The original title for this article was going to be 'Sorry Heteralocha, but you ain't that special'. I ended up deciding against that, however, as I realised that few readers would know what the hell I was on about, nor indeed what Heteralocha is. Heteralocha (Heteralocha acutirostris to be precise) is the Huia, a large wattlebird (callaeid), endemic to New Zealand, that became extinct some time around 1907 (though a few sightings occurred well after this date, leading some to speculate that it might have hung on for longer). What makes the Huia famous is that males and females differed markedly in bill size and shape, with females possessing an elongate, slender, decurved bill, and males a shorter, stouter, far straighter bill [John Gould's classic painting shown here]. Females were otherwise smaller than males. Supposedly a mated pair would work together in order to extract insect prey from rotten wood: the stout-billed male would heroically dig away to expose the tunnel made by a beetle grub, and the curve-billed female would then probe in and grab it (but read on). This is all absolutely amazing: one species acting (and looking) like two. And it's so amazing that the Huia has often been regarded as totally unique: Gill & Martinson (1991), for example, said 'It is the only bird known in which the bill of the male and female are radically different in shape'. Ah, sigh, if only this were true...
It turns out that the Huia isn't as unique as we used to think. Don't get me wrong: it was still remarkable, and indeed the degree of sexual dimorphism it exhibited (the female's bill was about 60% longer than the male's) was still above and beyond that of most of the species that we're about to look at. But the fact is that it wasn't totally unique. Recent work has shown both that Huia-like dimorphism evolved elsewhere in birds, and that sexual dimorphism in bill length and shape is actually quite widespread.
Of hummingbirds and woodhoopoes
Two bird groups in particular have become poster-children for the contention that the Huia wasn't unique: hummingbirds and woodhoopoes. Among hummingbirds, the best example is provided by the Purple-throated carib Eulampis jugularis of the Caribbean (Eulampis is an endemic Caribbean taxon and part of the mango radiation: mangoes are thought to be the sister-taxon to all other trochiline hummingbirds). The bills of females are about 30% longer than those of males and, while males have bills that curve downwards at about 15°;, those of females curve downwards by about 30°; (Temeles et al. 2000, Temeles & Kress 2003) [photos of both sexes shown above, from Ethan Temeles's site]. This pronounced and obvious dimorphism indicates that the sexes are exploiting different niches - or, exhibiting differential niche utilisation (Selander 1966) - and indeed field work has shown that the sexes utilise two different Heliconia species (or, in cases, two different morphs of the same species) that differ in flower size and shape. Incidentally, there are other hummingbirds with bill dimorphism: in the Saw-billed hermit Ramphodon naevius, for example, the bill-tip of males is (unlike that of females) hooked and serrated.
Green woodhoopoes Phoeniculus purpureus (also called Red-billed woodhoopoes) are tropical African woodland birds that forage in family groups and breed co-operatively, with up to ten helpers assisting a breeding pair. And like Huias and Purple-throated caribs, they exhibit strong sexual dimorphism in bill shape and length, with males having bills that are about 36% longer than those of females [image of both sexes here from Andrew Radford's site]. How is this dimorphism manifested in behaviour? Males and females seem to differ in foraging behaviour, with males doing more probing and females doing more pecking. As a result, the sexes differ in the sort of prey they obtain, with males obtaining larger prey that they collect on trunks, and females capturing smaller prey than they find on branches (Radford & du Plessis 2003). Males and females have similarly-sized bills on fledging, and juveniles of both sexes forage like adult females. By four months of age however, males have grown a longer bill and now forage like adult males (Radford & du Plessis 2003).
Dimorphic bills in woodpeckers and waders
While it's true that the degree of bill dimorphism present in the Purple-throated carib and Green woodhoopoe is poorly known, it hasn't exactly been overlooked, and in fact it's mentioned in many books and papers. Less obvious bill dimorphism has also been written about a lot. Bill dimorphism is well documented in woodpeckers and is well marked in several Caribbean species, including the Hispaniolan woodpecker Melanerpes striatus (where the bill of the male is more than 21% longer than that of the female), Puerto Rican woodpecker M. portoricensis (male's bill 18.9% longer than female's), Guadeloupe woodpecker M. herminieri (male's bill 19% longer than female's) and Cuban green woodpecker Xiphidiopicus percussus (male's bill 15.2% longer than female's) (Selander 1966) [Cuban green woodpecker shown here, image by pgiard, from here]. Some of these species don't just differ in the proportional length of the bill, but also in how deep it is as well, with the long-billed males having disproportionately shallow bills while the short bills of the females are disproportionately deep. The tongues of species where the males are disproportionately long-billed are also proportionally different in length. The fact that these dimorphic woodpeckers are island-endemics is probably not a coincidence, as we'll see in a moment.
Sexual dimorphism in bill length has also been noted in waders, with dowitchers, curlews and godwits exhibiting ranges that extend up to a difference of more than 30% in some godwits (I first mentioned this back here in January 2007, and said that I'd be returning to bill dimorphism eventually). The female is the longer-billed sex. While this sexual difference in bill length has led to the obvious proposal that males and females might be able to exploit different niches and avoid competition, it's not entirely clear from the work that's been done that this really is the case (Ferns & Siman 1994, Székely et al. 2000, Nebel et al. 2005), but it probably is.
Less pronounced bill dimorphism is also present elsewhere in birds and is usually limited to a difference in bill length of 11-14%. This is the case in the Varied sitella Daphoenositta chrysoptera, Great frigatebird Fregata minor and Gila woodpecker Melanerpes uropygialis. Among parrots, Bond et al. (1991) showed that Kea Nestor notabilis males (which are about 5% bigger than females in overall size) have a bill that is both 12-14% longer than that of females, and is less curved. Palm cockatoos Probosciger aterrimus also exhibit bill dimorphism (D'Ombrain 1933). It is also present in some pelicans, grebes and honeycreepers [dimorphism in Western grebe Aechmorphorus occidentalis shown here - male above, female below - from Selander (1966)].
Island endemics and the niche separation hypothesis
Island-dwelling birds appear to have a tendency to exhibit marked bill length dimorphism, with sexual bill length variations of between 15 and 21% present in the Maui parrotbill Pseudonestor xanthophrys, Cape Verde lark Alauda razae and in those Caribbean woodpeckers mentioned above. Female Rifleman Acanthisitta chloris have a slightly more upcurved, longer bill than do the smaller males (Hunt & McLean 1993). The Huia represents an extreme case of this of course, and the fact that island birds appear to exhibit more cases of bill dimorphism than their continental relatives led Selander (1966: an award-winning and much cited classic paper) to propose that, in monogamous species in which pairs shared a territory, divergent foraging habits became increasingly advantageous, allowing the sexes to avoid competition and hence improve their fitness. This has become known as the niche separation hypothesis (or as differential niche utilisation).
Can the incredible dimorphism displayed by the Huia be explained by the niche separation hypothesis? If so, why wasn't similar dimorphism evolved by the other wattlebirds? (the Kokako Callaeas cinerea and Saddleback Philesternus carunculatus). What appears to have made the Huia unusual compared to other wattlebirds was its apparent reliance on a comparatively rare prey species, the larvae of the Huhu beetle Prionoplus reticularis. Burton (1974) proposed that, unlike other wattlebirds, the Huia was under strong selective pressure to successfully obtain this prey. We infer that the sexes avoided competing for the same resource by foraging in different ways and in different places, just as has been documented in Green woodhoopoes for example, and indeed there is some observational data that supports this (read on). The other wattlebirds have a far more generalised diet and hence don't seem to have been under the same ecological pressure for the sexes to avoid competition, though male saddlebacks do have longer bills than females so may be partly affected by this (Moorhouse 1996).
Huias: perhaps weirder than you know
While the dimorphism present in the Huia is famous, less well known is that this dimorphism is most obvious in the rhamphothecae (the horny sheaths of the bill) and is not so obvious when you only look at the osteology. Female Huia skulls do have more slender, more curved jaw-tips and more gracile palatal bones than males, but overall male and female skulls look alike and in fact there is at least one skull where the sex is uncertain (Burton 1974) [in image below, rhamphothecae are shown in black. Male skull is above, female below. From Burton (1974)]. Those of us who work on fossil animals often wonder whether the keratinous structures we reconstruct on animal's heads are shown as too elaborate, or as not elaborate enough, but cases like the female Huia suggest that live animals can grow keratinous structures that go above and beyond what we might reasonably predict.
Besides the fact about dimorphism, the other 'fact' that everyone knows about the Huia is that males and females co-operated when feeding. The one account on which this idea is based (that produced by Sir Walter Buller in his 1888 A History of the Birds of New Zealand) really describes no such thing however: Buller actually documented how a captive male and female exhibited different styles of foraging when feeding from different parts of a rotten log, and did not share their food (Jamieson & Spencer 1996).
It is also not widely appreciated that the Huia was not just specialised in its degree of sexual dimorphism: its massive retroarticular process (a prong on the back of the mandible), prominent occipital crest and an accompanying hypertrophied musculature show that it was highly specialised for 'gaping': that is, for forcing the jaws open once they were wedged into a substrate or object. In fact Burton (1974) thought that the Huia was specialised for gaping 'perhaps more so than any bird now living' (p. 36). Rather than hitting wood in order to break it apart, we can infer from this that Huias levered open wood while foraging, and did so with impressive force. We should finish here, the thought of this amazing bird alive nowhere other than in our minds.
Refs - -
Bond, A. B., Wilson, K.-J. & Diamond, J. 1991. Sexual dimorphism in the Kea Nestor notabilis. Emu 91, 12-19.
Burton, P. J. K. 1974. Anatomy of head and neck in the Huia (Heteralocha acutirostris) with comparative notes on other Callaeidae. Bulletin of the British Museum (Natural History), Zoology 27, 1-48.
D'Ombrain, E. A. 1933. Notes on the Great black palm cockatoo. Emu 33, 114-121.
Ferns, P. N. & Siman, H. Y. 1994. Utility of the curved bill of the Curlew Numenius arquata as a foraging tool. Bird Study 41, 102-109.
Gill, B. & Martinson, P. 1991. New Zealand's Extinct Birds. Random Century, Auckland.
Hunt, G. R. & McLean, I. G. 1993. The ecomorphology of sexual dimorphism in the New Zealand rifleman Acanthositta chloris. Emu 93, 71-78.
Jamieson, I. G. & Spencer, H. G. 1996. The bill and foraging behaviour of the Huia (Heteralocha acutirostris): were they unique? Notornis 43, 14-18.
Moorhouse, R. J. 1996. The extraordinary bill dimorphism of the Huia (Heteralocha acutirostris): sexual selection or intersexual competition? Notornis 43, 19-34.
Nebel, S., Jackson, D. L. & Elner, R. W. 2005. Functional association of bill morphology and foraging behaviour in calidrid sandpipers. Animal Biology 55, 235-243.
Radford, A. N. & du Plessis, M. A. 2003. Bill dimorphism and foraging niche partitioning in the green woodhoopoe. Journal of Animal Ecology 72, 258-269.
Selander, R. K. 1966. Sexual dimorphism and differential niche utilization in birds. Condor 68, 113-151.
Székely, T., Reynolds, J. D. & Figuerola, J. 2000. Sexual size dimorphism in shorebirds, gulls, and alcids: the influence of sexual and natural selection. Evolution 54, 1404-1413.
Temeles, E. J. & Kress, W. J. 2003. Adaptation in a plant-hummingbird association. Science 300, 630-633.
- ., Pan, I. L. Brennan, J. L. & Horwitt, J. N. 2000. Evidence for ecological causation of sexual dimorphism in a hummingbird. Science 289, 441-443.
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Lets tease a little:
Is larger bill of a male bird simply a fighting tool in male-male competition, and feeding differences are by-product?
For mammals it is accepted that larger size of males is for sexual competition, but many mammals do exhibit sex-specific differences in foraging. Male elephant seals and sperm whales dive deeper and eat different prey, male european lynx hunt more young deer and less lagomorphs, male pantherine cats hunt larger prey, male bears hunt more and eat less plants etc.
In Raso Lark similar situation was recently observed. Large-billed males not only feed on different food, but also attack and displace females to worse feeding areas, resulting in a highly skewed sex ratio.
Prediction: whichever sex chooses the mate will have the more locally-adapted bill geometry. The other's bill will more resemble that of less dimorphic ancestors.
Fascinating.
1. You rightly point out that there are a number of seemingly reliable sightings post-dating its official extinction. The same is true for a number of other recently extinct species - the thylacine and passenger pigeon come to mind. Unfortunately in most cases this only means that the date is wrong, not that the species still exists. So, for example, I am fairly convinced that the thylacine hung on in Tasmania probably to within the last 30 years, but while I haven't given up hope completely I am rather pessimistic about its continued survival. The huia similarly has reasonable evidence to suggest survival for decades after 1907 - but I see no convincing reason to think there is any likelihood that still exists now.
2. When I was reading your post my initial thought was that the critical difference between the huia and all the other examples was the cooperative use of the different beaks - i.e. that rather than occupying somewhat different niches the male and female had to work together to most effectively occupy thier single niche. But then towards the end of your post you sort of demolished that one with your bombshell that it may be that they didn't cooperate as we thought at all. I am surprised to hear that this was based on a single account, as I assumed this was well established behaviour observed in the wild. Can I ask are we really sure this was the only basis for the idea?
If so it reminds me somewhat of a situation I noted years ago when I used to keep African lake cichlids. In the literature about cichlids in Lake Malawi you may read of the 'Malawi Eye-biter' (Dimidiochromis compressiceps) - which allegedly sidles upto other fish and neatly removes and eats their eyes. I have known a number of people who have kept this fish, and read accounts of others who have even bred it. While it is a serious predator of small fish, it is very peaceful with fish of similar size to itself (indeed much more peaceful than the highly agressive mbuna I kept) and I can find no evidence of this behaviour in captivity, indeed it was widely felt among those I knew who kept it, based on keeping the fish and reading acounts of actual observation in the wild, that the whole thing was a complete fallacy. I wouldn't go that far myself, but while it may occur rarely in the wild this certainly is not its normal behaviour.
I wonder how much of the behaviour we find referred to in the literature (popular and otherwise) as if it is typical is actually based on single unusual examples or even on misunderstandings.
Thanks for your post, it was a wonderful diversion during my lunch break at work. :)
Very odd indeed. Does the Huia have a very long "speared" tongue for grabbing bugs once the substrate is sufficiently pried open?
I am curious to know if anyone else notes that the body bill of the Huia up there is longer in the mandible than in the upper rostrum, while the rhamphotheca is nearly the same length, meaning that the upper beak is extended more from the bone than in the mandible. This may have some implications in reconstructing jaw shape and rhamphothecal anatomy in fossil birds and pterosaurs, which also seem to sport variant jaw lengths but are reconstructed with identically elongated rhamphothecae.
Thanks for comments.
Jerzy says: could bill dimorphism result from male-male competion? This was the focus of Moorehouse's paper (cited above). 'Because sexual selection acts predominantly on males, it cannot readily explain [pronounced sexual bill dimorphism] in a non-polyandrous species. Greater female divergence in foraging-related anatomy in a species in which males are the larger (and therefore presumably socially dominant) sex is, however, consistent with the hypothesis that sexual dimorphism can be an adaptation to reduce intersexual competition for food' (Moorhouse 1996, p. 19). Anyway, in the case of the Huia the male's bill resembles the inferred primitive condition more than does the female's, so male specialisation for intraspecific combat does not explain the dimorphism well.
Nathan's prediction: well, this works in some cases (like Huia and Purple-throated carib), but not all (woodpeckers, woodhoopoes, Saw-billed hermit).
Mark asked about the origin of the 'co-operative feeding' idea. For this you need to see Jamieson & Spencer (1996): I tried sending you a pdf but it bounced back. The 'co-operative feeding' idea does indeed originate with Buller (he published the same information both in his 1888 book and in an 1871 note), but he himself objected when other authors took his comments to imply food sharing between the pair. Jamieson & Spencer (1996) noted that, actually, 'the female may have occasionally derived some benefit from the male's chiselling, but the reason for the Huia being found most regularly in pairs was probably not for mutual assistance in foraging, as is often interpreted from Buller's work, but for reasons dealing with social or sexual interactions'. They concluded that 'there is no firm evidence that indicates that male and female Huia assisted each other in extracting grubs from wood, although Buller's original comment (and one by J. M. Wright, quoted in Oliver (1955: 518)) are suggestive' (p. 16).
Zach: the Huia's tongue was narrow and tapered to a slightly 'frayed' tip, and there were a few long papillae at the tongue's base (it wasn't sexually dimorphic). But they wouldn't have speared prey with the tongue: after enlarging whatever cavity the bird was exploring, it would then have had more space to move the bill tips around and to thereby grab and extract an object. You'll have to watch extant gape-feeders (like starlings and icterids) to see what I mean, I hope this makes sense.
Jaime: you're right - the female's mandible is longer than her upper jaw in the figure shown here. However, this is not clearly the case in another female Huia skull (with lower jaw) that Burton figures, and I don't think it's consistent across individuals.
One question. Bill morphology is very susceptible to wear, so which causes which? - do the sexes behave differently because they have different bills or are the bills different because the sexes differ in behaviour? - As woodhoopoes at least are hole nesters and in many bird species the female does a lot of nest site preparation I would suspect that the females bill would wear down more from pecking at rotten wood, which would account for at least some of the size difference
With sexual dimorphism rampant among birds, it makes sense that beaks are also dimorphic. With so many other genes being selectively activated and deactivated, beak dimorphism would seem more common than it is. I think the wrong question is still being asked, we should look at the cause of dimorphisms such as this in other species to see if a link between other traits and bill length/shape. This could shed light on why bill dimorphism is so minimal in a class of organisms with such widespread dimorphism.
Birds are more than famous for their showy secondary sex characteristics. I'm not surprised that beak differences are just as common as plumage differences.
This was a fun read.
Could this have to do with rearing young? When limited in foraging by a nest, being able to bring food back from 2 different niches seems a working strategy. Island examples might connect more to reduced competition in the "added" niche.