The curious case of the Red-bellied Spinipig

NB: The following should be prefaced - in the manner of any modern climate debate - with “…I’m not a taxonomic scientist, BUT…”

The July release of the “Illustrated Checklist of the Birds of the World. Volume 1: Non-passerines” (del Hoyo & Collar, Lynx Edicions/BirdLife) [1] marks the start of the brave new era in which BirdLife International team up with the Handbook of the Birds of the World (HBW) crew on the impressively ambitious, if slightly mad, project to review and illustrate the entirety of the world’s avifauna in two volumes. Since BirdLife Australia will adopt these changes by default, unfortunately this means Australia’s ‘official’ bird list is, yet again (groan), being decided by A BOOK. And in this case, a book extraordinarily revising all the species of the world on the premise of a single scientific paper, Tobias et al’s 2010 paper, “Quantitative limits for species delimitation” [2] [available open access here]. The Tobias paper outlines a hitherto untested numerical scoring method for defining whether a pair of related taxa are ‘distinct enough’ to qualify as separate species. The method uses sympatric (co-existing, hence undisputed) species pairs to calibrate a universal threshold, which can then be used to test allopatric (geographically separated) pairs, which can be much harder to define. The answer, it turns out, is 7.* 

In a rather left-field move, HBW/BirdlLife have thus resplit the Pilbara’s “Rufous-bellied Spinifex Pigeon” (or spinipig as the locals call them) Geophaps ferruginea, which compared to nominate plumifera (now White-bellied Spinifex Pigeon), is:

• generally redder [ferruginea = rusty]
• entirely red-brown below, lacking a white belly
• richer red-brown above (plumifera more grey-brown)
• only a grey and black pectoral band, i.e. lacks white band
• slightly smaller
• plume slightly shorter [3]
• iris red to orange-red (cf. yellow to orange-yellow) [4]

"Red-bellied" Spinifex Pigeon Geophaps [plumifera] ferruginea, Wickham WA. Note the red (not grey-brown) back.

The White-bellied form also has a southern/central subspecies leucogaster (larger; slightly redder (but variable) upper parts; belly with limited white i.e. more light brown). This form just extends into WA with an isolated population in the Rawlinson Ranges, which is reddish like ferruginea and with only limited white on the belly [4]. Nearby NT birds from the Petermann Ranges are also apparently intermediate between ferruginea and leucogaster [5].

The intergrade
The big problem is that the Red- and White-bellied forms abut in the southwest Kimberley, across two transitional forms originally named as subspecies, but dismissed as introgressed hybrids in HANZAB [6]:

• ’mungi’  - (Derby region, Grant & Edgar Ranges) - like ferruginea but pale; pink-buff breast; smaller. Interestingly a similar but unnamed pale form occurs in an isolated population in the Cape Range near Exmouth [4]. 
• ‘proxima’ -  like plumifera but redder upper parts like mungi; “very reduced” white breastband; variable white on belly (some like plumifera, some with a small white patch only). An example of ‘proxima’ from Mornington Station with reddish back and mottled belly can be seen on Rohan Clarke’s image collection.

Approximate distribution of Spinifex Pigeon taxa, with schematic representation of plumage. Race 'mungi' was included by HBW/BirdLife within ferruginea. The Cape Range population is unnamed but described by Johnstone & Storr as similar to 'mungi'. Dots represent records from Atlas of Living Australia (ala.org.au), which includes Birds Australia Atlas and state Museum records. Arrows indicate presumed past expansion of ferruginea.

Here’s what none other than Ernst Mayr, yes the man who invented the Biological Species Concept (and named proxima), had to say about this overlap (1951) [7]:

"...new subspecies proxima is not very striking. The reason it is included is to call attention to the fact that together with mungi it forms such a nice bridge between ferruginea and plumifera. The intergradation between the forms is perfect so far as the upper parts are concerned. There is however no sign of intergradation of the underparts". 

However HANZAB contradict even this on the underparts, in that birds at Fitzroy Crossing [=‘proxima’] “vary considerably" and some have very little white.

'Red-bellied' Spinifex Pigeons, Cossack WA. Note the entirely reddish belly and absence of white in the breastband.

So is it a species?
Well here’s what a few past authorities have concluded:

• Mayr 1951 [7]: “my studies indicate… the two are conspecific”… “In the west Kimberley the rufous-bellied and white-bellied populations agree in every character except the colour of the belly. The colour of the belly varies geographically (or even individually) in many species of birds and is not necessarily a species character.”
• Serventy & Whittell 1976 [3]: “…the habits of the two species are virtually identical … there is a case for placing all forms…as geographical representatives of one variable species”
• WA Museum taxonomists Johnstone & Storr [4]: “...considerable geographic variation within this species with white-bellied, red-bellied, and intermediate populations, making it difficult to recognise subspecies”
• HANZAB [6]: “...Introgression or hybridisation recorded at edges … appear to be recently isolated … much variation appears to be clinal”

Crome et al. (1980) [5] completed a very thorough study into geographical variation, including multi-character Principal Component Analysis and even captive breeding experiments out to F2 hybrids. They found that even beyond the obvious ‘proxima’ hybrid zone (which matched their F1 hybrids), whiteness of belly, redness of upperparts, and broadness of pectoral band continued to vary in a gradual cline from east to west. Birds from the Petermann Range (i.e. western extremities of leucogaster) approached western brown-bellied birds very closely in colour, but could be discriminated on size. They suggested ‘mungi’ and ‘proxima’ were not subspecies but enclaves of progressively introgressed ferruginea x plumifera hybrids left behind during past Pleistocene expansion, and that a similar contact zone in the south (i.e. with leucogaster) had since been extinguished by aridity of the Gibson Desert. So though one should never assume process from pattern, the situation in the Kimberley looks like the classic story of past allopatric divergence, followed by expansion, secondary contact and hybridisation, followed by introgression on each side (i.e. pale-bellied genes into ‘mungi’, reddish genes into ‘proxima’) creating what is sometimes called a ‘hybrid swarm’, and is now some way down the path of blending to a smooth cline. 

Spinifex Pigeon subspecies leucogaster, King's Canyon NT. Note the extensively buffy belly and narrow breastband. Photograph: Creative Commons Graham Winterflood

There are many examples in the literature of birds being originally (100+ years ago) diagnosed as species, then being relegated to subspecies after hybridisation was discovered. Modern species definitions are a little softer on hybridisation, as narrow hybrid zones between parapatric taxa are now regarded as evidence of an intrinsic barrier to gene flow. But at what point does an introgressed hybrid zone become a cline? Under the Helbig et al. [8] definitions used by the BOU this is quite clear: taxa joined by a distinct hybrid zone containing individuals of pure phenotypes plus first-generation hybrids and backcrosses may be termed ‘semispecies’. But: 

“…populations at opposite ends of a cline, even if they are fully diagnosable, should not be ranked as separate species, as gene flow is limited only through isolation by distance, not as a result of an intrinsic barrier. Diagnosable populations joined by a cline may be treated as subspecies …" [8]

One might suggest that if you need to resurrect not one but two long-synonymised ‘races’ of intermediate forms in order to define your ‘hybrid zone’, it’s looking a bit dodgy.

Herein lies the problem with the Tobias/HBW/BirdLife approach. It is clearly not enough to just pronounce that two taxa seem different enough to be species, therefore they are species - even if this diagnosis is made using a semiquantitative method. The Red-Bellied Spinipig seems dodgy by most modern species concepts. It certainly fails the classic Biological Species Concept (i.e. reproductive isolation), since these populations have formed persistent (thus fit and fertile) hybrid populations at some recent point after their initial differentiation, and can demonstrably interbreed today. It fails the Phylogenetic Species Concept on diagnosability grounds, because how can sensibly draw an arbitrary line between the ‘mungi’ / ‘proxima’ populations and assign birds on each side to two different species? It fails the Monophyletic Species Concept because of the obvious and extensive past gene exchange. It even looks dodgy on the old Morphological Species Concept (which in the absence of song or behavioural differences, is basically what Tobias boils down to here) since the split hinges on a few highly-correlated plumage characters (white breast band and belly feathers) against a background of extensive clinal and probably also ecophenotypic variation.

'Red-bellied' Spinifex Pigeon, Karratha WA, with its three favourite things: red rocks, spinifex, and nearby water.

________________________________________________

Other ’Tobias-species’ splits for WA

In other news, the Tobias/BirdLife/HBW revision has delivered two other non-passerine splits/re-splits for WA**, which both seem solider than the pigeon, though are yet to be tested genetically:

Black-shouldered Lapwing  Vanellus [miles] novaehollandiae
Most Aussies would know this form as the ‘Spur-winged Plover’ but a similar name is already taken by a central African lapwing. It has naturally colonised southwest WA, though in very small numbers. Compared to nominate miles:

• black cap extends down back of neck and down sides of upperbreast ‘lapels’
• less extensive yellow face mask which does not extend over and behind eye
• pendant wattle does not dangle as far below bill
• prominent yellow bony spurs on the carpus
• slightly larger (wing and tail)
• shorter bill
• different call according to some reports

These forms also hybridise to produce intermediate-looking offspring, particularly around the Lake Eyre region. But given the large area of potential contact, hybridisation is surprisingly limited, and is probably partly due to recent expansion from our human love of grass. Some past discussions on birding-aus [9] suggest that hybridisation in the supposed contact zone in southern Queensland is limited, and in other areas may have been exaggerated by intentional oversampling of hybrids. So this may well be a good species deserving of further study, subject to genetic assessment of gene flow.

Black-shouldered (Masked) Lapwing Vanellus [miles] novaehollandiae near Byron Bay, northern NSW

Australian Gull-billed Tern Gelochelidon [nilotica] macrotarsa
Two forms of Gull-Billed Tern occur in Australia, this locally-breeding form and a smaller migratory form visiting the northern coast during September-April, tentatively pigeon-holed as subspecies affinis. Compared to local macrotarsa, migratory ‘affinis’ are [10]:

• obviously smaller
• shorter legged (‘macrotarsa’ = 'long legs')
• darker grey upperparts, resulting in contrast with white upper tail coverts
• straighter bill, not decurved
• in non-breeding plumage (i.e. while in Australia) have a white crown with only small irregular black patches around the eye and ear (cf. large oval black patch of macrotarsa)
• more defined moult pattern, breeding plumage only likely in Australia from March-May (cf. macrotarsa, moult & timing of breeding plumage highly variable)
• strictly coastal, not on inland wetlands and grasslands

To quote Rogers et al [10] who studied these differences in some detail, “…these substantial differences … suggest that macrotarsa been isolated for a long time. A comprehensive genetic analysis ... is overdue”.

Australian Gull-billed Tern Gelochelidon [nilotica] macrotarsa at Forrestdale Lake south of Perth, January 2009. Note the non-breeding plumage with large oval eyepatch; Asian Gull-billeds in NBP show only a small black spot in front of and behind the eye, separated by a white 'eyelid' below the eye.

Australian Gull-billed Tern Gelochelidon [nilotica] macrotarsa at Lake Cooloongup south of Perth. This photograph was taken in late November; macrotarsa may be found in breeding plumage at any time of year, while Asian Gull-billeds are unlikely to be seen in breeding plumage outside of April-early May. 

Footnotes:
* If I had written the Tobias paper I would have made sure the magic species threshold scored out at 42.
** HBW/BirdLife have also split the Tasmanian Boobook.

A review of the new HBW can be found here: http://www.lynxeds.com/sites/default/files/reviews/World-Birdwatch-Ringing-in-the-changes-HBW-Alive-June-2014.pdf

References:
[1] del Hoyo J, Collar, NJ, Christie DA, Elliott A, Fishpool LDC (2014). HBW and BirdLife International Illustrated Checklist of the Birds of the World. Volume 1: Non-passerines. Barcelona and Cambridge UK, Lynx Edicions and BirdLife International.
[2] Tobias JA, Seddon N, Spottiswoode CN, Pilgrim JD, Fishpool LDC, Collar NJ (2010). Quantitaive criteria for species delimitation. Ibis 152: 742-746
[3] Serventy DL & Whittell HM (1976). Birds of Western Australia. Perth: University of Western Australia Press.
[4] Johnstone RE and Storr GM (1998-2004). Handbook of Western Australian birds (2 vols). Perth, Western Australian Museum.
[5] Crome FHJ, Carpenter SM, Frith HJ (1980). Geographic variation and taxonomy of the Spinifex Pigeon Geophaps plumifera. Aust J Zool 28: 135-150
[6] Marchant S. & Higgins PJ, et al. (eds) (1990-2006). Handbook of Australian, New Zealand and Antarctic Birds. (7 vols). Oxford University Press, Melbourne.
[7] Mayr E (1951). Notes on some pigeons and parrots from Western Australia. Emu 51: 137-145.
[8] Helbig AJ, Knox AG, Parkin DT, Sangster G, Collinson M (2002). Guidelines for assigning species rank. Ibis 144: 518-525
[9] Discussions on birdnig-aus c. June 2012
http://bioacoustics.cse.unsw.edu.au/archives/html/birding-aus/2012-06/threads.html#00154
http://bioacoustics.cse.unsw.edu.au/archives/html/birding-aus/2012-06/msg00156.html
[9] Rogers DI, Collins P, Jessop RE, Minton CE, Hassell CJ (2005). Gull-Billed Terns in north-western Australia: subspecies identification, moults and behavioural notes. Emu 105: 145-158