The puzzle of passive lingual protrusion in ruminants, part 3: explanation via a new hypothesis

...continued from https://www.inaturalist.org/journal/milewski/90158-the-puzzle-of-passive-lingual-protrusion-in-ruminants-part-2-deer-cervidae#

DISCUSSION

This preliminary investigation has emphasised how important search-images are. It is easy to overlook a whole syndrome, unless one knows what to look for.

I began with an apparently trivial impression that impalas are peculiarly inclined to protrude the tongue, in what seems to be a gratuitous way.

However, the puzzle has shifted and grown, in view of similar protrusion in various bovids, antilocaprids, and cervids.

The following footages of Odocoileus virginianus and Odocoileus hemionus show that the tongue remains protruded for seconds at a time, rather than merely being flicked in and out (https://mashable.com/video/deer-phil-collins-mashup and https://www.facebook.com/watch/?v=871447976548484).

Now, the main questions seem to be:

• why is it that pigmentation of the tongue is apparent only in bovids, antilocaprids, and giraffids, and not in cervids?
• why is the tongue so dark-pigmented in impalas, given that one of their peculiarities is that they do not extend the tongue in either foraging or grooming? and
• what is the possible chemosensory function of lingual protrusion in ruminants?

What follows is my attempt to answer the last - and by far the most important - of the above questions.

A NEW HYPOTHESIS OF VOMERONASAL OLFACTION IN RUMINANTS, BEYOND FLEHMEN

Olfaction, normally called a sense of smell, is performed by two different organs in vertebrates.

One is nasal (in the nose), and the other buccal (in the mouth).

In the first, air is breathed/sniffed into the nose, and chemical substances are perceived in a nasal epithelium (https://en.wikipedia.org/wiki/Olfactory_system).

In the second, chemical substances are drawn into the mouth by various actions, and perceived by means of a vomeronasal organ (https://en.wikipedia.org/wiki/Vomeronasal_organ and https://www.britannica.com/science/Jacobsons-organ and https://www.jstor.org/stable/2407844 and https://www.mdpi.com/2813-0545/2/4/31 and https://pubmed.ncbi.nlm.nih.gov/6439595/ and https://www.frontiersin.org/articles/10.3389/fnana.2011.00003/full).

It is the 'various actions' that have confused zoologists, to the degree that a whole syndrome in ruminants may have been overlooked.

There are at least two ways in which chemical substances are brought to the vomeronasal organ on the roof of the mouth, viz.

• by expressionless application of the retracted tongue to the vomeronasal organ, after protruding the tongue with the mouth nearly closed, and
• by means of 'flehmen' expressions, which differ among ungulates, felids, and canids, but always involve conspicuous retraction of the nostrils and opening of the lips/whole mouth (https://www.alamy.com/stock-photo-a-close-up-of-an-impala-flehming-etosha-national-park-etosha-namibia-49630687.html?imageid=AB2AA777-C474-46E0-B87E-70907E67D788&p=167660&pn=1&searchId=4f54d58eadfb521d0bf75b52c08479cb&searchtype=0).

The first is the 'primitive' way, familiar in reptiles, particularly lizards:
the tongue is protruded to pick up chemical substances from the air, which are then sensed vomeronasally, not nasally (https://www.youtube.com/watch?v=-n7z8ZRL4ZU and https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1439-0310.1979.tb00672.x#:~:text=Many%20lizards%20and%20all%20snakes,and%20possibly%20other%20environmental%20factors. and https://www.youtube.com/shorts/OLkiiuVjos8).

The second is the way familiar in mammals, including most ruminants (see https://www.inaturalist.org/posts/87240-flehmen-is-an-exaggeration-in-elephants-while-underplaying-the-reality-of-their-vomeronasal-dexterity#). 'Flehmen' is a 'derived', evolutionarily advanced way.

However, what has been lacking among zoologists, until recently, is a search-image for the first way, in 'evolutionarily residual' form, among mammals.

Flehmen has proved so distracting that few have investigated whether the inconspicuous way has been retained in mammals. I refer to lingual protrusion and retraction in the absence of any particular facial expression,

It is now known that vomeronasal chemoperception, without flehmen, does indeed occur in at least two genera of didelphid marsupials, viz. Monodelphis and Didelphis (https://www.sciencedirect.com/science/article/abs/pii/003193849390275K and https://pubmed.ncbi.nlm.nih.gov/9880164/#:~:text=The%20opossum%20Monodelphis%20domestica%20possesses,a%20stereotypical%20%22nuzzling%22%20behavior. and https://nutritionandmetabolism.biomedcentral.com/articles/10.1186/1743-7075-2-6 and https://psycnet.apa.org/record/1996-04855-006 and https://link.springer.com/article/10.1007/s10914-005-5731-5 and https://pubmed.ncbi.nlm.nih.gov/9880164/ and https://nutritionandmetabolism.biomedcentral.com/articles/10.1186/1743-7075-2-6 and https://animaldiversity.org/accounts/Didelphidae/).

Is it possible, then, that lizard-like vomeronasal function occurs also in certain evolutionarily advanced, eutherian mammals?

I hypothesise that the passive lingual protrusion documented in this series of Posts is indeed evidence of 'primitive' vomeronasal function in higher mammals.

But why ruminants, in particular?

Ruminants, by definition, regurgitate food habitually. This affects the chemosensory organs in both nose and mouth in ways that seem not to have been fully considered.

Rumination has various energetic and nutritional advantages, and also has an anti-predatory advantage in allowing the animals to concentrate their chewing into periods of potentially enhanced vigilance. However, by the same token, vigilance is compromised by rumination, particularly w.r.t. anti-predator olfaction.

Cud-chewing means that the intense, microbially generated odours of the rumen contents 'fill the head' during the bouts of rumination. This would tend to overwhelm normal olfaction, with the following potential consequences:

• during rumination, olfactory vigilance is effectively precluded, making ruminants reliant on visual and auditory vigilance,
• this visual and auditory reliance would explain the evolution of buccal and auditory semets for social/gregarious vigilance during rumination (https://www.inaturalist.org/posts/70156-subtle-diversification-of-buccal-semets-in-tragelaphin-antelopes-part-2# and https://www.inaturalist.org/posts/55694-ten-best-illustrations-of-auricular-semets-in-deer# and https://www.inaturalist.org/posts/55639-auricular-semets-in-alces-and-odocoileus-but-not-other-odocoileine-deer# and https://www.inaturalist.org/journal/milewski/89674-bleezes-flags-and-semets-in-the-adaptive-colouration-of-impalas-aepyceros-part-2#),
• there may be some compensation for the 'odorific saturation' associated with cud-chewing, by means of a partial reversion to chemosensory perception via the tongue and vomeronasal organ,
• the tongue and vomeronasal organ can be washed of ruminal odour by means of saliva, more immediately than the clearing of the nasal mucosa, and
• passive lingual protrusion, for the purpose of vomeronasal chemoperception, may occur particularly in the periods immediately after bouts of rumination, when the odours of the cud are still being cleared from the nasal olfactory organ.

Posted on February 24, 2024 04:09 PM by milewski