Tetrapod Zoology

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I’ve returned several times on this blog to the Slow-worm Anguis fragilis, a legless anguid lizard that occurs across Europe and Asia as far east as western Siberia. I find slow-worms very charismatic animals. Part of the appeal might be that they are easy to find in the places where I’ve lived, part of it might be that we Brits have such a poor reptile fauna that we hold those few species we do have in special regard, and part of it might be that they’re really cute and cool to look at. Slow-worms (there are actually two species: A. fragilis, and A. cephallonica of the Peloponnese and Ionian islands), and their close relatives within Anguidae, are relatively intelligent by lizard standards, and captive individuals exhibit behaviours suggesting that they learn to recognise their keepers. They’re long-lived; a captive slow-worm at Copenhagen lived for 54 years.

However, despite my affection for them, there are some members of the species that I, personally, find shockingly alien and difficult to come to terms with…

One thing that I find particularly interesting about slow-worms is the question of how big they get. I find this subject so interesting because, of all the slow-worms I’ve seen, none have ever been any longer than 25 cm. Other British people with experience of this species talk of individuals of between 25-30 cm as being exceptionally big, so I know I’m not alone [the individual shown at top, photographed in Cardiff, was reported as exceptionally large yet is 'only' about 30 cm long]. Despite this, some slow-worms well exceed these lengths, with the world record being 48.9 cm for a male discovered in Portsmouth (Fairfax 1965). That’s close to home: I don’t live in Portsmouth, but it’s the location of my academic base (the University of Portsmouth).

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Particularly big slow-worms are also reported to occur on Flat Holm and Steep Holm, two small islands in the Bristol Channel [in the adjacent photo, Steep Holm is the dome-shaped island on the right]. In 1975 British herpetologist Tony Phelps discovered a Steep Holm slow-worm that was 45 cm long, and estimated by him to be between 60 and 70 years old (presumably on the basis of its size). In 1984 an individual 39 cm long was photographed on Steep Holm by slow-worm expert Nick Smith but, because it had a regenerated tail, its original length (i.e., with its intact original tail) would have been about 530 mm, thus making it a new world record.

I’ve never visited Flat Holm or Steep Holm, but I have seen them, if that helps. It makes sense that exceptionally big slow-worms occur on small islands like this, but the fact that the global record-holder comes from Portsmouth is surprising, especially given that Portsmouth is highly urbanised and with very little good space for wildlife: for a flavour of the city, have a look at Graeme’s photos.

Having mentioned Steep Holm, I can’t resist saying a bit more about its wildlife. In 1977, Chinese muntjac Muntiacus reevesi were introduced to the island. Muntjac are all over Britain today following repeated waves of introduction that occurred from the 1870s onward, though quite why anyone would want them on a steep-sided island that has a total area of less than 0.25 sq km (63 acres) is a bit of mystery. Unsurprisingly, Steep Holm’s muntjacs have repeatedly tumbled to their deaths, with at least seven of the animals dying this way between 1984 and 1986. Interestingly, stomach contents showed that these unlucky muntjacs were in the habit of clambering down the steep cliffs to eat seaweed on the beaches (Legg & Parsons 1990). Elsewhere in the world, various populations of sheep, cattle and red deer visit beaches to eat seaweeds, so this behaviour is not without precedent.

Even stranger than the introduction of muntjac is the 1907 introduction of the Orkney vole Microtus arvalis orcadensis to Steep Holm. This was the brainchild of Cardiff chemist Robert Drane, who ‘looked forward to the surprise of someone happening to find [Orkney voles] on Steep Holm’ (Legg & Parsons 1990, p. 46). The attempt failed, however. The Orkney vole was first described as a new species in 1904 and initially thought to be a relict endemic that found refuge on the Orkneys after the spread across Pleistocene Britain of the Field vole M. agrestis (Hinton 1910). We now think that the Orkney vole was introduced by people to the Orkneys, with chromosomal studies indicating that the original population came from France or Spain. Anyway, I digress.

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Despite my failure to ever see a remarkably big slow-worm, a few of my friends and colleagues have been more lucky. One of my closest friends and allies is Stig Walsh: taphonomist, palaeontologist, artist, woodsman and all-round outstanding human being [adjacent photo features (left to right) me, Stig and Monja, Stig's girlfriend. Note the Steve Irwin t-shirt]. Curiously enough, Stig’s Portsmouth garden was once home to what appears to have been a particularly big adult male slow-worm, though unfortunately I never saw it and hence was never able to measure it. Stig got to photograph it however, and below is one of his images. As you can see, this animal was co-operative enough to align itself against some bricks that would allow its length to be estimated. I don’t yet know exactly how big those bricks are, so haven’t done this, but my estimate is that the animal exceeded 30 cm.

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More recently, my good friend Markus Bhler (whom regular blog readers might know better as Sordes) was lucky enough to encounter a particularly big male slow-worm in Germany. It was dead, perhaps as a result of ingesting poisoned prey, and measured about 45 cm. Markus has preserved the specimen and has kindly supplied photos [one is shown below]. Again, from my perspective the animal is a monster, and well outside my range of experience.

What’s weird is that some of these especially big slow-worms look quite different from the smaller animals I’m used to, and in fact this goes for many of the slow-worms that come from continental Europe. Superficially, what with their bulkier proportions and more clearly demarcated scales*, they look rather more like glass lizards Ophisaurus than do normal British slow-worms. Glass lizards are legless anguids that are sometimes described as particularly big slow-worms. Named for their particularly fragile autotomising tails, there are about 15 species that inhabit woodland and steppe habitats across North America, Morocco and Eurasia. The best known of them is O. apodus, the Sheltopusik. This is a huge Eurasian species that can reach 1.4 m.

* Slow-worms and glass lizards don’t just possess scales: they’re actually encased in subrectangular osteoderms. These are highly distinctive as fossils and help explain why the group has such a good fossil record.

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What makes the similarity between some slow-worms and glass lizards even more interesting is that a recent phylogenetic analysis found that slow-worms are not just closely related to glass lizards, they apparently are glass lizards; in other words, they are deeply nested within Ophisaurus, being most closely related to O. apodus (Macey et al. 1999). My speculation is that the Ophisaurus-like slow-worms of continental Europe are basal members of the slow-worm lineage, and that British populations form an unusual, presumably young, clade. This could all be nonsense, but it’s a working hypothesis. Population-level work of the sort needed to test it has been published on some Asian glass lizards (Lin et al. 2003), but not on slow-worms so far as I know.

Are slow-worms really glass lizards? If they are, this raises a few problems for the classification and taxonomy of these lizards. There is also the alternative view, promoted by Sullivan (1987), that slow-worms, Old World glass lizards, and American glass lizards represent highly disparate lineages that have been separated since the Eocene at least and are only alike due to convergence. While I wanted to cover all of this here, it’ll have to wait, like so much else… to another time.

More on anguids soon, but this time on rather more exotic forms.

For previous articles on the British herpetofauna see Beasts of Portland, Spiky-frilled, lek-breeding amphibious salamanders, Britain’s lost tree frogs and Hunting green lizards in Dorset.

Refs – -

Fairfax, R. A. 1965. Very large English slow-worm. British Journal of Herpetology 2, 229.

Hinton, M. A. C. 1910. A preliminary account of the British fossil voles and lemmings; with some remarks on the Pleistocene climate and geography. Proceedings of the Geologists Association, London 21, 489-507.

Legg, R. & Parsons, T. 1990. Steep Holm Wildlife. Wincanton Press, Wincanton.

Lin, S.-M., Chang, W.-S., Chen, S.-L., Shang, G. & Lue, K.-Y. 2003. Taxonomic status of the legless lizard Ophisaurus (Squamata: Anguidae) in Taiwan: molecular data, morphology, and literature review. Zoological Studies 42, 411-419.

Macey, J. R., Schulte, J. A., Larson, A., Tuniyev, B. S., Orlov, N. & Papenfuss, T. J. 1999. Molecular phylogenetics, tRNA evolution and historical biogeography in anguid lizards and related taxonomic families. Molecular Phylogenetics and Evolution 12, 250-272.

Sullivan, R. M. 1987. Parophisaurus pawneensis (Gilmore, 1928), new genus of anguid lizard from the middle Oligocene of North America. Journal of Herpetology 21, 115-133.

Comments

  1. #1 Neil
    May 8, 2007

    Despite much effort this year I STILL havent seen a Slow worm. I have manged to see to grass snakes and massive (for british frogs anyway) Marsh frogs for the first time this year.
    Next time you see Mark and Richard could you please give them some tips on finding slow-worms as there going to help me find some when I come to Portsmouth next – though they don’t know it yet :)

  2. #2 John Scanlon
    May 8, 2007

    Hi Darren, and thanks for getting back to the important stuff (scaly and legless). Has anyone tried introducing Ophisaurus to Britain? Apart from making great pets, my impression from wandering through a few European museums is that they’ve been popular as artists’ models since antiquity (in classical statuary, most serpents, hydras and ‘pythons’ seem to have Ophisaurus faces, with oriental vipers in distant second place). Then of course there’s the Basilisk in the Harry Potter movie (Ophisaurus with a few frills and fangs stuck on)…

  3. #3 Larry Ayers
    May 8, 2007

    Being a resident of Missouri in the USA I’ve never encountered, or, truth to tell, ever even heard of slow-worms. Legless snake-like lizards! All we have around here are skinks.

  4. #4 luca
    May 9, 2007

    Cool,

    first and only animal I did preserve in alcool was a smallish (10 cm) slow worm (or glass lizard?), found when I was some seven years old during a scout outing. I kept it for years ’til my mum got rid of me when I was away. grr…

  5. #5 Hai~Ren
    May 9, 2007

    Well that’s fascinating, the thought that slow-worms and glass lizards are closely allied.

    So, if it does turn out that slow-worms are nested amongst the glass lizards, does this mean Ophisaurus is paraphyletic? Or will Anguis be sunk into Ophisaurus? (The latter seems a little difficult, considering the whole family is named after the slow-worms)

  6. #6 Darren Naish
    May 9, 2007

    Well that’s fascinating, the thought that slow-worms and glass lizards are closely allied.

    So, if it does turn out that slow-worms are nested amongst the glass lizards, does this mean Ophisaurus is paraphyletic? Or will Anguis be sunk into Ophisaurus? (The latter seems a little difficult, considering the whole family is named after the slow-worms)

    If Anguis is nested within Ophisaurus s. l., then this makes the latter paraphyletic, yes. To avoid this paraphyly, Macey et al. (1999) proposed that all glass lizards and slow-worms be sunk into the oldest name (Anguis Linnaeus, 1758). Another solution would be to rename only those ‘Ophisaurus‘ species closest to Anguis, to retain Ophisaurus only for the type species and its closest relatives, and to give other names to the species that neither group with Ophisaurus or Anguis. Some authors (e.g., Sullivan 1987) have argued that Old World glass lizards aren’t close to Ophisaurus proper, and should be regarded as a separate taxon, Pseudopus. I’ll cover all of this in more detail in another post.

    Response to John: glad you liked the post. I am not aware of any records of glass lizard introductions to the UK, but I’m sure they would survive if someone were to introduce them. Good point about the classical influence. I reckon this is because they have freaky looking faces and quasi-human eyes…

  7. #7 David Marjanovi?
    May 9, 2007

    I’m sure Anguis has priority…

    There are no skinks in Europe, at least north of the Alps and Pyrenees. Ice ages and east-west mountain ranges will do that to a continent. That’s why the palaeobatrachids and albanerpetontids are extinct *snif*.

  8. #8 Sordes
    May 9, 2007

    Hallo Darren!

    Nice to see the picture of my slow-worm at this post. Perhaps I should add for the others that it is even a bit longer, somewhere between 45 and 48cm, but not as thick as it looks on the photo(because the glass acts like a lense). It would be really interesting to know how old it was.
    But to come on the distribution of british and continental slow-worms, I have my doubts that the british population is evolutionairy younger, as they still posses external relics of hind limbs, what mainland slow-worms doesnt, so this is a bit problematic. If british slow-worms possess a primitive anatomic feature, continental slow-worms should possess it too, if they are evolutionairy older.

  9. #9 Graeme
    May 9, 2007

    Thanks for the link! I have to confess that I’ve never seen any form of slow-worm or snake in Portsmouth proper. In fact besides birds (some of which are very interesting) and a couple of local foxes, wildlife is rare. Plenty of (non-feral) cats, but I can’t recall seeing much above the insect scale. But then I spend most of my time in a fourth-floor flat or in uni/gunwharf…..

  10. #10 Zach Miller
    May 9, 2007

    I’m no expert on slow-worms or glass lizards, so I have to ask: what anatomical differences separate the two? Also, do you think that slow-worm/glass lizard evolution mirrored that of snake evolution? The two have wildly different skull structures, sure, but that seems secondary to the fact that both groups lack LIMBS. So, in studying the evolution of legless snakes, couldn’t we learn something about the evolution of snakes?

    I keep reading about snake evolution without reading mention of legless lizards, which bothers me. Always with the burrowing or aquatics or mosasaurs.

  11. #11 Rajita Rajvasishth
    May 9, 2007

    Nice blog — Happy to have discovered this one. Perhaps, it can be a model for biology blogs.

    I had a question: In the days when I studied vertebrate zoology it was believed that Ophiodes and Anguis/Ophisaurus represent two independent convergent cases of limblessness in Anguidae. But I was recently discussing this issue with my friend who suggested that they might actually been monophyletic base on morphological features of the cranial nerve exits. Has this issue been recently addressed? When do the earliest unambiguous anguids and anniellid appear in the fossil record?

  12. #12 Sordes
    May 10, 2007

    BTW David, there is a species of skinks in Europe the snake-eyed skink Ablepharus kitaibelii which inhabits east-and south-east Europe. Many years ago I saw one at Samos, Greece, it look like a small slow-worm with legs.

  13. #13 Mark Lees
    May 10, 2007

    If my garden is anything to go by slow worms must be one of the commonest terrestrial vertebrates in the UK (well in South Wales anyway). I never use pesticides and often use old pieces of carpet to prevent weeds growing in beds that have been dug over. Lifting the carpets during Summer (particularly early Summer) tends to reveal a good stock of slow worms (and occasionally a toad or grass snake). Indeed my younger nephew called one part of my garden “Slow worm city”.

    The colours are rather variable, browns, good coppery tones and coppery pinks. The sizes vary significantly. At this time of year I see quite a lot of last year’s juveniles, I’ve never measured them but I guess they are 7-10cm long and very thin. When they are that young I dont find the width of the head a good way of distinguishing male from female, but the dorsal stripe is already a good identifier. Indeed one ecologist I know reckons that the dorsal stripe on the female was the most reliable way of distinguishing them early on – any one know if thats true? Big specimens seem to mostly be around 15-20cm, but the girth is very variable, with some of them impressively thick. I have never seen a record breaker, in fact I’m quite sure I have never seen one longer than about 22/23cm.

    A friend of mine used to live just down the road from me, and had a garden that consisted mostly of rough grass strimmed a few times a year. He used to place corrugated sheets of iron on the ground to attract the slow worms. On one occasion, on a Summer evening we lifted one and saw a scene a bit like one of those ‘snake balls’ I have seen on TV, where snakes hibernate communally. I didn’t count how many, but my recollection is that there must have been a several dozen slow worms, many of them tangled together. It was a weird sight!

    Those east-west mountains David referred to, as well as the Med, cost Europe a lot more than just a few herps – our whole flora and fauna is rather depauperate due to them.

  14. #14 Darren Naish
    May 10, 2007

    Lot of neat comments there, thanks everyone. I’ll try to respond, briefly, to everything…

    Markus/Sordes wrote…

    I have my doubts that the british population is evolutionairy younger, as they still posses external relics of hind limbs, what mainland slow-worms doesnt, so this is a bit problematic. If british slow-worms possess a primitive anatomic feature, continental slow-worms should possess it too, if they are evolutionairy older.

    The British population has only been isolated for about 7000 years, so if it really does have any differences from continental populations they must be very recently evolved. I had no idea that British slow-worms possessed skeletal hindlimb relicts, what is your source for this? [I just checked a skeletonized slow-worm in my collection, and didn't see anything that looked like a hindlimb element]. Remember also that retention of a plesiomorphy does not show that any one taxon or population is necessarily ‘more primitive’ than another.

    Zach asked…

    I’m no expert on slow-worms or glass lizards, so I have to ask: what anatomical differences separate the two? Also, do you think that slow-worm/glass lizard evolution mirrored that of snake evolution? The two have wildly different skull structures, sure, but that seems secondary to the fact that both groups lack LIMBS. So, in studying the evolution of legless snakes, couldn’t we learn something about the evolution of snakes?

    There are loads of detailed differences between slow-worms and glass lizards; the most obvious are that slow-worms lack the lateral skin fold of glass lizards and, while glass lizards are oviparous and very long-tailed, slow-worms are viviparous and shorter-tailed. As for what legless lizards tell us about the evolution of snakes, the easy answer is to direct you to…

    Wiens, J. J. & Slingluff, J. L. 2001. How lizards turn into snakes: a phylogenetic analysis of body-form evolution in anguid lizards. Evolution 55, 2303-2318.

    It’s available, free, here.

    Rajita wrote…

    I had a question: In the days when I studied vertebrate zoology it was believed that Ophiodes and Anguis/Ophisaurus represent two independent convergent cases of limblessness in Anguidae. But I was recently discussing this issue with my friend who suggested that they might actually been monophyletic base on morphological features of the cranial nerve exits. Has this issue been recently addressed? When do the earliest unambiguous anguids and anniellid appear in the fossil record?

    Yes, South American Ophiodes is almost certainly convergent with glass lizards and not closely related to them; the genetics indicates that it’s a diploglossine close to galliwasps. If there’s morphological support for a grouping of Ophiodes with glass lizards, that’s news to me and I don’t think it’s been published (correct me if I’m wrong). On fossils, anguids are present as early as the Upper Cretaceous (e.g., Odaxosaurus from Wyoming and elsewhere). Anniellids have a supposed Eocene record in Apodosauriscus from the Eocene of Wyoming. Anniella itself has a fossil record going back to the Miocene.

    And that’s that. If you like anguids, you’ll (hopefully) love what’s coming next.

    Oh, and Mark.. I know people who would love to visit your garden :)

  15. #15 Sordes
    May 11, 2007

    Hallo Darren!

    I saw many years ago a documentation about british wildlife, and there was said that the british slow-worms still possess small external limb relics, and I think they even showed them. This was about ten years ago, but I still can remember that there was a slow-worm which had something like a skin fold which resembled small stumpy leg relics. I also thought that I read somewhere about it. But well, perhaps Im wrong.

  16. #16 Darren Naish
    June 11, 2007

    I finally got round to checking the literature on the pelvic/hindlimb skeleton of Anguis. Descriptions and diagrams of the Anguis pelvis and sacrum were provided by Paul Stokely (1947). In the pelvic girdle, all three bones are fused and both the pubes and ischia only persist as short nubbins of bone. The iliac process is a long, curved structure [not unlike that of a squamate with unreduced limbs] that has a sacral contact with the vertebral column. There is no obvious acetabulum and he confirmed (p. 741) that no hindlimb bones at all are present.

    However, Stokely’s Anguis specimen was from Germany – so is it possible that the anatomy that he described is different from that of British specimens? I dug out the pelvis from a British slow-worm in my collection: it looks identical to the one figured by Stokely (including in its lack of acetabulum), so I provisionally conclude that this typical British slow-worm was like the German specimen used by Stokely in lacking any and all hindlimb elements. Furthermore, I assume that all British slow-worms are like this. I would be happy to be corrected however!

    Ref – -

    Stokely, P. S. 1947. Limblessness and correlated changes in the girdles of a comparative morphological series of lizards. The American Midland Naturalist 38, 725-755.

  17. #17 Sordes
    June 11, 2007

    Interesting, I ask me why I once heard about this alleged relics of hind limbs in british slow-worms.
    By the way, I?ve seen some further members of our local herpetofauna in the last days. For many years I have seen only one specimen of Natrix natrix, what was last year in the pond of a botanical garden. Yesterday I saw a really huge specimen on a way. It was really enormous, at the thickest part as thick as an egg (most probably because it ate a frog or a mouse)and very long. Later at the day I saw 3-4 subadult specimens in a pond. What a great day. Today I found at a completely different location a tiny specimen of N. natrix, only about 15cm in length, and thinner than a pencil. At the first look I thought is was a worm,and then a baby slow-worm, because I had never suspected to see a baby snake there. I hope I´ll be able to show some of the photos on my blog in the next time.This are really beautyful animals, and it is really a shame that still people sometimes try to kill them.

  18. #18 Sordes
    August 5, 2007

    Hallo Darren! I just wrote in my blog about the giant slow-worms in my collection, and Michael Schneider (Webmaster and head of the “Verein für kryptozoologische Forschungen”) showed me a photo of another very large slow-worm he photographed in his garden (here).
    The plates are around 60cm wide, so this one was also a very large speciemen. BTW, I sized the pictures of the “pickled” giant slow-worm on my blog to life-size, this gives already a better idea about the actual size (here).

  19. #19 sandra sharpe
    August 17, 2007

    I think I may have just seen a baby slow worm. It was about seven inches long, more gold coloured than copper, and moved quite quickly across the ground. I did see a grass snake last weekend, wound round some blackberry stems – we left that well alone.

  20. #20 Mark Johnson
    June 10, 2008

    Until I started work in a factory in Watford, (some 8 years ago), I had never seen a Slow Worm. Now I see them every year especially in our canteen. This tends to lead to screams of “Snake, Snake”. It is usually me that picks them up and puts them outside. This I found difficult as they are hard to grip and on one occasion I was amazed when the tail fell off and wriggled like mad whilst the Slow Worm played dead. Now I use card to scoop them up. Also whilst in Turkey in May this year I was really lucky to see a massive, what I thought, was a Slow Worm. It was at least 4 foot long and some 3 inches in gerth. A magnificent creature. I had no idea they could grow so big.

  21. #21 Darren Naish
    June 10, 2008

    Hi Mark. The 4 ft-long animal was not a slow-worm but a glass lizard. Thanks for the comment!

  22. #22 Stig Walsh
    March 24, 2011

    An old post, but interesting to read, as I don’t think I ever read it when it was current. I think you were right with your size estimate for ‘Bernhardt Schlange’ (our nickname for the slow worm that looked like a snake). Shame we didn’t see it againg for a few years before we left that house – most likely a cat got it (and caustic soda di for the extremely large frog; please don’t ask).

    Oddly enough, I used to live only a few miles from Steep Holm and Flat Holm – tried to get there once in a dingy and ran out of fuel fighting the infamous Bristol Channel tide…

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