One of my long-running plans on Tet Zoo has been to review passerine phylogeny. After decades of people saying that oscine passerines are (except larks and corvids) far too alike for anyone to construct a sensible phylogeny, a flurry of (mostly molecular) studies have meant that – as I like to say – the passerine tree is finally coming together. Alas, I’m nowhere near able to review current hypotheses of passerine evolution in depth (and didn’t I say something recently about not starting any new major Tet Zoo projects?).
Well done to those of you who correctly identified the ‘mystery’ bird as an Asian black bulbul or Himalayan black bulbul Hypsipetes leucocephalus; more specifically, as a white-headed example of the nominate form H. l. leucocephalus. This individual was photographed in captivity here in England: wild ones occur from eastern Afghanistan through northern Pakistan and India to southern China, and also in parts of Myanmar, Laos and Thailand. It’s somewhat ironic that a bird known as the ‘Black’ bulbul can have a strikingly white head and breast, and indeed most populations and species within the species complex that includes H. l. leucocephalus are mostly greyish, dark-headed birds [photo below - by J. M. Garg, from wikipedia - shows a properly dark-headed H. l. psaroides, photographed in Himachal Pradesh, India].
I said that there was, potentially, a lot to say about this species. Some of you suggested that the bird might instead be H. madagascariensis. If we’re being as specific as possible then that’s wrong, but it’s not entirely wrong, since the two have been regarded as part of the same species by some authors (see the historical review in Dickinson & Dekker 2002). There is in fact a whole complex of white-headed and dark-headed bulbuls of this sort (occurring in Madagascar, the Mascarenes, southern India and Sri Lanka); authors have differed whether they regard these as many distinct species, or as subspecies and/or intermediates of just one or a few species.
Warren et al. (2005) examined the phylogeny and biogeography of these confusing birds, using mtDNA from 32 individuals. Because H. philippinus from the Philippines was the sister-taxon to all the other taxa and because Asian birds long referred to as ‘H. madagascariensis‘ were also recovered as ‘basal’ in the tree, it seems that these bulbuls originated in Asia and then spread across the western Indian Ocean, apparently some time between the Late Pliocene and Middle Pleistocene (Warren et al. 2005). A more recent expansion of H. madagascariensis from out of Madagascar apparently led to the colonisation of Aldabra and the Comoros [this discussion treats H. philippinus as a species of Hypsipetes, but it probably warrants placement in another clade... read on].
As is so often the case, the molecular lineages identified by Warren et al. (2005) didn’t match with the species conventionally identified on the basis of morphology. The old, Asian ‘H. madagascariensis‘ population was substantially removed from ‘true’ H. madagascariensis of Madagascar, for example, while populations of both the Comoro black bulbul H. parvirostris and Philippine bulbul H. philippinus were non-monophyletic (Warren et al. 2005). Also interesting is that the relatively large, greenish Hypsipetes species found on various Indian Ocean islands were not close relatives (as usually thought), but represented convergently similar, independently evolved descendants of small, grey species. [A little bit of Asiatic/Indian Ocean bulbul variation is depicted in the image below... ignore the Hypocolius].
The fact that these Indian Ocean bulbuls came from continental Asia mirrors the colonisation history of at least a few other Indian Ocean birds, squamates and other animals, including owls, magpie-robins, and the group of pigeons that includes dodos and solitaires. Once upon a time, it was thought that just about all of the animals of the Mascarenes came from India or south-east Asia, but we now know that many groups also invaded from Africa, including sunbirds, kestrels and mabuya skinks. While the phylogeny of Indian Ocean bulbuls indicates that they colonised the big islands first, note that this isn’t necessarily what happened to all the groups that invaded the region: fruit bats, for example, seem to have colonised the small, remote islands first.
And also worth noting – in part because, again, it’s kind of contrary to ‘tradition’ – is that weird little island endemics can sometimes invade continents and produce continental radiations (Filardi & Moyle 2005). This notion of ‘upstream’ colonisation is contrary to the better known idea whereby continental colonists move ‘downstream’ across ocean archipelagos.
All-inclusive Hypsipetes vs smaller Hypsipetes, and separate Ixos, Microscelis, Iole, Hemixos and Tricholestes
As hinted at from this little discussion, the species included within Hypsipetes are variable in size and looks. There are mostly light species, mostly dark species, crested ones, crestless ones, and small ones and large ones. Depending on how you have your genericometer is calibrated, these could easily be subsumed within the one ‘genus’ ooor they could best be split up into at least five different ‘genera’. And, surprise surprise, over the years a large number of different generic names have been created for the different species: the result being that, if Hypsipetes sensu lato should be shot to pieces, there are already names associated with the different fragments.
Indeed, noting that “The issue of the correct generic names for the species within this complex has, apparently, been long avoided by those who have had to deal with it”, Gregory (2000, p. 164) brought attention to the generic names that are available for the different subdivisions of Hypsipetes sensu lato. Among these, the name Hypsipetes Vigors, 1831 itself has to go with H. psaroides, a junior synonym of H. leucocephalus. Then there’s Ixos Temminck, 1825, which has to go with the Sumatran bulbul Ix. virescens and similar species (and which, you’ll note, pre-dates Hypsipetes!*), Microscelis Gray, 1840, which has to go with the Brown-eared bulbul M. amaurotis [shown here, from wikipedia] and similar species, Iole Blyth, 1844, which has to go with the Buff-vented bulbul I. olivacea and similar species, Hemixos Blyth, 1845, which has to go with the Ashy bulbul H. flavala and similar species, and Tricholestes Salvadori, 1874, the type species of which is the Hairy-backed bulbul T. criniger. There are several other available names too. Some ornithologists have been using at least some of these names for a while as they feel that the constituent taxa look ‘different enough’ to warrant separation from Hypsipetes sensu stricto. As we’ll see, phylogenetic studies might lend support to the idea that Hypsipetes sensu lato should be split up, and hence that these names should come back into general use. The composite image below shows (left to right) Buff-vented bulbul Iole olivacea [photo by Lip Kee Yap, from wikipedia], Chestnut bulbul Hemixos castanonotus [photo by Charles Lam, from wikipedia], and Mountain bulbul Ixos mcclellandii [photo from wikipedia].
* See Dickinson & Gregory (2002) for a discussion of the nomenclatural history of Ixos. It was long ignored as a potential senior synonym of Hypsipetes because its type species was (wrongly) thought to be Turdus phoenicopterus Temminck, 1821, the bird now known as Campephaga phoenicea (the Red-shouldered cuckoo-shrike). Now that Ixos is definitely associated with bulbuls, Pycnonotidae Gray, 1840 is a junior synonym of Ixodidae Bonaparte, 1838. Because this name is already widely used for a group of ticks, there were plans at one stage to get the new name Ixosidae used for bulbuls (Bock 1994). Dickinson & Gregory (2002) said of this matter that it seemed most sensible that “the status quo should be maintained and the family name Pycnonotidae retained” (p. 88), and this is far as things have gone. Thanks to Lars Dietz for bringing Dickinson & Gregory (2002) to my attention.
Bulbuls within the passerine tree
It is universally agreed that Hypsipetes is a bulbul – a member of the passerine group Pycnonotidae – though this, of course, doesn’t necessarily mean that it’s true. In the ‘traditional’ passerine classifications that tended to make it into both textbooks and the popular literature (that is, those of Gadow, Stresemann, Wetmore and Mayr), bulbuls were typically placed within an assemblage that also includes other robust-billed, mostly frugivorous passerines, like waxwings, leafbirds, orioles, cuckooshrikes and bowerbirds.
Sibley & Ahlquist (1990) were the first authors to propose that oscine passerines consisted of two major radiations: one including all crow-like forms (Corvida) and one including all sparrow/finch/warbler-like forms (Passerida). Passerida, in turn, consisted of three clades: Muscicapoidea, Sylvioidea and Passeroidea. I’ll be here all day if I start to elaborate on the content, membership and historical nomenclature of these groups, so I’ll stop there. We’re only interested for now in Sylvioidea: a group thought by Sibley & Ahlquist (1990) to include nuthatches, tits, tree-creepers, wrens, kinglets, bulbuls, leaf warblers, white-eyes and babblers. Nuthatches, treecreepers, wrens and gnatcatchers – grouped together as Certhioidea – may represent a distinct lineage closer to Muscicapoidea and Passeroidea (most likely Muscicapoidea) than to the remaining birds originally included in Sylvioidea, and tits (Paridae and Remizidae or Remizinae) seem to be a distinct lineage as well. The ‘remainders’ have indeed been recovered as a clade for which the name Sylvioidea has been co-opted (Alström et al. 2006).
Incidentally, one problem with the names that have been used for the major passerine clades is that explicit definitions have (to my knowledge) never been published. Ergo, when a certain group of workers recovers a particular clade, they then find themselves being uncertain as to which name it should have. Somebody really should work on this, hint hint. I’ll make things a little clearer here (perhaps) by saying that Sylvioidea should be all oscine passerines closer to the respective type species of Sylvia than to the respective type species of Muscicapa (representing the Muscicapoidea) and Passer (representing the Passeroidea). A substantially simplified phylogeny of Passerida is shown below [all images from wikipedia] (sorry it’s so small: I can only post images at a maximum width of 490 pixels).
Bulbuls among the sylvioids
In recent years, Sylvioidea has become famous for being fabulously confusing and poorly resolved, incorporating as it does the babblers, laughingthrushes, bulbuls, greenbuls, African warblers, white-eyes and so many others. Luckily, I don’t need to worry about the majority of those groups now. Within this massive clade, Alström et al. (2006) found bulbuls to be the sister-group to a sylvioid clade that included Hirundinidae (swallows and martins), Cettidae (bush warblers and kin), Aegithalidae (long-tailed tits) and Phylloscopidae (leaf warblers and kin). Larks (Alaudidae) were the sister-taxon to this ‘bulbuls + other sylvioids’ clade.
A few other positions for bulbuls have been recovered by other studies – Sefc et al. (2003), for example, found them to be the sister-group to swallows – but most workers have recovered a similar topology to Alström et al. (2006), though sometimes with less resolution (e.g., Johansson e al. 2008). Some taxa conventionally included within Pycnonotidae – namely the nicators, greenbuls and Madagascan endemics Oxylabes and Crossleyia – belong elsewhere within Sylvioidea (Cibois et al. 2001, Beresford et al. 2005, Johansson et al. 2008).
Sorting out the bulbuls
Where does Hypsipetes fit among bulbuls as a whole? A few phylogenetic studies devoted to the relationships and diversification of bulbuls have now been published. In a study mostly designed to test the phylogeny of the Criniger bulbuls of Asia and Africa (better known as the Asian bearded bulbuls), Pasquet et al. (2001) found Hypsipetes to be part of an ‘Asian clade’ that also included Pycnonotus and the Asian Criniger taxa (Pycnonotus isn’t exclusive to Asia, and invaded Africa at some point in its history). The African Criniger species belonged in an African clade together with Bleda, Phyllastrephus and other bulbuls, so Criniger was recovered as non-monophyletic.
And so was Hypsipetes (here I’m talking about Hypsipetes sensu lato), since three of its species formed a clade that was closer to the Asian bearded bulbuls than was a H. propinquus + H. criniger clade (Pasquet et al. 2001). Because the name Criniger Temmink, 1820 should remain associated with its type species (African C. barbatus), the Asian species previously included in the genus should be renamed: some authors have already done this, and have used Alophoixus Oates, 1889 (originally coined for ‘C.’ phaeocephalus, the Grey-headed bearded bulbul or Yellow-bellied bulbul [shown here: photo by Lip Kee Yap, from wikipedia]) for the Asian bearded bulbuls. This is what Pasquet et al. (2001) chose to do, though they did allude to the idea that Alophoixus should be used for phaeocephalus alone and that a new name should be created for the remaining Asian bearded bulbuls. There’s another idea that they didn’t mention: this being that all ‘Asian crinigers’ be sunk into the otherwise paraphyletic Hypsipetes. To my knowledge, this latter idea has never been seriously proposed.
Incidentally, note that two of the three or so polytypic genera included in that small study were found to be non-monophyletic: a common theme in phylogenetic studies of passerines. I don’t think it’s as widely realised as it should be that all too many polytypic ‘genera’ of tradition are artificial, non-monophyletic assemblages.
Results essential identical to those of Pasquet et al. (2001) were reported by Jønsson & Fjeldså (2006) but, then, their’s was a supertree study. Moyle & Marks (2006) produced a larger analysis incorporating a lot more species. They also found Hypsipetes sensu lato to form a clade with the Asian bearded bulbuls (the Hook-billed bulbul Setornis criniger was in there as well), and again recommended that the name Alophoixus be used for the Asian bearded bulbuls.
Most recently, Oliveros & Moyle (2010) included numerous Asian bulbuls within a much larger phylogeny and recovered a similar topology [a section of their phylogeny is shown below]. It has many implications for the species included Hypsipetes sensu lato. Here’s where we come back to all those generic synonyms mentioned earlier on. Oliveros & Moyle (2010) recovered a distinct structure within ‘Hypsipetes-group bulbuls’, and found many of the divergences within this clade to be equally as old as, or older than, the divergences present between many other of the Asian bulbul ‘genera’.
In order of divergence from older to youngest, they recovered clades that corresponded to Iole, Hemixos, Hypsipetes sensu stricto, Microscelis, and Ixos. Even this treatment doesn’t result in a totally tidy nomenclature, since the species conventionally included in Ixos didn’t form a clade. The Hairy-backed bulbul T. criniger – often included in Hypsipetes – wasn’t a part of the ‘Hypsipetes group’ at all, but was recovered as the sister-taxon to the clade that includes the Asian bearded bulbuls (those ‘Asian crinigers’) and all the ‘Hypsipetes-group bulbuls’ (Oliveros & Moyle 2010).
As usual, you could make the argument that we should stick to tradition and just lump all of the species concerned into one super-inclusive Hypsipetes genus and be done with it… but, to my mind, it seems more informative (and more interesting) to have the taxonomy reflect the phylogeny. None of these changes affect Hypsipetes leucocephalus – since it will be forever associated with the name Hypsipetes – but they do very much affect our view of Hypsipetes in the old, inclusive sense of the name. At last, Hypsipetes goes only with those confusing white- and dark-headed bulbuls like the white-headed Black bulbul that started this whole discussion.
If you made it though the whole of this article, you might now have a rough idea of bulbul phylogeny and diversity, but we’ve hardly touched on them at all really. At least I’ve started – at long last – to make one minor inroad into the terrifying, gargantuan nexus that is the world of passerine phylogeny. Much more one day.
For previous Tet Zoo articles on passerines see…
- Vampire finches and the path to parasitism
- Coccothraustes: most bizarre of finches
- An encounter with a crossbill
- Beasts of Portland: the location of wheatears, the spread of wall lizards, the scat of a lynx
- Lots of sunbirds have dumb names
- Sexual dimorphism in bird bills: commoner than we’d thought
- Ifrita the poisonous passerine
- Pseudopodoces, the corvid that wasn’t
- From Morocco, with larks, babblers, gazelles, owls and GIANT DINOSAUR BONES
- Goodbye Bulo Burti boubou (sort of)
- Passerine birds fight dirty, a la Velociraptor
- Dead baby birds: why here, why now?
- Great tits: murderous rapacious flesh-rending predators!
- Redstarts: good
Refs – -
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Beresford, P., Barker, F. K., Ryan, P. G. & Crowe, T. M. 2005. African endemics span the tree of songbirds (Passeri): molecular systematics of several evolutionary ‘enigmas’. Proceedings of the Royal Society of London B 272, 849-858.
Bock, W. J. 1994. History and nomenclature of avian family-group names. Bulletin of the American Museum of Natural History 222, 1-281.
Cibois, A., Slikas, B., Schulenberg, T. S. & Pasquet, E. 2001. An endemic radiation of Malagasy songbirds is revealed by mitochondrial DNA sequence data. Evolution 55, 1198-1206.
Dickinson, E. C. & Dekker, R. W. R. J. 2002. Systematic notes on Asian birds. 25. A preliminary review of the Pycnonotidae. Zoologische Verhandelingen Uitgegeven door het Rijksmuseum van Natuurlijke Historie te Leiden 340, 93-114.
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Jonsson, K., & Fjeldsa, J. (2006). A phylogenetic supertree of oscine passerine birds (Aves: Passeri) Zoologica Scripta, 35 (2), 149-186 DOI: 10.1111/j.1463-6409.2006.00221.x
Moyle, R. G. & Marks, B. D. 2006. Phylogenetic relationships of the bulbuls (Aves: Pycnonotidae) based on mitochondrial and nuclear DNA sequence data. Molecular Phylogenetics and Evolution 40, 687-695.
Oliveros, C. H. & Moyle, R. G. 2010. Origin and diversification of Philippine bulbuls. Molecular Phylogenetics and Evolution 54, 822-832.
Pasquet, É., Han, L.-X., Khobkhet, O. & Cibois, A. 2001. Towards a molecular systematics of the genus Criniger, and a preliminary phylogeny of the bulbuls (Aves, Passeriformes, Pycnonotidae). Zoosystema 23, 857-863.
Sefc, K. M., Payne, R. B. & Sorenson, M. D. 2003. Phylogenetic relationships of African sunbird-like warblers: Moho (Hypergerus atriceps), Green hylia (Hylia prasina) and Tit-hylia (Pholidornis rushiae). Ostrich 74, 8-17.
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