Mayr 2003). If you’re more familiar with the inclusion of these birds within Coraciiformes – the name previously used for rollers, kingfishers, bee-eaters, todies, motmots, hoopoes and hornbills – then you’ll be interested to know that there is now good evidence indicating that this grouping is artificial. More about that another time.
Anyway, this phylogenetic data indicates that the ancestors of ground hornbills were woodland or forest birds, and that the unusual behavioural characters of ground hornbills – the carnivory, the terrestriality, the striding gait (other hornbills hop when on the ground), the savannah habitat – are derived novelties. Indeed it’s been suggested at times that the Bucorvus species are so unusual compared to other upupiforms that they should get their own ‘family’, Bucorvidae (Kemp 1995). This wasn’t followed in the most recent review of the group however (Kemp 2001). What’s more, we know that ground hornbills have been doing what they do for quite a long time, as a fossil member of the genus, Bucorvus brailloni, is known from the Miocene (Brunet 1971). It’s from north of the Moroccan Atlas Mountains, and hence well north of where ground hornbills occur today.
While there are good phylogenetic reasons for thinking that ground hornbills descended from arboreal forest-dwelling ancestors, it’s unfortunate that there aren’t yet any fossils to support this. A few alleged hornbill fossils have been reported from Eocene and Miocene Germany and France (Geiseloceros robustus, Cryptornis antiquus and Homalopus picoides) but Olson (1985) showed that none of them are really hornbills. However, hornbills almost certainly originated in the Eocene at least, as we now know that close relatives of hoopoes had appeared by this time (Mayr 2000). We are simply missing the fossils.
Of course you don’t need to compare ground hornbills with Cretaceous predatory dinosaurs, or with hominids or other primates, to make them interesting. But I can’t help coming back to Russell & Séguin’s ‘dinosauroid’ hypothesis. No, post-Cretaceous maniraptorans wouldn’t end up looking like scaly tridactyl plantigrade humanoids with erect tailless bodies. They would be decked out with feathers and brightly coloured skin ornaments; have nice normal horizontal bodies and digitigrade feet; long, hard, powerful jaws; stride around on the savannah kicking the shit out of little mammals; and in the evenings they would stand together in the trees, booming out a duet of du du du-du, a deep noise that would reverberate for miles around.
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Refs - -
Alexander, G. D., Houston, D. C. & Campbell, M. 1994. A possible acoustic function for the casque structure in hornbills (Bucerotidae). Journal of Zoology 233, 57-67.
Brunet, J. 1971. Oiseaux miocénes de Beni-Mellal (Maroc); un complement à leur etude. Notes et Mémoires Services Géoloques (Morocco) 31, 109-111.
Bousfield, E. L. & LeBlond, P. H. 1995. An account of Cadborosaurus willsi, new genus, new species, a large aquatic reptile from the Pacific coast of North America. Amphipacifica 1 (supplement 1), 1-25.
Burton, P. J. K. 1984. Anatomy and evolution of the feeding apparatus in the avian orders Coraciiformes and Piciformes. Bulletin of the British Museum of Natural History (Zoology) 47, 331-443.
Huxley, T. H. 1867. On the classification of birds; and on the taxonomic value of the modification of certain of the cranial bones observable in that class. Proceedings of the Zoological Society of London 1867, 415-472.
Kemp, A. C. 1995. The Hornbills. Oxford University Press, Oxford.
- . 1996. Hammer of the savannah. BBC Wildlife 14 (5), 32-36.
- . 2001. Family Bucerotidae (Hornbills). In del Hoyo, J., Elliott, A. & Sargatal, J. (eds) Handbook of the Birds of the World, vol. 3. Lynx Edicions, Barcelona, pp. 436-523.
- . & Kemp, M. I. In press. How often might Southern ground hornbills fledge two chicks? Data from the Kruger National Park, 1967-1999. In Proceedings 4th International Hornbill Conference, Mabula Game Lodge, Bela Bela.
Kinnaird, M. F., Hadiprakarsa, Y.-Y. & Thiensongrusamee, P. 2003. Aerial jousting by Helmeted hornbills Rhinoplax vigil: observations from Indonesia and Thailand. Ibis 145, 506-508.
Martin, G. R. & Coetzee, H. C. 2004. Visual fields in hornbills: precision-grasping and sunshades. Ibis 146, 18-26.
Mayr, G. 2000. Tiny hoopoe-like birds from the Middle Eocene of Messel (Germany). The Auk 117, 964-970.
- . 2003. On the phylogenetic relationships of trogons (Aves, Trogonidae). Journal of Avian Biology 34, 81-88.
- ., Manegold, A. & Johansson, U. S. 2003. Monophyletic groups within ‘higher land birds’ – comparison of morphological and molecular data. Journal of Zoological and Systematic Evolutionary Research 41, 233-248.
Murie, J. 1873. On the Upupidae and their relationships. Ibis 15, 181-211.
Olson, S. L. 1985. The fossil record of birds. In Avian Biology, Volume III, pp. 79-238.
Ottley, W. 1879. Bucorvus abyssinicus, on the vessels in its head and neck. Proceedings of the Zoological Society of London 1879, 461-467.
Russell, D. A. & Séguin, R. 1982. Reconstruction of the small Cretaceous theropod Stenonychosaurus inequalis and a hypothetical dinosauroid. Syllogeus 37, 1-43.