I really must get this series on pouches, sacs and pockets finished. Last time, we looked at baleen whales (and then I got distracted by Caperea): in these animals, a large, inflatable laryngeal sac is used in producing loud, resonating noises (though roles in gas storage or the mechanics of exhalation have also been suggested).
During the rut, males adopt a characteristic posture where the head and neck are kept low and the throat is extended [shown here, from Frey et al. (2007)]. Because the air sac is seen to inflate and deflate as the deer calls, an acoustic role for the sac is obvious (the noises made by calling reindeer are difficult to describe: they make hoarse, repetitive guttural noises).
Exactly what effect the throat sac has on the sounds generated in the larynx is unclear. One suggestion is that the sac augments the acoustic output of the vocal tract, such that the resulting noise combines output from the mouth and nose with output from the sac, emitted via the soft tissues of the neck. In other words, the sac ‘filters’ the sounds produced in the vocal tract (in acoustics, a filter is “a resonator that absorbs energy at certain resonance frequencies” (Freyet al. 2007, p. 151)). Because displaying males approach females broad-side in what’s been called a ‘broadside acoustic display’, it appears likely that the sounds generated by these deer mostly emanate sideways.
Other acts of acoustic weirdness in Cervidae
The evolution of this remarkable laryngeal structure is made all the more, err, remarkable by the fact that it’s (so far as we know) completely novel within Cervidae, this despite the fact that other deer lineages have evolved profound modifications to enhance their calls [calling male Red deer shown below, image by Bill Ebbesen, from wikipedia. That lump in the throat corresponds to a highly mobile larynx that descends way down in the neck during vocalisation. Read on].
As we’ve seen before, Red deer Cervus elaphus and Fallow deer Dama dama use laryngeal retractors and an elastic thyrohyoid linkage to pull the larynx down toward the chest and thereby decrease the formant frequencies of their calls (Fitch & Reby 2001, McElligott et al. 2006) (and formant frequencies are known to correlate with female preference and mating success in both Red and Fallow deer: see Charlton et al. (2007), Vannoni & McElligott (2008) and Reby et al. (2010). Incidentally, it’s probably true to say – as some have – that the vocal behaviour of Red deer has been more studied than that of any other mammal outside of Primates). Wapiti C. canadensis retract the larynx markedly as well (and I follow Geist (1999) and Groves (2005) in regarding the Wapiti as a separate species from Red deer*). Phylogenies show that Red deer and Wapiti belong to a disparate lineage relative to Fallow deer (e.g., Pitra et al. 2004): even if Cervus and Dama are sister-taxa, there are still numerous taxa in the Cervus clade that lack the laryngeal structures seen in the C. elaphus + C. canadensis clade, and seen in D. dama. Their similar laryngeal anatomies must therefore have evolved convergently.
* Some other deer traditionally included in C. elephus also deserve to be recognised as separate species: I will avoid discussing this mess for now and point the interested reader to Pitra et al. (2004) and Groves (2005).
Similar elastic structures are absent in reindeer: there’s no indication that they can move the larynx in the same way.
Peculiar noises are also made by some other large deer, but in this case I’m not talking about vocal noises; White-lipped deer Przewalskium albirostre, Père David’s deer Elaphurus davidianus, Red deer, Wapiti and Reindeer all produce clicking or cracking noises in their joints as they walk (McCullough 1969, Thomas & Toweill 1982, Geist 1999). Red deer only seem to produce the cracking noise in the forelimbs, while Reindeer at least produce cracking in both fore- and hindlimbs.
We looked some time ago at joint-clicking in eland: remarkably, the noises made by the joints of these antelopes form part of their dominance displays (Bro-Jørgsen & Dabelsteen 2008). Could the same be true of the joint-clicking deer? A popular idea is that the clicking noises provide information on the whereabouts of other herd members, and also on the approach of possible danger. I don’t know if anyone has studied this (though humans who hunt deer have certainly been very interested in it) – let me know.
One more interesting thing to note on deer and acoustics: it has been suggested that the enormous palmate antlers of Moose Alces alces may work as parabolic reflectors that help collect sound (Bubenik & Bubenik 2008) [spectacular Alaskan moose shown below; photo by Donna Dewhurst, from wikipedia. Note the profound asymmetry in the antlers… fluctuating asymmetry, another subject I must cover some time].
Moose ears are large and sensitive, but these authors showed that a moose can increase the acoustic pressure in its ears by about 19% if it points the ears towards the antlers rather than toward the sound source. I would assume that this effect is incidental given that the antlers are still shed annually, mostly play a role in sexual combat and display, and are absent in females (one would assume that they would be retained year-round, and be present in females, if an acoustic role provided a selective advantage). However, moose that inhabit Alaskan tundra environments have the biggest antlers, and this is a habitat where sound travels furthest. Then again, visual signals would also travel furthest, so – as usual – things are not clear-cut.
Reindeer are ‘grotesque giants’
Having shown that Reindeer are unexpectedly weird by virtue of their laryngeal sacs, it’s only right to say that they’re really interesting for lots of other reasons: with their elaborate antlers (proportionally, the biggest of any deer), cursorial specialisations, large body size (second largest New World deer), long neck manes, large fat stores and highly peculiar, complex pigmentation (they have capes, rump patches, lateral stripes, forehead patches, eye rings and ‘socks’*), they’re flamboyant animals that can be regarded as ‘extreme’ members of their group (incidentally, the neck mane might be a visual signal linked to the neck sac) [Rangifer and Alces are shown in the diagram below as extreme members of the mostly New World deer clade that includes brockets, roe deer, reindeer and moose (from Geist (1999))].
Geist (1999) referred to animals of this sort as ‘grotesque giants’ and noted that they tend to have evolved in cold, harsh Ice Age environments. Gould used the term ‘asynchronous hypermorphs’ for the same set of species. Other examples – according to Geist – include moose, wapiti, muskox, woolly rhinos, short-faced bears and humans.
* Pigmentation patterns are highly variable in reindeer, with some forms being far more elaborately patterned than others. Eurasian tundra reindeer are the most elaborate.
More laryngeal bullae than you can shake a stick at
So far in this series of articles, we’ve looked at primates, baleen whales and reindeer. But these are far from the only mammals with laryngeal diverticula located on the midline of the throat: small sac-like structures located on the ventral surface are also present in opossums (Didelphis), quolls (Dasyurus), some phalangers (Trichosurusand Phalanger), swamp wallabies (Wallabia), hedgehogs (Erinaceus), squirrels (Sciurus), marmots (Marmota), water voles (Arvicola), tapirs (Tapirus), horses (Equus), boar (Sus), eland (Tragelaphus), saiga (Saiga), takin (Budorcas), some bears (Ursus), wolves (Canis lupus), southern sea lions (Otaria) and various others (see Frey et al. (2007) for a complete list: their table, with adjacent diagrams showing laryngeal diverticula position, is shown here).
In some taxa, these structures are associated with enlarged hyoid bullae (like those looked at previously in apes and howler monkeys), but in others they are not. And in some of these mammals, these diverticula are paired; in others they are single. In the marsupials with a laryngeal diverticulum, and also in eland, saiga and takin, the structures are housed inside an inflated bulla formed from the thyroid cartilage (and are thus contained within the larynx). As yet, the role that these many diverticula might play in vocalising and other aspects of behaviour has been little investigated for most of the species concerned. Roland Frey and his colleagues have, however, been publishing some great studies on the laryngeal anatomy and vocalisation in such species as muskox, takin and weird gazelles. More soon!
For the previous articles on pouches, pockets and sacs in mammal heads, necks and chests, see…
And for previous Tet Zoo articles on deer, see…
Refs – –
Bro-Jørgsen, J. & Dabelsteen, T. 2008. Knee-clicks and visual traits indicate fighting ability in eland antelopes: multiple messages and back-up signals. BMC Biology 2008, 6: 47 doi:10.1186/1741-7007-6-47
Bubenik, G. A. & Bubenik, P. G. 2008. Palmated antlers of moose may serve as a parabolic reflector of sounds. European Journal of Wildlife Research 54, 533-535.
Charlton, B., Reby, D. & McComb, K. 2007. Female red deer prefer the roars of larger males.Biology Letters 3, 382-385.
Fitch, W. T. & Reby, D. 2001. The descended larynx is not uniquely human. Proceedings of the Royal Society of London B 268, 1669-1675.
Frey, R., Gebler, A., Fritsch, G., Nygrén, K., & Weissengruber, G. E. (2007). Nordic rattle – the hoarse phonation and the inflatable laryngeal air sac of reindeer (Rangifer tarandus)Journal of Anatomy, 210, 131-159
Geist, V. 1999. Deer of the World. Swan Hill Press, Shrewsbury.
Groves, C. 2005. The genus Cervus in eastern Eurasia. European Journal of Wildlife Research52, 14-22.
McCullough, D. R. 1969. The Tule Elk. Its History, Behavior and Ecology. University of California Press, Berkeley.
McElligott, A. G., Birrer, M. & Vannoni, E. 2006. Retraction of the mobile descended larynx during groaning enables fallow bucks (Dama dama) to lower their formant frequencies.Journal of Zoology 270, 340-345.
Pitra, C., Fickel, J., Meijaard, E. & Groves, C. 2004. Evolution and phylogeny of old world deer. Molecular Phylogenetics and Evolution 33, 880-895.
Reby, D., Charlton, B., Locatelli, Y. & McComb K. 2010. Oestrous red deer hinds prefer male roars with higher fundamental frequencies. Proceedings of the Royal Society of London B 277, 2747-2753.
Thomas, D. C. & Toweill, D. E. 1982. The Elk of North America; Ecology and Management. Stackpole Books, Harrisburg, PA.
Vannoni, E. & McElligott, A. G. 2008. Low frequency groans indicate larger and more dominant Fallow deer (Dama dama) males. PLoS ONE 3(9): e3113. doi:10.1371/journal.pone.0003113
Hornorkesteret 