Sunday, May 21, 2006

The most freaky of all mammals: rabbits

I made the point in a previous post (on gulls) that many animals which we take for granted are, when you think about them, actually very odd. And for a long time I’ve been thinking that this is oh so true of one of the mammals I see the most, the rabbit Oryctolagus cuniculus. Actually, I don’t have that species specifically in mind, but in fact all lagomorphs. Before I start on the generalizations, I’ll take this opportunity to point out (for those who might not know) that – while we have millions of bunnies here in the UK – they’re not native. The rabbit is in fact an animal of the Mediterranean region, and it’s supposed to have been introduced by the Normans after the conquest of 1066. However, there is apparently no mention of rabbits in the Domesday Book (written in 1086), and they don’t get a mention in the literature until 1176 (and even then only in a report about the Scilly Isles). It’s on the basis of this that some workers think it more likely that rabbits were actually introduced by the Crusaders in the 12th century (McBride 1988). We do have two native lagomorphs by the way, the Brown hare Lepus europeaus* and the Blue hare L. timidus*. Within Lagomorpha, rabbits and hares make up the clade Leporidae, and the less well-known pikas (aka ochotonids) form their sister-taxon.

* The correct species name for the Brown hare is controversial and the reality/monophyly of the Blue hare has recently been contested. I don’t want to cover these issues here: if you’re interested see Waltari & Cook (2005) and Ben Slimen et al. (2006).

Musings on Watership Down

It’s not in line with the rest of this post, but I’ll never forgive myself if I miss this opportunity to talk about Watership Down. I must confess to never having read Richard Adams’ 1972 book, but I really like the film and I like it more the more I see it. While not exactly zoologically accurate (the rabbits have religion, mythology, language, human emotions, team up with a friendly Black-headed gull Larus ridibundus, and learn how to use boats, among other things), some of it is not a million miles away from what we really know about rabbit society.

Two things make the film particularly memorable. Firstly, it begins with the rabbit myth of creation. In the beginning Frith, the lord of creation, made all animals alike, and they ate grass together. But El-ahrairah, the first rabbit, produced so many children that Frith became angry: control your people, or I will do something about it. El-ahrairah did nothing about it, so Frith did. He gave each of the animals a gift, and they were no longer the friends of El-ahrairah’s children – they wanted to catch them and kill them. The weasel. The stoat. The fox. The hawk. The owl. But Frith also gave El-ahrairah a gift – a bright white tail that flashed as a warning, long legs to run fast, and big ears to hear his enemies. The sequence ends as Frith tells El-ahrairah “All the world shall be your enemy, prince with a thousand enemies, and whenever they catch you, they will kill you. But first they must catch you, digger, listener, runner, prince with a swift warning. Be cunning and full of tricks and your people shall never be destroyed”. It’s a good way to start a film. The second thing that makes the film memorable is how dark and disturbing it is in places. Some of the main rabbit characters are killed by predators, caught in snares, or buried alive. Death, overall, is an important part of the story, as it is in the real lives of rabbits I suppose.

Why rabbits are just wrong

Moving on… why regard rabbits as ‘the most freaky of all mammals’? To begin with, just look at how weird they are. They’re familiar to us, but their anatomy is actually highly odd. Example? Their teeth are strange, with cusps and folds that have proved almost impossible to homologise with those of other placental mammals. The sides of their snout bones are decorated with a bizarre lattice-work of filigree bone texture (why?). Their incisive foramina (openings on the bony palate) are uniquely elongate (for what purpose?). A thin splint from their frontal bones projects down and forward, finger-like, among the snout bones. Their hindlimbs are proportionally elongate relative to their forelimbs (odd for a quadupedal mammal, when you think about it). Their ankle bones are uniquely strange, with the calcaneum housing a canal that runs diagonally through the bone (Bleefeld & Bock 2002). No other mammal has anything remotely like this. The undersides of their feet are completely covered by thick fur – that’s odd, and unique. And don’t get me started on their genitals (read on).

Many aspects of their physiology and behaviour are also odd compared to what we’re more familiar with. Get this: when baby rabbits suckle, the milk is ejected in one big squirt that only occurs after the mother has been sufficiently stimulated by the paddling action of the babies’ paws. Male rabbits also squirt, but this time the liquid is urine, and it gets squirted over potential mates. As is reasonably well known, lagomorphs practice refection – that is, they have to ‘rescue’ nutrients from their digested food by ingesting their own caecal pellets (they therefore only produce dry droppings once the food has been through the system twice). And lagomorphs are also odd in practicing so-called absentee care, with mother rabbits spending just 0.1% of their time with their young.

What, if anything, is a rabbit? (homage to Wood)

Working on the assumption that organisms should be regarded as freaky when we can’t even work out what they are, rabbits excel. Albert Wood (1957) explored this area when he wrote ‘What, if anything, is a rabbit?’. Check out the first paragraph of his paper: ‘The title of this paper is slightly modified from that of an article I encountered some years ago, which appeared to be approaching the problem of the relationships of the Lagomorpha, or rabbits and their relatives, from the most basic point of view. This paper, entitled “Gibt es Leporiden?”, seemed to be questioning the very existence of such animals. Investigation showed, however, that the question involved was not whether members of the family Leporidae existed, but whether rabbit-hare hybrids did. Since then, I have met no one who questions the existence of rabbits and hares, and I have been reluctantly forced to accept them.’ (Wood 1957, p. 417).

Originally, rabbits were included in Rodentia, and they weren’t formally separated from them until Gidley (1912) did so. What makes this decision particularly interesting is that Gidley suggested that lagomorphs had no close relationship to rodents at all, but shared some intriguing similarities with artiodactyls. While a few authors commented on this idea after Gidley, the evidence for it isn’t great. Mostly it comes down to a superficial similarity between certain Cenozoic artiodactyls (like cainotheres) and lagomorphs, and the transverse chewing style and artiodactyl-like ankle structure of lagomorphs.

It’s also been noted that lagomorphs possess similarities with the pantodonts and dinoceratans of the Palaeogene. If you know what the members of these groups looked like, you’ll understand why positing an affinity between them and lagomorphs is so radical. I’ll cover it in another post some time. Lagomorph ancestry has also been sought among the various hoofed mammals collectively termed ‘condylarths’, and in particular they’ve been tied to periptychids like Ectoconus. For reasons of time and space I don’t want to expand on this point either, but I may do so later.

Bunnies: Mesozoic relicts, or para-marsupials?

In keeping with the idea that lagomorphs have no close living relatives, it has been proposed at times that they might have descended from groups that were otherwise entirely restricted to the Mesozoic. Based on tooth cusp morphology, Gidley (1906) suggested that lagomorphs descended from triconodontids. McKenna (1982, 1994) argued that lagomorphs are part of a larger placental clade [termed Anagalida in McKenna & Bell (1997)] that includes as its most basal members the Cretaceous zalambdalestids, although the evidence for this has more recently been assessed and rejected.

Most zoologists would be surprised to hear that, in a few features, lagomorphs resemble marsupials more than they do placentals, and it’s on the basis of these features that some workers have actually suggested that lagomorphs might be close kin of marsupials (albeit not necessarily members of Marsupialia or even Metatheria). Gregory (1910) drew attention to the arterial foramen present in the last cervical vertebra, supposedly uniquely shared by lagomorphs and marsupials (but actually occurring more widely among placentals); Hartman (1925) showed that egg development in the lagomorph fallopian tube was uniquely marsupial-like; and Petrides (1950) pointed out that lagomorphs are unique among placentals in possessing a pre-penile scrotum, a character also otherwise limited to marsupials. That’s right, a pre-penile scrotum. A scrotum that is further away from the anus than the penis is. I’ve actually, err, manipulated a few rabbits to observe this remarkable configuration, thus far without success, but then the individuals in question were neutered. Hm. Anyway: so, are rabbits actually some long-lost freakish sister-group to metatherians?

The primate hypothesis, and the resurrection of Glires

Protein sequences led Graur et al. (1996) to argue that lagomorphs were closest to primates, and these authors further argued that morphological characters used to unite lagomorphs with rodents and other groups were not really indicative of affinity. This hypothesis was hailed at the time as the most likely answer to Woods’ ‘What, if anything, is a rabbit?’, but it suffers from that widespread problem of assuming that one body of evidence must somehow outweigh, or be superior to, all the other data.

The most recent assessment of the morphological and fossil data indicates that lagomorphs are, after all, most closely related to rodents, with the two forming the larger clade Glires. This is supported by the detailed morphology of Palaeocene proto-lagomorphs like Gomphos, and by a big data set with good character support across nodes (Asher et al. 2005). According to recently published phylogenetic definitions, the term Lagomorpha is best restricted to the pika-rabbit clade (viz, the crown-clade) and the old name Duplicidentata is applied to the stem-group that includes Lagomorpha. If you’re interested, both morphological and molecular data supports the inclusion of Glires within the more inclusive clade Euarchontaglires, and herein there are the primates, dermopterans and tree shrews.

So after all that, rabbits really do seem to be part of a clade that is closest to rodents. Sadly, they aren’t para-marsupials, close kin of Uintatherium, or relict survivors from a long-lost Cretaceous radiation. But I still think they’re freaky.

The photo above was borrowed from the IUCN/SSC Lagomorph Specialist Group’s site.

PS - note that I keep my promises. A post on the strangeness of rabbits was promised way back in January: see Graeme's Pleistocene megafrog.

Coming next: late-surviving Mesozoic synapsids. Yeah, really. For the latest news on Tetrapod Zoology do go here.

Refs - -

Asher, R. J., Meng, J., Wible, R. R., McKenna, M. C., Rougier, G. W., Dashzeveg, D. & Novacek, M. J. 2005. Stem Lagomorpha and the antiquity of Glires. Science 307, 1091-1094.

Ben Slimen, H., Suchentrunk, F., Memmi, A., Sert, H., Kryger, U., Alves, P. C. & Ben Ammar Elgaaied, A. 2006. Evolutionary relationships among hares from north Africa (Lepus sp. or Lepus spp.), cape hares (L. capensis) from South Africa, and brown hares (L. europaeus), as inferred from mtDNA PCR-RFLP and allozyme data. Journal of Zoological Systematics 44, 88-99.

Bleefeld, A. R. & Bock, W. J. 2002. Unique morphology of lagomorph calcaneus. Acta Palaeontologica Polonica 47, 181-183.

Gidley, J. W. 1906. Evidence bearing on tooth-cusp development. Proceedings of the Washington Academy of Science 8, 91-110.

- . 1912. The lagomorphs an independent order. Science 36, 285-286.

Graur, D., Duret, L. & Guoy, M. 1996. Phylogenetic position of the order Lagomorpha (rabbits, hares and allies). Nature 379, 333-335.

Gregory, W. K. 1910. The orders of mammals. Bulletin of the American Museum of Natural History 27, 1-524.

Hartman, C. G. 1925. On some characters of taxonomic value appertaining to the egg and ovary of rabbits. Journal of Mammalogy 6, 114-121.

McBride, A. 1988. Rabbits & Hares. Whittet Books (London).

McKenna, M. C. 1982. Lagomorph interrelationships. Geobios, mémoire spécial 6, 213-223.

- . 1994. Early relatives of Flopsy, Mopsy, and Cottontail. Natural History 103 (4), 56-58.

- . & Bell, S. K. 1997. Classification of Mammals: Above the Species Level. Columbia University Press (New York).

Petrides, G. A. 1950. A fundamental sex difference between lagomorphs and other placental mammals. Evolution 4, 99.

Waltari, E. & Cook, J. A. 2005. Hares on ice: phylogeography and historical demographics of Lepus arcticus, L. othus, and L. timidus (Mammalia: Lagomorpha). Molecular Ecology 14, 3005-3016.

Wood, A. E. 1957. What, if anything, is a rabbit? Evolution 11, 417-425.


Anonymous Anonymous said...

Came in from PZ Myers' blog and was hooked. Great stuff!

Let me strongly recommend _Watership Down_, the book. It's excellent.

So, some marsupials also have a pre-penile scrotum. Is there reason to think this might be a primitive mammalian characteristic?


Doug M.

7:52 AM  
Blogger Gon said...

You convinced me!!! I think I'm going to consider rabbits like they should be considered. Weird. Odd. Freaky.

¡Very Nice post!

3:07 PM  
Anonymous Anonymous said...

Very interesting! I recall reading (sorry, I don't have the book to hand) that rabbits proper were "originally" limited to one coast of Spain, where they'd been stranded by the last ice age. When the early Roman explorers sailed by that coast, they thought rabbits were just another sort of hare. Since they were already raising hares, they brought some of the new type back for variety, and tossed them into the leprorariums where they kept the hares. These consisted of a yard with a low stone wall, which was sufficient to contain the surface-dwelling hares. Rabbits, of course, can burrow....

5:04 PM  
Anonymous Anonymous said...

Interesting... I enjoyred reading this post, thanks.

8:26 PM  
Blogger Randy said...

The rabbit is in fact an animal of the Mediterranean region, and it’s supposed to have been introduced by the Normans after the conquest of 1066.

But I've seen a documentary that shows a vicious killer rabbit present in England in 932 AD! Somewhere in the region of the Cave of Caerbannog. They must have been there before then.

12:33 AM  
Blogger Karl Steel said...


Great piece and a place where a medievalist can be kind of useful. If you'd like to know more about the introduction of rabbits into England and in particular the uses to which they were put, see

Bailey, Mark. “The Rabbit and the Medieval East Anglian Economy.” Agricultural History Review 36.1 (1988): 1-20.

Here's a key bit:
“In the Middle Ages rabbit-warrens represented almost the sole source of supply for rabbits and their scarcity made them a valuable and fiercely guarded commodity. Indeed, the collapse of the grain market in the later fourteenth and fifteenth centuries encouraged some landlords to develop their warrens as an alternative source of income, to the extent that rabbiting can be classed as an unlikely but successful late medieval growth industry” (2).

12:52 AM  
Blogger Steve Sailer said...

Thanks, most interesting and informative.

By the way, the book "Watership Down" is one of the great stories of the English at war. Author Richard Adams was a commando dropped on the far side of the Rhine in Operation Market Garden in September 1944 in Gen. Montgomery's audacious attempt to win the war by Christmas. Unfortunately, the Rhine bridge turned out to be "A Bridge Too Far" and Adams, like Hazel the leader of the rabbits, had to cross the Rhine and lead his men out of German-occupied territory. For a week, they lived the rabbit life, with a thousand enemies, and 25 years later Adams blended that adventure, his boyhood wanderings on Watership Down, and "The Private Live of the Rabbit" into one of the unique accomplishments in English literature.

8:36 AM  
Blogger Jean C said...

Wow, I didn't know that about Watership Down. But I did want to recommend the book. That book is wonderful.

10:14 PM  
Anonymous Anonymous said...

Yeah. Um. I'm not going to bother to tear apart your entire lifes work here, but one thing I just HAVE to say is that the scrotum is indeed closer to the anus than the penis is. Go fondle an untouched buck and you'll see why some of your sources are a bit out dated

11:52 PM  
Blogger Darren Naish said...

It's not exactly my life's work. But I shall go fondle some bucks immediately anyway.

12:14 AM  
Blogger Darren Naish said...

I missed about 10 minutes of a documentary about mooses because of your TV show. That's all I'll say, but as a note to my blog readers I would like to bring to attention the fact that your TV show isn't exactly zoologically oriented.

10:45 PM  
Anonymous Anonymous said...

Hmmm, I am not freaky!

From the house rabbit

8:20 PM  
Anonymous inchirieri apartamente cluj said...

A really nice documentation upon rabbits. You have make quite a reserch into their history and origins. It is a valuable article. Thanks.

9:56 AM  
Blogger Giliell said...

HI, been lured in here from Pharyngula, too.

Are you sure about the pellet-chewing? AFAIK (pet owner knowlege), they don't eat all their poo, but produce a special kind of poo in their appendix that they eat again. This special poo looks different, like a bunch of grapes, smells much stronger and is usually eaten inmediately, you hardly ever see it lying around. I've never seen any of ours eat the regular pellets.

BTW, the book Watership Down gives a lot of biological info on rabbits, taken from R.M. Lockley's "The Private Life of the Rabbits"

10:19 AM  

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