Wednesday, July 05, 2006

The war on parasites: a pigeon’s eye view

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.

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.

Western scrub-jays are yet another example of resource polymorphism, an area discussed previously when relevant to oystercatchers (go here). 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 [the scrub-jay photo used here is from TexasPhotoArchives].

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 (therby 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). You can see the high-speed video of this (and also get pdfs of some of Dale Clayton's papers) here. 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 (go here for more on this), 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. And as it happens there’s quite a lot to say about this. More in the next post… The war on parasites: an oviraptorosaur’s eye view.

The image at top shows a preening pigeon superimposed on a closeup image of a pigeon feather. Lice are trying to hide between the barbs, and hence escape preening. The image was produced by Dale Clayton and Sarah Bush (University of Utah) and I took it from the Innovations Report site.

PS - for the latest news on Tetrapod Zoology do go here.

Refs - -

Clayton, D. H. 1990. Mate choice in experimentally parasitized rock doves: lousy males lose. American Zoologist 30, 251-262.

- ., Lee, P. L. M., Tompkins, D. M. & Brodie, E. D. 1999. Reciprocal natural selection on host-parasite phenotypes. American Naturalist 154, 261-270.

- ., 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.

- . & Walther, B. A. 2001. Influence of host ecology and morphology on the diversity of Neotropical bird lice. Oikos 94, 455-467.

Moyer, B. R., Peterson, A. T. & Clayton, D. H. 2002. Influence of bill shape on ectoparasite load in Western scrub-jays. Condor 104, 675-678.

Mouritsen, K. N. & Madsen, J. 1994. Toxic birds: defence against parasites? Oikos 69, 357-358.


Blogger pluvialis said...

Awesome post!

9:37 PM  
Blogger VaneWimsey said...

But if scrub jays' beaks have changed in response to feeding pressure, despite an increased parasite load, doesn't that mean (from the evidence of this one case, anyway) that parasite load is NOT a significant factor in beak evolution?

5:43 AM  
Blogger Steve Bodio said...

I am a tetrapod guy myself but I sometimes wish you would write more on parasite evolution, one of the world's most fascinating subjects. Great post!

4:01 PM  
Blogger Darren Naish said...

Thanks to all for their comments.

Response to Vanewimsey: good point, but do note statements in the post that ectoparasite control might be ONE OF the bill's most important functions, not THE most important function. And as I said (third paragraph), I think it's safe to assume that resource acquisition remains the 'primary' function of the bill.

10:55 PM  
Blogger monado said...

This is slightly off-topic, but did you hear of the study of head-lice in humans found two types so different it concluded that one of them must have transferred from Homo erectus? Mega-cool: we must have been interacting.

5:59 AM  
Blogger Darren Naish said...

Thanks Monado. On a similar note, there's a paper in the new PLoS Genetics which argues that modern big cats became infected with the ulcer-forming Helicobacter bacteria they possess after eating Helicobacter-carrying humans. Very neat.

1:55 PM  
Anonymous Anonymous said...

Are these populations of scrub-jays found near each other? You mention oak woodland and pinyon/juniper populations, but that sounds like coastal California and interior populations, which are pretty much allopatric and used to be considered as separate (sub)species--California Jay and Woodhouse's Jay I believe. So wouldn't this be a case of differences among related taxa rather than resource polymorphism in a single species? Or am I off base?

2:59 AM  

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