Tetrapod Zoology

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Several weeks ago, I and a group of colleagues from the University of Portsmouth (Dave Martill, Robert Loveridge and Richard Hing) set off on a trip to the Cretaceous exposures of Morocco. We were to be joined by Nizar Ibrahim from University College Dublin – our team leader – and by Samir Zouhri and Lahssen Baidder from the University of Casablanca. Our primary aim was to discover Cretaceous dinosaurs, pterosaurs and other fossil reptiles, but we were also interested in studying the region’s geology, and to learn about the sedimentology, palaeoenvironment and taphonomic setting of the rocks that yielded the animals, particularly those of the famous Kem Kem Formation, source of Deltadromeus and Carcharodontosaurus. Morocco is an amazing country, and we experienced most of its extremes, from deep snow and blizzards in the Atlas Mountains to the aridity, heat and immense sand dunes of the Sahara. We experienced a day of sandstorms, crossed several rivers in flood, and saw the desert come to life after rain. The nights were usually clear and cold. Everywhere we went we were treated to the tremendous hospitality of the Moroccan people, whether they lived in the big, bustling cities likes Marrakesh or Casablanca, or in the small, rural villages in the south.

For me (and for some other members of the team, particularly Richard), this was also the chance to see a lot of amazing African wildlife for the first time. I’m pleased to report that we had the most extraordinary luck, eventually seeing most (though not all) of the creatures I hoped we might. If you’re reading this article (and those that will follow) in the hope of hearing loads of stuff about rebbachisaurs, noasaurs and carcharodontosaurs, you’re going to be somewhat disappointed I’m afraid. If you like passerines and waders however: woo-hoo, jackpot! Unless stated otherwise, the photos were taken by Bob – thanks Bob…

Distracted by Cyanopica

Before getting to Morocco, we drove through France and Spain. In Spain we stopped to watch Griffon vultures Gyps fulvus and Spotless starlings Sturnus unicolor and we also drove through areas where Azure-winged magpies were abundant. I cannot help but get a feeling of disbelief and wonder where a creature that I’ve always regarded as exotic and almost semi-mythical is suddenly commonplace and easy to see. Cyanopica is a very cool bird. Its disjunct distribution (Iberian Peninsula and eastern Asia, and nowhere in between) once resulted in the idea that it had been introduced to Iberia by Spanish or Portugese sailors during the 16th century, but genetic data and fossils (from Gibraltar) have shown that its modern distribution is relictual and that the populations have been separated for over a million years (Cooper & Voous 1999, Cooper 2000, Fok et al. 2002) [image below from wikipedia].

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In fact morphological and genetic data indicate that the Iberian and Asian groups can be treated as distinct species: C. cyanus Pallas, 1776 is the Asian one and the Iberian one has to be called C. cooki Bonaparte, 1850 (Fok et al. 2002, Kryukov et al. 2004). In Asia, there are indications that Azure-winged magpies are able to quickly expand their range and to colonise new areas when conditions are right: this provides indirect support for the hypothesis that, during the Pleistocene at least, they were clearly so adaptable and mobile that they were able to colonise the entire breadth of Eurasia. But if this is so, why hasn’t the European population gotten out of Iberia? Humans may be the answer: because Spanish farmers regard it as an agricultural pest, it has suffered from a long history of persecution (there is a tradition of destroying its nests), and this may have prevented eastwards expansion (Kryukov et al. 2004). Incidentally, the position of Cyanopica within Corvidae is kind of controversial: Ericson et al. (2005) found it to group weakly with the Perisoreus jays and to be near the base of a major clade that includes Old World ‘core corvids’ and New World jays. That rules out any close relationship with magpies proper, and also with the Asian magpies and treepies.

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Anyway, back to the trip… after crossing the Strait of Gibraltar and staying overnight in Ceuta (a Spanish city located in north Africa) we were in Morocco proper, and almost immediately were treated to excellent views of White storks Ciconia ciconia and Cattle egrets Bubulcus ibis [shown here, image © Bob Loveridge]. I counted over 40 storks at a rubbish dump. Egrets were also hanging out at the dumps, as well as in any field with livestock. Little egrets Egretta garzetta were commonplace too, and it was easy to distinguish them from the far stockier, paler-billed Cattle egrets (or, it was for me anyway). Here in England, Little egrets are now common birds that don’t deserve a second glance: they first bred here in 1996 (at Brownsea Island, Dorset) and in a 2003 survey more than 400 birds were counted at a single site (this was in Essex). Cattle egrets now seem to be doing the same thing. A load came over to southern England in 2007, and in 2008 they were reported breeding here for the first time (this was in Somerset). The Cattle egret is already probably the world’s most widely distributed bird, having colonised all seven continents* from an African centre of origin.

* Yes, I said all seven: the Antarctic records are from the South Orkney, South Shetland and Argentine islands. White storks at a rubbish dump shown below [image © Bob Loveridge].

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Also abundant and easy to spot were members of the highly distinctive African magpie subspecies Pica pica mauretanica. Its blue eye-ring is not really obvious at any distance, but it also differs from other Old World magpies in having less white on the wing and a tail that isn’t iridescent green. Indeed it’s distinct enough from other Old World magpies for some people to suggest that it should be regarded as a proper species, the so-called Maghreb magpie P. mauritanica.

Gulls, terns and waders

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With a bit of time to kill – and keen to experience some of the region’s wildlife – Dave, Bob, Richard and I visited one of the wetland regions in the north-east of the country (I failed to record the name of the exact place we visited: it was possibly Lac de Sidi Bourhaba). A local guide took us out on his boat and knew exactly where to take us to see all the local specialities: his identifications were generally excellent but sometimes off. Anyway, it proved pretty incredible, with multiple new species for all of us. Among the first birds we looked at were the gulls. Among a mixed group of Lesser black-back Larus fuscus (or is it L. graellsii?) and Yellow-legged gull L. cachinnans (or is that L. michahellis?) were several Audouin’s gull Ichthyaetus audouinii, one of the rarest gulls in the world: it’s restricted entirely to the Mediterranean region [Audouin's gulls at front of image shown at top, © Bob Loveridge]. Once you know what to look for, this species is highly distinctive, with dark eyes and bill, grey-green legs and a more elegant look than white-headed gulls. Slender-billed gulls Chroicocephalus genei were also present, though at times quite difficult to distinguish from winter-plumaged Black-headed gull C. ridibundus [Black-headed gull shown at bottom of adjacent image, © Bob Loveridge]. Seeing Slender-billed gulls and Audouin’s gull in the same place was interesting, as one of my childhood memories from bird books was the inference that Audouin’s might be an evolutionary intermediate between the Slender-billed gull and white-headed gulls like the Herring gull. Alas, this never stood the test of time, and the two are about as far apart as they could possibly be in modern phylogenies (Pons et al. 2005). Black-headed and Mediterranean gull C. melanocephalus stood obligingly together.

Caspian terns Hydroprogne caspia flew overhead [one is shown in the second image down in adjacent composite, © Bob Loveridge] and Sandwich terns Thalasseus sandvicensis [shown in third image down, © Bob Loveridge] were present on a sandbar (the taxonomy I’ve used for terns follows that suggested by Bridge et al. (2005)). We then moved on to the mudflats where Grey plovers Pluvialis squatarola, Ruddy turnstones Arenaria interpres and Ringed plovers Charadrius hiaticula were fairly abundant. This region is apparently the only place in the western Palaearctic where sightings of the extremely rare Slender-billed curlew Numenius tenuirostris can be essentially guaranteed, but we didn’t have time to look around the whole area and didn’t get to see any. One book on bird-watching in Morocco states that local guides often point to long-billed waders and identify them as Slender-billed curlews when they are in fact something else. Indeed our own guide did exactly this, claiming that what was clearly a Bar-tailed godwit Limosa lapponica was a curlew. I don’t think this is deliberate deception as he didn’t have the advantage of binoculars! We did see Greenshank Tringa nebularia [image below, © Bob Loveridge], Redshank T. totanus, Little stint Calidris minuta and Greater flamingo Phoenicopterus ruber. I discovered that I struggle to distinguish Kentish plover Charadrius alexandrinus from Ringed plover when the latter is in winter plumage. Marsh owls Asio capensis were also in the area but we didn’t have time to see them. We would have encounters with other owls later on however.

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After visiting Casablanca and meeting up with Nizar, we drove to Marrakesh. A weird sounding, noisy bird in a street tree turned out to be a Common bulbul Pycnonotus barbatus, the first I’d seen. Bulbuls (pycnonotids) are strange birds, at least if you’re European and not from Africa or Asia. With robust bills and (usually) hair-like filo-plumes on the nape, they’re short-winged frugivores of forests and scrublands. They seem to be sylvioid passeridans closely related to babblers and to a huge assortment of mostly warbler-like African passerines, though the long-tailed tits, bushtits and swallows are apparently part of the same major clade. Incidentally, bulbuls are able to eat large quantities of wax (Horne & Short 1990).

More next: Atlas birds and desert tetrapods…

Refs – –

Bridge, E. S., Jones, A. W. & Baker, A. J. 2005. A phylogenetic framework for the terns (Sternini) inferred from mtDNA sequences: implications for taxonomy and plumage evolution. Molecular Phylogenetics and Evolution 35,459-469.

Cooper, J. H. 2000. First fossil record of Azure-winged magpie Cyanopica cyanus in Europe. Ibis 142, 150-151.

– . & Voous, K. H. 1999. Iberian Azure-winged magpies come in from the cold. British Birds 92, 659-665.

Ericson, P. G. P., Jansén, A.-L., Johansson, U. S. & Ekman, J. 2005. Inter-generic relationships of the crows, jays, magpies and related groups (Aves: Corvidae) based on nucleotide sequence data. Journal of Avian Biology 36, 222-234.

Fok, K. W., Wade, C. M. & Parkin, D. T. 2002. Inferring the phylogeny of disjunct populations of the azure-winged magpie Cyanopica cyanus from mitochondrial control region sequences. Proceedings of the Royal Society of London B 269, 1671-1679.

Horne, J. F. M. & Short, L. L. 1990. Wax-eating by African common bulbuls. Wilson Bulletin 102, 339-341.

Kryukov, A., Iwasa, M. A., Kakizawa, R., Suzuki, H., Pinsker, W. & Haring, E. 2004. Synchronic east-west divergence in azure-winged magpies (Cyanopica cyanus) and magpies (Pica pica). Journal of Zoological Systematics & Evolutionary Research 42, 342-351.

Pons, J.-M., Hassanin, A., & Crochet, P.-A. 2005. Phylogenetic relationships within the Laridae (Charadriiformes: Aves) inferred from mitochondrial markers. Molecular Phylogenetics and Evolution 37, 686-699.

Comments

  1. #1 Hai~Ren
    December 19, 2008

    Looks like you really had a great time, looking at both extinct and extant creatures.

    Bulbuls are familiar to my part of the world, and can be seen quite often in gardens and parks, or as pets.

  2. #2 Sven DiMilo
    December 19, 2008

    Herps, please! Tortoises? Uromastyx?

  3. #3 Jerzy
    December 19, 2008

    At last some interesting creatures! ;-)

    Isnt it surprising that azure-winged magpie didnt spread to North Africa, nor bulbul and tchagra didnt move north to Iberian peninsula?

    Slender-billed curlew was last seen in Morocco sometime in 1990s, so you didnt really miss it.

  4. #4 Simon M. Clabby
    December 19, 2008

    Never mind the birds, what about the arboreal goats?

  5. #5 neil
    December 19, 2008

    I cannot help but get a feeling of disbelief and wonder where a creature that I’ve always regarded as exotic and almost semi-mythical is suddenly commonplace and easy to see.

    I’ve had the exact same experience with these corvids. My first encounter with Cyanopica was watching them raid garbage cans in a park in Andalucía. My second encounter with them (in the wild at least) was watching them do exactly the same thing on the PKU campus in Beijing.

  6. #6 neil
    December 20, 2008

    I am insanely jealous. Azure magpies, white storks, and loads of other birds that would cause a major twitch if they turned up here.

    And bobs pics are great. Any idea what camera/lens he was using?

  7. #7 David Marjanovi?
    December 20, 2008

    C. cyanus

    Cyanopica cyana, surely?

    My second encounter with them (in the wild at least) was watching them do exactly the same thing on the PKU campus in Beijing.

    I missed them there :-(

  8. #8 shiva
    December 20, 2008

    I thought N. tenuirostris was “officially” extinct, and reports of its continued existence were in the same sort of disputed zone as those of things like Ivory-billed Woodpecker…

    As for white-headed gulls, i posted a comment asking what the “official” number of species in England was in a previous thread, but i think it got lost among debates on cladistics… is there a consensus?

    I ask because, here in Birmingham, there seem to be *at least* 4 different adult wing shades, ranging from the very pale, lanky, pink-legged obvious Herring Gulls to the almost-crow-black obvious Lesser Black-Backs, but there are 2, possibly 3 intermediate “colour phases”, to the extent that it almost looks like a continuum like human skin/hair colour…

    I’ve seen Little Egrets as far north as by the M6 somewhere near Stoke-on-Trent.

    Very bizarre about the population distribution of those magpies…

  9. #9 Graham King
    December 20, 2008

    Darren, delighted to hear you had such a varied and enjoyable time seeing so much.

    Your enthusiasm is contagious in that different but overlapping world of yours from mine
    (I always like to see birds, & often try to mimic their calls in hope of a reply; but you know far more and in far greater detail about the far more birds you see!)

    and great photos with it.
    Ta for these glimpses!

    Wax-eating birds, hmm, now that is an intriguing ability.

  10. #10 Dartian
    December 20, 2008

    Shiva:

    I thought N. tenuirostris was “officially” extinct, and reports of its continued existence were in the same sort of disputed zone as those of things like Ivory-billed Woodpecker…

    The slender-billed curlew is rare but not extinct, AFAIK. Perhaps you’re thinking of the North American Eskimo curlew Numenius borealis? Its continued existence is very much in doubt.

    As for the official number of English gull species, I can’t help, I’m afraid. Gull taxonomy is a topic for the true expert, and I’m not one. But I may point out that elsewhere in the western Palearctic, the gull colour range is even wider than in the UK. The lesser black-backed gulls of the nominate subspecies, Larus fuscus fuscus, have the blackest black backs of them all; blacker even than the backs of the greater black-backed gull L. marinus.

    At the other extreme, some highly arctic gull species have either extremely pale grey backs (glaucous-winged gull L. glaucoides) or all-white backs (ivory gull Pagophila eburnea).

  11. #11 chris wemmer
    December 20, 2008

    Great field report and birding. I remember seeing sections of giant trees that had once been logged in the Atlas Mountains. Can’t remember if it was at the Wildlife Department or a museum in Rabat. The vegetation on those mountains has changed a lot. Be sure to hunt this down on your next trip there.

  12. #12 tai haku
    December 20, 2008

    I think with every day passing since the last confirmed siting (has there been one this decade?) N. tenuirostris moves deeper into presumed extinct territory. With that said its continued existence is at least feasible off the back of how little we know about where it breeds.

  13. #13 Darren Naish
    December 20, 2008

    Slender-billed curlew sightings have been reported lately, but never more than a couple in one year. Wikipedia’s entry has data and citations. A British record from 2004 was probably a misidentification.

  14. #14 Dr. Nick
    December 20, 2008

    From Dartian:

    At the other extreme, some highly arctic gull species have either extremely pale grey backs (glaucous-winged gull L. glaucoides) or all-white backs (ivory gull Pagophila eburnea).

    L. glaucoides is the Iceland gull.

    Glaucous-winged gulls L. glaucescens (not to be confused with the glaucous gull L. hyperboreus of the high arctic) are abundant here in northwestern North America and have middling gray backs, without black wing tips.

    Ain’t gull taxonomy a hoot?

  15. #15 Erik Knatterud
    December 20, 2008

    Fascinating wildlife. One of those species, a lone stork stayed and still does in our area, east of the lake
    Mjoesa, 100 km north of Oslo in Norway. It did not migrate back south to Spain this fall. So far it endures the cold, sleet and snow, it seems to survive from food found on a local waste dump. Will it survive and become a semi arctic stationary stork population?

  16. #16 Nathan Myers
    December 20, 2008

    It’s one thing to eat wax, and another to digest it. Are you saying they extract nourishment from the wax they eat?

  17. #17 Darren Naish
    December 20, 2008

    Are you saying they extract nourishment from the wax they eat?

    Yes. Remember that there are birds whose diet consists of pretty much nothing but wax (the honeyguides). These birds have even been reported coming into churches to eat candle wax, and I’m sure I recall reading of cases where people had kept captive individuals and fed them nothing but wax. Last I heard, no-one had any idea how this might work. I remember this subject coming up previously in the series of articles on oxpeckers (they don’t eat candle wax or bee wax, but ear wax produced by large artiodactyls. Yum).

  18. #18 wolfwalker
    December 21, 2008

    …set off on a trip to the Cretaceous exposures of Morocco.

    first thought: damn, a perfectly good setup line, lost.

    Second thought: well, being a Brit, maybe he hasn’t ever heard of the fabled Bing & Bob on The Road to Morocco.

    Someone claimed a sighting of Eskimo Curlew in Nova Scotia two years ago, and even got a photo or two. But the photos were poor quality and not conclusive.

    Yeah, gull taxonomy is a mess. The Larus species form a classic species-swarm, and at least here in North America, the American Ornithological Union seems to be arguing over exactly how many species there are. A lot of expert birders seem to consider Kumlien’s Gull almost a species in its own right, not just a subspecies of Iceland Gull.

    I envy you being able to bird North Africa, Darren. So many species you just don’t get anywhere else, and so many more than only occur as vagrants elsewhere.

  19. #19 Dartian
    December 21, 2008

    L. glaucoides is the Iceland gull.

    So it is. My mistake, Dr. Nick.

  20. #20 David kelly
    December 21, 2008

    “As for white-headed gulls, i posted a comment asking what the “official” number of species in England was in a previous thread, but i think it got lost among debates on cladistics… is there a consensus?”

    As far as I am aware the BOU recognise

    L argentatus European herring Gull
    L smithsonianus American Herring Gull
    L michaellis Yellow-legged Gull
    L cachinnans Caspian Gull
    L glaucoides Iceland Gull
    L hyperboreus Glaucous Gull
    L fuscus Lesser Black-backed Gull
    L marinus Great Black-backed Gull
    L glaucescens Glaucous-winged Gull

    as the large white-headed gulls having occurred in Britain.

    As for Slender-billed Curlew see http://news.bbc.co.uk/1/hi/uk/7764009.stm

    David

  21. #21 shiva
    December 21, 2008

    David – thanks for the info. I know there aren’t any hyperboreus, glaucoides or marinus in Birmingham, because they don’t get *that* pale, and the darkest ones are the smallest… and i’m guessing smithsonianus and glaucescens, being North American species, are rare vagrants, so unlikely to be among the regular gull population of an inland city (though they’re both well within the colour range)… so that leaves 4 species, which corresponds reasonably well with my observations.

    However, there are the really black-winged fuscus (as black as a crow), and then some birds that are very noticeably lighter than them, but definitely too dark to be michahellis or cachinnans… i have no idea what they are (unless one or other of those last 2 is considerably darker than the photos of it on Wikipedia make it out to be)…

    On the curlews, i wonder if European Curlew and Whimbrel ever hybridise, and if so what the hybrid would look like…

  22. #22 David Kelly
    December 22, 2008

    Larus fuscus has 3(?) widely recognised subspecies and Larus argentatus has 2.

    The darkest one is L.f. fuscus (aka Baltic Gull), this is as dark as a Larus marinus, then there is L.f. intermedius which is lighter but not as light as L.f. graellsi, this is the subspecies which breeds in Britain. Chances are that in Birmingham your seeing examples of birds conforming to these “subspecies” (although not very dark, darker and very dark oversimplifies their identification).

  23. #23 David Marjanovi?
    December 23, 2008

    Last I heard, no-one had any idea how this might work.

    Well, they or their gut bacteria must have an enzyme that cuts the wax at the oxygen atom. Once that is done, the rest is relatively straightforward — you get a fatty acid and an insanely long alcohol which you can most likely turn into a fatty acid.

    Of course, that doesn’t get them any protein. Is there any in bee wax? Do the bees spit in their wax…?

    oxpeckers (they don’t eat candle wax or bee wax, but ear wax produced by large artiodactyls. Yum).

    Not that I knew anything, but I bet that’s straightforward fat that any idiot can digest.

  24. #24 Nathan Myers
    December 23, 2008

    Finchwench (linked from my name below) keeps a bulbul that nips at her candles. Maybe Sara can be persuaded to perform experiments…

  25. #25 Tommy Tyrberg
    December 25, 2008

    I don’t believe the theory that persecution prevents Cyanopica from spreading. In that case why didn’t they spread during previous interglacials? There isn’t a single fossil of it outside southern Spain, not even in the very rich french fossil record. Admittedly not a lot of museums have comparative material of Cyanopica, but its size is distinct among corvids, so it should have been noticed. It seems that, like the Florida Scrub Jay, a biogeographically similar case, it has remained stuck down in its little peninsula for a million years.

    By the way it’s michahellis, not cachinnans you see in Morocco, and also did you know that the only gull with a long history in the Mediterranean is audouinii, the other gulls are completely absent from pre-holocene deposits, there were lots and lots of shearwaters instead.

  26. #26 Dartian
    December 30, 2008

    Tommy Tyrberg:

    the only gull with a long history in the Mediterranean is audouinii, the other gulls are completely absent from pre-holocene deposits, there were lots and lots of shearwaters instead.

    Very interesting and quite surprising. One would think that a gull, and particularly a ‘herring gull’ (sensu lato), could make a living pretty much anywhere. Apparently, though, many/most gulls are commensals on human civilization to a greater extent than often realized, at least at lower latitudes.

  27. #27 Horwood Beer-Master
    January 8, 2009

    I would love to see Azure-winged Magpies in the wild! They’re one of those species I’ve had a particular fascination with since first learning about them. Unfortunately I’ve only managed to see them in captivity thus far.

    It’s a strange thought that my Nephew (who’s due to be born this spring sometime) will be growing up thinking of things like Little Egrets as totally familiar and un-exotic birds, in much the same way as I think of Collared Doves (unlike my Dad who remembers when they first arrived).

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