Thanks to everyone who had a go at identifying the ‘mystery object’ I was recently photographed holding. Obviously, said object is an antler. So, well done if you got that bit right. But it’s a very weird antler.

It obviously comes from one of the larger deer species and is consistent in overall anatomy with a cervine (and not with any of the mostly North American odocoileines – the white-tailed deer, mule deer, brockets, moose, reindeer and so on). Unlike the majority of cervine deer, however, it lacks the relatively short brow and bez tines that normally project anterodorsally from near the base of the main beam. Instead, there are two roughly equal-sized branches, both of which are forked at their tips.

A variety of antlers from my personal collection, badly photographed. The main thing to note here is the presence of what seems to be a hypertrophied brow tine in the 'Elaphurus' antler.

This very distinctive anatomy is characteristic of the globally endangered, extremely peculiar Pre David’s deer, David’s deer or Milu Cervus davidianus (previously Elaphurus davidianus). While the posterior branch of the antler is probably the beam, the long anterior branch is generally thought to be a massively enlarged brow tine, in which case the bez tine has been lost. I grew up knowing this species as Pre David’s deer but now normally think of it as the Milu. I’ll use both names here as and when I see fit. Hey, it’s my blog.

Milu photographed at Greater Vancouver Zoo by Canuckle, from wikipedia.

The light brown colour of that antler, its large size and somewhat ‘woody’ feel and surface texture are also consistent with this identification, as is the fact that it comes from a collection of English antlers. In recent history, England has been as much the home of this distinctive deer as its native China. I can’t totally exclude the possibility that the antler isn’t from a freak member of another deer species (deer are notoriously plastic in antler development), but I think Pre David’s deer is the most likely identification, and other people who have seen and handled the antler think this too. Well done Dartian, welsh peregrine, Sordes, puppygod, AnimalDoc, larajlcouldwell, PlatypusKimberly and everyone else who identified it as a Pre David’s deer antler.

Late discovery, survival in captivity, salvation by exportation – a curious history

Reconstruction of the Taiwanese E. formosanus, by Tori Morris.

Pre David’s deer has a particularly interesting (and oft-recounted) history (if you share my interests you’ll already be fairly familiar with it). Fossils show that the species previously occurred widely in China (Wu 1991) and also on Japan and in Korea. In addition, five fossil species thought to be part of the same lineage (and conventionally classified as additional species in the genus Elaphurus) have been named from the Late Pliocene and Pleistocene: E. bifurcatus from northern China, E. menziesianus from eastern China, E. akashiensis and E. shikamai from Japan, and E. formosanus from Taiwan [adjacent reconstruction from here on deviantart].

Due to unspecified reasons (but most likely hunting for the supposed aphrodisiac qualities of its antlers), C. davidianus became extinct in the wild about 1000 years ago (though read on), with only a single captive herd at Beijing’s Imperial Hunting Park remaining. Chinese people knew these deer by several names, including Milu (also written Mi-Lou) and Sibuxiang (also written Sze-pu-hsiang and Ssu-pu-hsiang). The latter apparently means something like “unlike the other four”, the “other four” being some combination of cow, deer, horse, donkey, camel and goat. Entrance to the park was forbidden on pain of death (Laidler & Laidler 1992).

The species remained unknown to European until the 1860s when Pre Armand David – perhaps best known today for his discovery of the Giant panda Ailuropoda melanoleuca – learnt of that single captive herd, by then consisting of 34 animals. Heuvelmans (1995) says that David eluded the guards to the park and scaled the wall, thereby making sight of these deer for the first time (other sources say that he found a section of wall that was being repaired, and stood on a pile of bricks to peer over it). He later bribed the guards and managed to obtain a pair of antlers and two skins that he sent back to France; these were described by Henri Milne-Edwards in 1866 as a new species named in his honour.

One of the Duke of Bedford's deer, as figured by Richard Lydekker in 1903.

The Chinese herd then became the victim of misfortunate. In 1894 and/or 1895, flooding from the Han River swept through the hunting park, destroying part of the wall. Some of the deer escaped, but they were eaten by starving local peasants. Deer were also killed during the Boxer Rebellion in 1900 (Laidler & Laidler 1992, Heuvelmans 1995, Nowak 1999). Some sources imply that all of the deer were killed at this time, but it actually seems that the last of them survived at Beijing Zoo until 1922. And while convention has it that the hunting park herd was the only remaining population (that is, that the species was long extinct in the wild), Dobroruka (1970) reported two skins, collected on the island of Hainan (off the southern coast of China) in 1869. If this report is accurate, the species did actually persist in the wild much later than generally thought. Li et al. (2011) recently studied captive Milu herds to see if they still react to the predators they would once have lived alongside, and showed that they seem to respond to the tiger as a potential source of danger. Incidentally, I’m pretty sure that I recall seeing the Milu’s story portrayed in comic strip form on children’s TV during the 1980s - I think in the BBC series Blue Peter. Does anyone else know what I’m talking about?

Anyway, after 1922, the Milu was extinct in China. Fortunately, a number of individuals had been illegally exported to various collections in Europe. The Duke of Bedford became especially interested in this curious deer and, following the purchase of specimens from various collections, ended up with 18 of them. It is 11 of this 18 that formed the ancestral stock for the modern population of c. 2000. People began sending individuals back to China during the 1950s and herds were released into the wild in China during the 1980s. Somewhat surprisingly, inbreeding depression does not (yet) seem severe in these animals (Sternicki et al. 2003).

Fighting Milu stags. Photo by T. Voekler, from wikipedia.

Incidentally, England very nearly had its own feral population of Milu. In 1981, 12 members of a herd kept near Swindon in Wiltshire escaped simultaneously from captivity (Baker 1990). All 12 individuals returned to captivity, apparently of their own accord, but – had they bred – they could very well have established a wild colony. We already know that the Milu is easily hardy enough to survive in the wild in western Europe. Incidentally, the Milu readily produces hybrids with the Red deer C. elaphus, and the hybrids are readily fertile too. However, different breeding seasons mean that the two don’t ordinarily mate on contact, so hybrids have to be produced via artificial insemination (Tate et al. 1997). Hybrids are large (larger than average Red deer) and long-headed [one of these hybrids is shown below].

It looks weird, it acts weird

Pre David’s deer is pretty weird looking. It’s a very large deer with highly pronounced sexual size dimorphism (males are typically about 214 kg while females are more like 150 kg). It has an especially long snout with a superficially cow-like face that appears to be peculiarly flat dorsally (Colin Tudge once described its face as “lugubrious”). Its hooves are especially large and seemingly not well suited for movement on hard ground: one of several features indicating specialisation for life in wet, swampy grassland. Its tail has a tassel at the end and is the longest of any deer. It has a shaggy coat, with long guard hairs being present throughout the year.

Milu stags engaging in parallel marching, their antlers adorned with mud and foliage. Photo by Jon McGowan.

Many aspects of its behaviour, biology and life cycle are odd. Many male deer spray their bodies with urine during the rut in order to make themselves as pungent as possible. Uniquely, Pre David’s deer swings “the penis horizontally from side to side with an upward swing at the end of the traverse” (Geist 1999, p. 102). Males also seem to adorn their antlers with mud and vegetation more than other deer do, and it’s even been suggested that their peculiar antlers are somehow specialised for this sort of decoration (Walton & Hosey 1984). They roar often compared to other deer but various aspects of their dominance displays (especially the parallel marching) are much like those of Red deer and very different from those of the three-pronged Asian deer (axis deer, sambar and kin) they’re sometimes supposed to be closest to. Uniquely for cervine deer, males grow their antlers over the winter, shedding them in December or January. They’re also known to grow two sets of antler in a year, but only when extensive hand-feeding is provided.

Milu box in bipedal pose (note to self: must discuss bipedality in deer some time) and also bite with their fairly large canines. Females fight as well as males. I’m sure you all know that female animals fight (either against other females, or against offending males), but I just wanted to remind you – you sometimes get the impression from nature documentaries that aggression is just for the boys.

The weirdest deer - - the weirdest origin?

Exactly how Pre David’s deer might be related to other deer has been somewhat controversial, as is admittedly usual for aberrant, weird-looking species.

Male Milu, by Lilly M, from wikipedia. Looks weird.

Partly this is because it combines features of various different deer groups. Geist (1999) suggested that Pre David’s deer evolved from early, three-pronged, axis-style deer and that its large size and behavioural and morphological similarities with Red deer and so on were convergences. Pitra et al. (2004) found Pre David’s deer to belong to a lineage that also included Eld’s deer C. eldi. This Eld’s deer + Milu clade was the sister-group to a much larger one that included the majority of other cervine deer (including the many forms of Red deer and Sika, sambars and axis deer).

Cervid phylogeny from Pitra et al. (2004). You should be able to see the Eld's deer + Milu clade near the middle of the diagram. Click to enlarge.

However, because the Milu combines features of Eld’s deer (including adaptation to swampy habitats, weird antlers that lack a bez tine, absence of a rump patch and presence of large canines) with those of more ‘advanced’ cervine deer like Red deer and Wapiti C. canadensis (it adopts a head-down dominance posture, is temperate-adapted, has tines on the beam that are nearly at right angles), it’s something of an anomaly in deer phylogeny. It could be a fairly primitive cervine that has convergently evolved ‘advanced’ characters, presumably as its ancestors moved into temperate climes. But could it be exactly what it looks like – that is, a weird (and self-perpetuating) hybrid between ‘primitive’ and ‘advanced’ cervine deer?

Well, this is exactly what Meijaard & Groves (2004), Pitra et al. (2004) and Groves (2005) have suggested. They think that an Eld’s deer-type maternal parent mated with a Wapiti-type paternal parent some time in the Late Pliocene, and that the Milu lineage is the result. Mitochondrial data puts Pre David’s deer close to Eld’s deer, but studies of its y chromosome have yet to reported, so far as I can tell. According to these authors, it’s now most appropriate to sink Elaphurus into Cervus.

Italian sparrow, by I. Ivanov.

The idea that new species might arise via hybridisation from phylogenetically distinct parental species has become increasingly popular in recent years, mostly as molecular investigations have revealed genetic contributions from different parental ancestors in the genomes of some populations. Among tetrapods, classic examples include certain of the whiptail lizards, but the hybrid origins of Audubon’s warbler Dendroica auduboni (or D. coronata auduboni) and the Italian sparrow Passer italiae are now quite well known. We saw recently that the Wisent or European bison Bison bonasus (or Bos bonasus) might have arisen following hybridisation between members of the bison and aurochs lineages, and the recent discovery that Neanderthals and Denisovans have contributed to the gene pool of Homo sapiens also raises the possibility that our own species emerged after complex hybridisation involving more than two species.

More work is needed before we can be more confident about this hypothesis. It seems odd, but I don’t really see why it can’t be true: we already know that phylogenetically disparate deer lineages can produce fertile hybrids without problem, we know that hybridisation is not rare in the wild (despite what textbooks have taught you about the ‘biological species concept’), we know that those entities we term species can be produced in this way, and we know that Pre David’s deer exhibits a curious mix of features that seemingly ‘belong’ to other lineages.

If this proposal is valid, what might it mean for nomenclature? Elaphurus has mostly been given its own ‘genus’ because it’s morphologically distinctive compared to other deer. The fact that it was potentially created by hybridisation doesn’t negate this; hybrids between distantly related parental taxa often look peculiar and we don’t go around given them distinct new taxonomic names, but I suppose we should if they become self-perpetuating lineages that persist for millions of years. However, the idea that Elaphurus (and Axis, Rucervus and Rusa) should be absorbed into Cervus has become increasingly popular lately due to phylogenetic work (Pitra et al. 2004, Groves 2005).

Milu x Red deer hybrid, from the cover of the issue of Journal of Heredity that included Tate et al. (1997).

And what would a hybrid origin mean for the depiction of cladograms and other evolutionary trees? Should the Milu be shown occupying two different positions on diagrammatic trees, or should we show lineages from the Eld’s deer group and Wapiti group merging to create the Milu lineage? These are just musings that I’m throwing out there for debate – I don’t especially have answers (though do note that cladograms are not generally meant to be evolutionary trees: rather, they’re schematic representations of branching sequences).

I’ve always had a great fondness of Pre David’s deer, and I’ve long been familiar with its interesting back-story, its unusual morphology, and the controversy over its phylogenetic position. But I admit that I had no immediate plans to write about any of this stuff and have only ended up doing so because I happened to be given a box full of antlers about a week ago. I hope you find this very special deer to be as fascinating as I do, and thanks to those of you who had a go at guessing the identity of that unusual antler in the first place. Thanks to Richard Reeves for supplying the antler!

For previous Tet Zoo articles on deer, see...

Refs - -

Baker, S. J. 1990. Escaped exotic mammals in Britain. Mammal Review 20, 75-96.

Dobroruka, L. J. 1970. To the supposed former occurrence of the David’s deer, Elaphurus davidianus Milne Edwards, 1866, in Hainan. Mammalia 34, 162-164.

Geist, V. 1999. Deer of the World. Swan Hill Press, Shrewsbury.

Groves, C. 2005. The genus Cervus in eastern Eurasia. European Journal of Wildlife Research 52, 14-22.

Heuvelmans, B. 1995. On the Track of Unknown Animals. Kegan Paul International, London.

Laidler, K. & Laidler, L. 1992. Pandas: Giants of the Bamboo Forest. BBC Books, London.

Li C, Yang X, Ding Y, Zhang L, Fang H, Tang S, & Jiang Z (2011). Do Pre David's Deer Lose Memories of Their Ancestral Predators? PloS one, 6 (8) PMID: 21887286 [free pdf]

Meijaard, E. & Groves, C. P. 2004. Morphometrical relationships between South-east Asian deer (Cervidae, tribe Cervini): evolutionary and biogeographic implications. Journal of Zoology 263, 179-196.

Nowak, R. M. 1999. Walker’s Mammals of the World, Sixth Edition. The Johns Hopkins University Press, Baltimore and London.

Sternicki, T., Szablewski, P. & Szwaczkowski, T. 2003. Inbreeding effects on lifetime in David’s deer (Elaphurus davidianus, Milne Edwards 1866) population. Journal of Applied Genetics 44, 175-183.

Pitra, C., Fickel, J., Meijaard, E. & Groves, P. C. 2004. Evolution and phylogeny of old world deer. Molecular Phylogenetics and Evolution 33, 880-895.

Tate, M. L., Goosen, G. J., Patene, H., Pearse, A. J., McEwan, K. M. & Fennessy, P. F. 1997. Genetic analysis of Pre David’s x Red deer interspecies hybrids. The Journal of Heredity 88, 361-365.

Walton, R. A. & Hosey, G. R. 1984. Observations on social interactions in captive Pre David’s deer (Elaphurus davidianus). Applied Animal Ethology 11, 211-215.

Wu, J.-y. 1991. The ungulates of northern China. Rangifer 14, 57-64.