Here’s an old article ‘from the archives’. Actually, it's two articles combined: both originally appeared at Tet Zoo ver 1 in 2006, and both are included together in Tetrapod Zoology Book One. I’ve made no effort to update the text (bar minor tweaks). If I did, I’d write about the various new Cretaceous fleas and other parasitic or possibly parasitic arthropods since reported from the Mesozoic fossil record. Other additions and corrections would be included as well – hey, we can cover them in the comments section.
Don’t take this the wrong way, but I love parasites, and if only there were more parasitic tetrapods I might get seriously, seriously interested in them. Not only is the biology and evolution of parasites really fascinating, the anti-parasite responses evolved by host species are too. And as we’re going to see here, parasites might be so important to some tetrapods that their presence has exerted a significant evolutionary pressure. In particular we’re going to look at how birds have evolved to cope with certain ectoparasites. As we’ll see, it may be that ectoparasites have had a significant effect on the evolution of other tetrapod groups too. [Adjacent image, by Dale H. Clayton and Sarah E. Bush, University of Utah, originally from this 2003 article].
Feathers get dirty, damaged, stuck together and, perhaps most significantly, they harbour ectoparasites, including feather lice, fleas, bugs, ticks and feather mites. Though there are bird species with specialized pedal claws that function in preening (namely herons, pratincoles and nightjars), birds rely on their bills when cleaning their feathers and removing ectoparasites. In fact so important is the bill in keeping the feathers clean and relatively free of parasites that preening may – if the conclusions of some recent studies are to be accepted – be one of the bill’s most important functions.
The over-riding factor controlling bill shape has, conventionally, been thought to be food type and resource acquisition. Clearly this is still one of the most important, if not the most important factor controlling bill shape, otherwise we wouldn’t have curlews, ibises, sword-billed hummingbirds, flamingos, crossbills, or all those oystercatcher polymorphs. But ornithologists have lately started to notice that bill shape makes an awful lot of difference to parasite load. Given that parasites have been shown to have a major impact on fitness, and therefore on breeding success (Clayton 1990) and even on survival rate (Clayton et al. 1999), it follows that anti-parasite adaptations might be really important.
One of the first studies to document this anti-parasite function was Clayton & Walther’s (2001) on Peruvian Neotropical birds and their lice. Looking at species as diverse as owls, woodpeckers, barbets, jacamars, swifts, hummingbirds, pigeons, tyrant flycatchers, ovenbirds and swallows, they showed that those species with longer maxillary overhangs (viz, long edges to the upper mandibular tomia that overlap the edges of the lower mandibular tomia when the bill is closed) harboured less lice species than those species with short overhangs. Moyer et al. (2002) then noted that bill shape had an effect on parasite loads even within a single species: the Western scrub-jay Aphelocoma californica [Photo below courtsey of Msulis].
Western scrub-jays are yet another example of resource polymorphism, an area discussed previously when I've written about oystercatchers. Those scrub-jays inhabiting oak woodland have hooked bills with long maxillary overhangs while those of pinyon-juniper woodlands have pointed bills with short overhangs: the oak woodland birds eat acorns while the pinyon-juniper woodland birds extract seeds from pine cones. Because they use their jaw tips as forceps to get the seeds out, the pinyon-juniper woodland birds seem to have secondarily reduced their overhangs. These two different bill shapes appear to correlate directly with louse control, as pinyon-juniper woodland Western scrub-jays have significantly more lice than the oak woodland Western scrub-jays, and this is despite the fact that oak woodland birds are physically larger and inhabitants of a more humid environment than pinyon-juniper woodland birds (Moyer et al. 2002). Pretty compelling stuff.
Dispatching certain ectoparasites – notably fleas and feather lice – isn’t easy because the tough, flattened bodies of these arthropods are really good at resisting pressure. Simply grabbing the parasite and biting on it (thereby exerting vertical force onto the animal) isn’t good enough, and Clayton & Walther (2001) proposed that the birds have to generate a shearing force in order to kill a captured parasite. Keep in mind that, once captured in the bill, the parasites do actually have to be killed, as if they’re dropped they simply jump or climb straight back onto the host.
To test the idea that maxillary overhangs might function in parasite control, Clayton et al. (2005) trimmed the bills of juvenile Rock doves Columba livia (sorry, I can’t bring myself to call them Rock pigeons [their new ‘official’ name]). This only involves removing 1-2 mm of the tomium by the way – it isn’t anything like the brutal de-beaking indulged in by the factory chicken industry. Clayton et al. (2005) found that the trimming had no significant effect on the pigeon’s feeding efficiency, so maxillary overhangs apparently do not exist for reasons related to feeding. But trimming did have a major impact on parasite load: trimmed birds were unable to keep their parasite loads down and exhibited a significant increase in feather damage relative to untrimmed birds. Trimmed birds that were allowed to regrow their overhangs “caused an immediate reduction in lice” (p. 815).
Does the overhang work by allowing shearing of captured parasites? Using both high-speed video and data from strain gauge apparatus, it seems that pigeons move the lower jaw and upper maxillary overhang in concert, with the lower jaw exerting compressive strain against the overhang and generating a shearing force. This happens incredibly quickly, with the lower jaw being moved forward up to 31 times per second (Clayton et al. 2005, p. 815). The physical damage observed on lice killed by untrimmed pigeons was consistent with death by shearing: decapitation, lacerations of the exoskeleton and missing legs.
So the case, as demonstrated across a diverse range of avian taxa, looks pretty good. Maxillary overhangs really are important in parasite control, and the adaptive radiation of beak morphology should be re-assessed with both feeding and preening in mind.
But, like any interesting discovery, this now raises several new questions. Not all birds have maxillary overhangs: as Clayton et al. noted, many birds with specialized bills (including oystercatchers, darters, herons, woodpeckers, hummingbirds and scythebills) lack overhangs altogether, yet we know that these species have ectoparasites. We saw earlier how some birds have evolved pedal claws that probably function in preening, but given that these are also absent in some of the groups that lack overhangs, other defensive adaptations must be present. Some passerines are now known to be toxic [see links below], and it’s been suggested that these toxins might function in parasite control (Mouritsen & Madsen 1994). In fact it’s worth wondering if toxins are actually more widespread, and if they might be present in species that lack morphological structures that function in parasite control. Toxic oystercatchers? Well, maybe not, as birds can also use sunning, dust-bathing and other behaviours to control ectoparasites.
Obviously, Clayton et al. (2005) only considered what implications their study might have for living birds. But as a palaeontologist I’m going to do the logical thing and wonder what this might mean for fossil feathered taxa.
An oviraptorosaur’s eye view
Fossil birds belonging to the same groups as extant species surely used their bills in the same manner as extant species, so dodos, teratorns and presbyornithids almost certainly found their bills to be as essential for preening as do modern pigeons, raptors and ducks. But of course we know that feathers weren’t unique to ‘modern-type’ birds: they were also present in the birds of the Mesozoic (going all the way back to the archaeopterygids, and including a diverse aviary of yandangornithids, confuciusornithids, enantiornithines, hesperornithines and others) AND they were also present in non-avialan maniraptoran theropods. We know that true feathers were present in oviraptorosaurs, microraptorines and almost certainly troodontids (Jinfengopteryx, a luxuriantly feathered little theropod described in 2005 as an archaeopterygid, is almost certainly a troodontid). Furthermore, probable ‘proto-feathers’ (rather simple quill-like integumentary structures, almost certainly the morphological ancestors of true, complex feathers) were present in compsognathids, tyrannosauroids and alvarezsaurids at least.
We also know that ectoparasites were infesting feathers by the Cretaceous at least. How do we know this? Martill & Davis (1998, 2001) described an isolated feather from the Lower Cretaceous Crato Formation of Brazil that is covered in more than 240 hollow spheres that are almost certainly feather mite eggs [UPDATE: since I wrote this, it’s been argued that the spheres are the eggs of aquatic crustaceans. Some ostracod species often use submerged feathers and leaves as substrates for egg-laying]. We also know that fleas were present in the Lower Cretaceous as there are two particularly good ones known from Australia (Riek 1970), and we also know of possible fleas and odd long-legged possibly parasitic insects from the Lower Cretaceous of Russia (Ponomarenko 1976). Terrestrial birds whose plumage is superficially similar to that of fuzzy small theropods are notorious for harbouring ectoparasites, with kiwis in particular being reported to crawl with numerous fleas, ticks, feather mites and lice (Kleinpaste 1991). So, I would be confident that Mesozoic birds, and fuzzy and feathered non-avialan theropods, had to contend with ectoparasites. What then did they do about parasite control?
Unfortunately we don’t know enough about the rhamphothecae of Mesozoic birds and bird-like maniraptorans to determine whether or not they had a maxillary overhang: the preservation simply isn’t good enough. But maybe some of these animals didn’t need a maxillary overhang given that many of them had teeth. Indeed several Mesozoic maniraptorans possess just a few teeth at the jaw tips, or even just in the upper jaw tips.
Take the feathered turkey-sized short-skulled oviraptorosaurs Protarchaeopteryx* and Caudipteryx (if you’ve heard that these animals aren’t oviraptorosaurs but actually flightless birds, ignore it: it’s a theory based on wishful thinking and misinterpretation of morphological evidence). In Protarchaeopteryx, teeth are restricted to the premaxillae and anterior parts of the maxillae and dentaries, with the premaxillary teeth being a few times taller than the others (Ji et al. 1998). In Caudipteryx [adjacent life reconstruction by Matt Martyniuk of DinoGoss], four procumbent teeth are present in each premaxilla, but the rest of the skull is edentulous. Incisivosaurus – closely related to, and possibly congeneric with, Protarchaeopteryx – has a reduced compliment of teeth, all of which are restricted to the anterior parts of the jaws, and two enlarged, bunny-like incisiform teeth project from each premaxilla (image at top: widely available on the web). Later oviraptorosaurs were toothless, but the bony premaxillary margins of their upper jaw were serrated, raising the possibility that the tomium was serrated too. Could these serrations have been used in ectoparasite control?
* Not a typo! I’ve lost count of how many times I’ve seen this name ‘corrected’ (to ‘Protoarchaeopteryx’) by well-meaning editors.
Among other non-avialan feathered maniraptorans, it’s worth noting that microraptorines also exhibit an unusual premaxillary dentition. In Sinornithosaurus, a diastema separates the premaxillary teeth from the maxillary teeth, and the premaxillary teeth appear notably shorter than the maxillary ones (Xu & Wu 2001). While proportionally small premaxillary teeth are seen elsewhere in theropods (e.g., in tyrannosauroids), the combination of reduced dentition and diastema isn’t, and we know without question that microraptorines had complex, vaned feathers on their limbs and tails. It’s at least suggestive that the premaxillary teeth were used for preening.
Having mentioned tyrannosauroids, I might also note that forms combine proportionally small premaxillary teeth with quill-like integumentary structures that would have needed preening (or is grooming the correct term here?). Could those little premaxillary teeth have been specialized for ectoparasite control? I know this is grotesque speculation of the worst kind, but read on.
Moving now to Mesozoic birds, given that there was a trend in some lineages toward reduction and loss of teeth, it follows that members of these lineages exhibit reduced numbers of teeth relative to archaeopterygids and non-avialan theropods. It seems that these birds lost the teeth from the back of the jaws first, and kept their premaxillary and dentary-tip teeth the longest. Even in forms that don’t have a reduced dentition however, we see slight heterodonty, and thus some suggestion that the anterior-most teeth were being used for something special. In archaeopterygids for example, the premaxillary teeth are more peg-like and more procumbent than are the other teeth. Aberratiodontus - an odd toothed bird from the Chinese Jiufotang Formation - has teeth lining both its upper and lower jaws, but is reported to have rather small teeth at the jaw tips (Gong et al. 2004).
When we start looking at some of the more unusual Mesozoic birds groups, we see marked specialisation of the rostral-most dentition. Bizarre long-tailed, robust-jawed Jeholornis (almost certainly synonymous with Shenzhouraptor, and perhaps with Jixiangornis too), known from stomach contents to have eaten seeds at least occasionally, has just three very small teeth at each lower jaw tip (Zhou & Zhang 2002): the upper jaw was edentulous.
The unusual long-armed Sapeornis, also from the Jiufutang Formation, had a rather short, Caudipteryx-like skull, and short, conical, unserrated, procumbent teeth projected from its premaxillae (Zhou & Zhang 2003). Its dentaries were toothless (and its maxillae probably were too). The somewhat similar Omnivoropteryx, also from the Jiufutang Formation, was also short-skulled, and also has just a few procumbent teeth restricted to the premaxillae (Czerkas & Ji 2002).
Most (but not all) enantiornithines were toothed, and ancestrally they had teeth lining their upper and lower jaws as archaeopterygids did. But in the Yixian Formation enantiornithine Protopteryx there are just two conical, unserrated teeth in the premaxillae and two subtriangular teeth at the dentary tips (Zhang & Zhou 2000). It doesn’t seem that having a total of four teeth is a tremendously useful thing if you need those teeth to procure or dismember your food, and it’s intriguing that Protopteryx possesses highly elongate, strap-like rectrices that would (presumably) have needed careful preening. The euenantiornithine Eoenantiornis has four subconical teeth in each premaxilla while there were probably six or seven teeth in each dentary, the rostral-most two of which were larger than the others (Zhou et al. 2005). Long-skulled Longirostravis has ten small, conical teeth restricted entirely to its slim jaw tips (Hou et al. 2004) and short, conical teeth are similarly only at the jaw tips in another long-skulled enantiornithine, Longipteryx (Zhang et al. 2001). And there are yet other examples of this sort of thing.
So far as I can see from all these unusual patterns of dentition, there are three possible explanations:- (1) as dental reduction occured, a gradual step-wise loss of teeth simply meant that premaxillary and/or dentary-tip teeth were the last to go; (2) premaxillary and/or dentary-tip teeth were retained in specialized taxa that used those teeth to procure or dismember whatever it was that they were eating; (3) premaxillary and/or dentary-tip teeth were retained - even when not essential to foraging or feeding - as they were used in ectoparasite control.
While it’s nice to speculate – and so far that’s all I’ve done here – how might we test the idea that these Mesozoic taxa were using their unusual rostral teeth to preen with? Herein lies the rub, as I can't think of a reliable test. So far as we know, feathers aren’t abrasive enough to leave any sort of distinctive microwear on teeth, or even on rhamphothecae, so there isn’t going to be any sort of tooth wear that can be correlated with preening [UPDATE: in mammals, distinctive ‘grooming marks’ are left on teeth, so I still hold out hope that structures of this sort are findable in toothed dinosaurs]. It’s possible that there might be some sort of correlation between tooth spacing and feather morphology, but I find this unlikely.
Conversely, we can test the idea that teeth were used in feeding, as feeding does leave visible sorts of micro- or macrowear. Earlier I mentioned the bunny-like teeth of Incisivosaurus, and because its incisiform teeth do exhibit wear facets, they were almost certainly used in feeding. This confirms ‘explanation 2’ given above, and therefore indicates that ‘explanation 3’ didn’t apply in this case. But the two ‘explanations’ aren’t mutually exclusive, as the teeth could still have been important in ectoparasite control.
Those short premaxillary teeth present in tyrannosauroids have conventionally been regarded as having a primary role in feeding, and it might be easy to confirm this by looking for micro- or macrowear. And yes, I consider it highly speculative to wonder if those teeth might have functioned in grooming/preening, but I couldn’t resist mentioning it (I have SEM data on the premaxillary teeth of the tyrannosauroid Eotyrannus, but it doesn't reveal anything especially relevant).
Finally, if specialised teeth could be shown to have no important function in foraging or feeding behaviour it might then be logical to infer that preening was their primary function - - but, how on earth would you show that they had ‘no function’ in foraging or feeding behaviour? This just isn’t possible in Mesozoic animals when so little is known of their ecology. An analogy does come to mind: it’s been shown that the unusual dentary teeth of Impala Aepyceros melampus have a morphology specialised for a primary function in grooming. If impalas were extinct I suppose it’s possible that people might have worked this out, but how would you verify it? Does anyone have any better ideas?
I’m far from the first person to look at Mesozoic feathered theropods this way – many other people have mentioned these ideas before, and artists have even illustrated ectoparasite control in dinosaurs. In Dinosaurs of the Air Greg Paul illustrated a Sinosauropteryx scratching in order to remove ectoparasites, and the cover of The Dinosauria, Second Edition (the current industry-standard volume on dinosaurs) features a Sinosauropteryx (this time by Mark Hallett) nibbling at its proto-feathers, again presumably for reasons of ectoparasite control.
But I don’t think anyone’s really married data on Mesozoic birds and other theropods with the new work of Dale Clayton and colleagues on ectoparasite control in extant birds. Maybe this idea will bear proverbial fruit down the line, but for now this is where my contribution ends.
Finally, here’s another spin on this subject. Theropods weren’t the only Mesozoic tetrapods with a furry coat of integumentary fibres: we also know that pterosaurs were fuzzy too. So did they also have to contend with ectoparasites? I’ll say no more on this topic, but perhaps it can be elaborated on at another time.
For previous Tet Zoo articles on some of the topics relevant here, see...
- Sexual dimorphism in bird bills: commoner than we’d thought
- Ifrita the poisonous passerine
- Aberratiodontus: worst paper ever?
- The incredible bill of the oystercatcher
- Sunbathing birds
- Three remarkable hummingbird discoveries
- Did dinosaurs and pterosaurs practise mutual sexual selection?
- There are giant feathered tyrannosaurs now… right?
Refs - -
Clayton, D. H. 1990. Mate choice in experimentally parasitized rock doves: lousy males lose. American Zoologist 30, 251-262.
Clayton, D. H., Lee, P. L. M., Tompkins, D. M. & Brodie, E. D. 1999. Reciprocal natural selection on host-parasite phenotypes. American Naturalist 154, 261-270.
Clayton, D. H., Moyer, B. R., Bush, S. E., Jones, T. G., Gardiner, D. W., Rhodes, B. B,. & Goller, F. 2005. Adaptive significance of avian beak morphology for ectoparasite control. Proceedings of the Royal Society London B 272, 811-817.
Clayton, D. H. & Walther, B. A. 2001. Influence of host ecology and morphology on the diversity of Neotropical bird lice. Oikos 94, 455-467.
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