Why have two coexisting bovids, the sable antelope (Hippotragus niger) and Lichtenstein's hartebeest (Alcelaphus lichtensteini), diverged in vomeronasal (flehmen) expression?

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The sable antelope (Hippotragus niger, https://www.inaturalist.org/taxa/42334-Hippotragus-niger) and Lichtenstein's hartebeest (https://en.wikipedia.org/wiki/Lichtenstein%27s_hartebeest and https://www.inaturalist.org/observations?taxon_id=132659) are sympatric and biologically comparable.

Both species are

• gregarious bovids (https://en.wikipedia.org/wiki/Bovidae),
• of similar body size (about 150-200 kg),
• approximately restricted to the miombo biome (https://en.wikipedia.org/wiki/Miombo),
• specialised on a diet of grasses growing on nutrient-poor soils, and
• less sexually dimorphic (e.g. with horns present in both sexes) than expected for gregarious, polygynous ruminants.

However, the sable antelope and Lichtenstein's hartebeest differ remarkably in their facial expressiveness when using the vomeronasal organ (https://en.wikipedia.org/wiki/Vomeronasal_organ# and https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6050168/) for intraspecific communication.

Various mammals exhibit a facial expression called 'flehmen' (https://en.wikipedia.org/wiki/Flehmen_response) when 'sniffing' for hormones/pheromones and other substances of sociosexual significance. In many cases, this is done by paying attention to the urine of conspecifics, and in some cases the urine is taken in liquid form into the mouth, before flehmen is expressed.

In ungulates, flehmen is an expression in which

• the muzzle is lifted and the jaws open wide enough to inhale slowly by mouth,
• the nose is retracted, at least partly closing the external nares, https://en.wikipedia.org/wiki/Nostril),
• the upper lips are fully raised,
• the tongue is withdrawn.

(Note that flehmen does not involve any action of the tongue-tip in touching a surface/material of interest and then placing the tongue-tip at the location of the vomeronasal organ on the roof of the mouth. Please see https://www.inaturalist.org/journal/milewski/87240-flehmen-is-an-exaggeration-in-elephants-but-it-underplays-the-reality-of-vomeronasal-function-in-proboscideans#)

This expression seems to aid the passage of hormones/pheromones to the vomeronasal organ via the roof of the mouth, while simultaneously reducing the distraction of normal olfaction, by reducing nasal inhalation.

Flehmen can thus be thought of as an expression facilitating 'smell' by means of the mouth, or a deliberate and fine-tuned 'tasting of the air'.

This expression occurs in adult males of about 86% of all ungulates (https://en.wikipedia.org/wiki/Ungulate and https://www.ultimateungulate.com/Ungulates.html#:~:text=Did%20you%20know%3F,more%20are%20on%20the%20brink.).

Flehmen is most commonly seen when males monitor the urine of females for oestrus (https://en.wikipedia.org/wiki/Estrous_cycle).

However, our two species are remarkably deviant from the norm, in opposite ways.

In the case of the sable antelope, what is odd is that flehmen is expressed by not only males but also

• females,
• juveniles, and
• even infants (https://repository.si.edu/bitstream/handle/10088/11676/Thompson1995a.pdf?sequence=1&isAllowed=y and https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1439-0310.1995.tb00359.x and page 117 in Estes 1991, https://books.google.com.au/books/about/The_Behavior_Guide_to_African_Mammals.html?id=jUm7QgAACAAJ&redir_esc=y).

In the case of Lichtenstein's hartebeest, what is odd is that no flehmen expression has ever been observed at all, even in mature males.

What this means is that the sable antelope has boosted flehmen to its maximal incidence among all ungulates, whereas Lichtenstein's hartebeest - like all members of the genera Alcelaphus and Damaliscus - seems to have downplayed this expression to the point of losing it completely.

Indeed, in Alcelaphus and Damaliscus, males seem to take no interest in the urine of females (please see https://pubmed.ncbi.nlm.nih.gov/3368534/).

On page 126, Estes (1991) states of the sable antelope:
"Bulls accompanying a herd routinely urine-test all females...Other cows and even young calves also perform the urine test very frequently, unlike other ungulates." (This applies also to Hippotragus equinus, page 117.)

The following show flehmen in mature males of the sable antelope:

https://www.alamy.com/stock-photo-sable-antelope-ram-in-flehmen-21736175.html

https://www.sciencephoto.com/media/1254316/view/sable-antelope-herd

https://www.google.com.au/search?q=Sable+antelope+courting&sca_esv=586929607&sxsrf=AM9HkKluPU2epZ-HheCpkS7Vimqar52VmQ%3A1701426661462&source=hp&ei=5bVpZZPOGZPe2roPsfe_uAc&iflsig=AO6bgOgAAAAAZWnD9RYRJZSUnci1gjJybd4Is_hjsruu&ved=0ahUKEwjT1I-ehO6CAxUTr1YBHbH7D3cQ4dUDCAw&uact=5&oq=Sable+antelope+courting&gs_lp=Egdnd3Mtd2l6IhdTYWJsZSBhbnRlbG9wZSBjb3VydGluZzIIEAAYgAQYogQyCBAAGIAEGKIEMggQABiABBiiBDIIEAAYgAQYogRIsK4BUJgVWIGqAXADeACQAQGYAeICoAGIRKoBCDAuNC4yOC40uAEDyAEA-AEBqAIKwgIHECMY6gIYJ8ICBxAuGOoCGCfCAgQQIxgnwgIREAAYgAQYigUYkQIYsQMYgwHCAg4QABiABBiKBRixAxiDAcICDhAuGIAEGIoFGLEDGIMBwgIREC4YgAQYsQMYgwEYxwEY0QPCAgsQABiABBixAxiDAcICCxAuGIAEGIoFGJECwgIIEC4YgAQYsQPCAg4QLhiDARixAxiABBiKBcICERAuGIMBGMcBGLEDGNEDGIAEwgIFEAAYgATCAhEQLhiABBiKBRixAxiDARjUAsICFBAuGIAEGIoFGJECGLEDGIMBGNQCwgIREAAYgAQYigUYkQIYsQMYyQPCAgsQABiABBiKBRiSA8ICCBAAGIAEGLEDwgILEC4YgAQYsQMYgwHCAhQQLhiDARiRAhjUAhixAxiABBiKBcICCxAuGIMBGLEDGIAEwgIFEC4YgATCAgcQABiABBgKwgIGEAAYFhgewgIIEAAYFhgeGA_CAggQLhgWGB4YCsICCBAAGBYYHhgKwgIKEAAYFhgeGA8YCsICCxAAGIAEGIoFGIYDwgIFECEYoAHCAgcQIxiwAhgnwgIHEC4YDRiABMICBxAAGIAEGA3CAgYQABgeGA3CAggQABgIGB4YDcICChAAGAUYHhgNGA_CAgQQABgewgIIEAAYBRgeGA_CAgYQABgIGB7CAggQABgIGB4YCsICBBAhGBXCAgcQIRigARgKwgIEECEYCg&sclient=gws-wiz#fpstate=ive&vld=cid:562796a8,vid:lKJZQKCNvdY,st:0

https://www.google.com.au/search?q=Sable+antelope+courting&sca_esv=586929607&sxsrf=AM9HkKluPU2epZ-HheCpkS7Vimqar52VmQ%3A1701426661462&source=hp&ei=5bVpZZPOGZPe2roPsfe_uAc&iflsig=AO6bgOgAAAAAZWnD9RYRJZSUnci1gjJybd4Is_hjsruu&ved=0ahUKEwjT1I-ehO6CAxUTr1YBHbH7D3cQ4dUDCAw&uact=5&oq=Sable+antelope+courting&gs_lp=Egdnd3Mtd2l6IhdTYWJsZSBhbnRlbG9wZSBjb3VydGluZzIIEAAYgAQYogQyCBAAGIAEGKIEMggQABiABBiiBDIIEAAYgAQYogRIsK4BUJgVWIGqAXADeACQAQGYAeICoAGIRKoBCDAuNC4yOC40uAEDyAEA-AEBqAIKwgIHECMY6gIYJ8ICBxAuGOoCGCfCAgQQIxgnwgIREAAYgAQYigUYkQIYsQMYgwHCAg4QABiABBiKBRixAxiDAcICDhAuGIAEGIoFGLEDGIMBwgIREC4YgAQYsQMYgwEYxwEY0QPCAgsQABiABBixAxiDAcICCxAuGIAEGIoFGJECwgIIEC4YgAQYsQPCAg4QLhiDARixAxiABBiKBcICERAuGIMBGMcBGLEDGNEDGIAEwgIFEAAYgATCAhEQLhiABBiKBRixAxiDARjUAsICFBAuGIAEGIoFGJECGLEDGIMBGNQCwgIREAAYgAQYigUYkQIYsQMYyQPCAgsQABiABBiKBRiSA8ICCBAAGIAEGLEDwgILEC4YgAQYsQMYgwHCAhQQLhiDARiRAhjUAhixAxiABBiKBcICCxAuGIMBGLEDGIAEwgIFEC4YgATCAgcQABiABBgKwgIGEAAYFhgewgIIEAAYFhgeGA_CAggQLhgWGB4YCsICCBAAGBYYHhgKwgIKEAAYFhgeGA8YCsICCxAAGIAEGIoFGIYDwgIFECEYoAHCAgcQIxiwAhgnwgIHEC4YDRiABMICBxAAGIAEGA3CAgYQABgeGA3CAggQABgIGB4YDcICChAAGAUYHhgNGA_CAgQQABgewgIIEAAYBRgeGA_CAgYQABgIGB7CAggQABgIGB4YCsICBBAhGBXCAgcQIRigARgKwgIEECEYCg&sclient=gws-wiz#fpstate=ive&vld=cid:7d6fc8a2,vid:2rdGZ5ntfYo,st:0

On page 138, Estes (1991) states:
"Antelopes of the genera Alcelaphus and Damaliscus are the only bovids so far known that do not urine-test females (i.e., sample the urine, then curl the lip and/or open the mouth in the flehmen grimace). Yet they have an apparently functional vomeronasal organ. How do they find out when a cow is coming into heat?"

I have found no relevant depictions of Lichtenstein's hartebeest. This is unsurprising, because there is no behaviour drawing the attention of photographers.

However, the following shows how males of a congener sniff the posterior of females, with the mouth closed:
https://www.superstock.com/asset/red-hartebeest-alcelaphus-buselaphus-male-following-female-mountain-zebra-national/1890-175253

INTERPRETATION

Can any reader explain the extreme incidence of flehmen in the sable antelope, vs its absence in Lichtenstein's hartebeest?

Possible clues include the following:

The genus Hippotragus, including the sable antelope, is extreme among ruminants in its sociosexual behaviour.

The relevant syndrome comprises a confusing combination of facets, including:

• intimidating horns (designed for harm rather than ornamentation and ritual), present in both sexes and relatively precocial,
• minimisation of skin-contact among individuals, with no mutual grooming and minimal maternal grooming,
• female emulation of masculine self-advertisement and assertiveness,
• conspicuous dark/pale contrast on the face, suggesting 'warning colouration',
• loose bonding between infants and mothers, and
• delayed expulsion of adolescent males from the group.

Please also see:
https://www.sciencedirect.com/science/article/abs/pii/016815919190241O
https://psycnet.apa.org/record/1991-26644-001
https://www.sciencedirect.com/science/article/abs/pii/S0003347285702618

When this syndrome is sufficiently understood, could the emphasis on flehmen emerge as somehow compatible/complementary/compensatory with the other facets?

For its part, Lichtenstein's hartebeest is not 'opposite' or 'converse' to the sable antelope, because it too is relatively sexually monomorphic among ruminants.

However, the main peculiarities of Alcelaphus are in anatomy, including

• elevated withers (http://www.africaimagelibrary.com/media/dac8a16c-4daf-4029-a23b-1399c0203fef-lichtenstein-s-hartebeest-alcelaphus-lichtensteini-kafue-nati),
• a narrow, elongated muzzle (particularly the nasal bones, https://www.taxidermyjungle.co.uk/product/taxidermy-hartebeest-skull-by-edward-gerrard/ and https://www.dreamstime.com/stock-photo-hunting-trophy-hartebeest-african-safari-skull-zambia-hanging-wall-image55206249), and
• a tight gape, in which the mouth can be opened to such a limited extent as to preclude the biting off of any food item by means of the premolars.

These anatomical features are consistent with extreme cursoriality (speed and endurance in running), and specialisation for selectively grazing relatively short grasses by taking bites that are not only small, but obligatorily so.

This suggests that flehmen has been lost in Alcelaphus (and Damaliscus) partly because this expression is constrained by the exceptional 'tightness' of the mouth.

Wildebeests (Connochaetes) have faces as elongated as those of other alcelaphins, but do show the flehmen expression (https://www.flickr.com/photos/willievs/6688231029 and https://upload.wikimedia.org/wikipedia/commons/8/8f/Day_27_Blue_Wildebeest_%28Connochaetes_taurinus%29_in_%22flehmen%22_behavior_..._%2853263592042%29.jpg).

This is perhaps explained by the fact that the muzzle is broader in wildebeests than in other alcelaphins, allowing enough flexibility for an 'eversion' of the upper lip that may be constrained in Lichtenstein's hartebeest.

The only ungulates, as far as I know, that rival alcelaphins in the tightness of the gape are giraffes (Giraffa). However, giraffes, unlike Lichtenstein's hartebeest, show flehmen (https://www.mdpi.com/2076-2615/13/3/354).

This is perhaps explained by the length and flexibility of the upper lip (https://www.alamy.com/stock-photo-network-giraffe-giraffa-camelopardalis-reticulata-mouth-medium-close-123022996.html?imageid=A2C6F341-234A-4E90-BE61-4D80D09DD187&p=75502&pn=1&searchId=93599c4de3243ce8afad2bbc76259296&searchtype=0 and https://www.alamy.com/giraffe-licking-a-pole-close-up-of-a-giraffe-giraffa-camelopardalis-licking-a-wooden-pole-giraffes-have-specially-adapted-lips-and-a-prehensile-h-image212450119.html?imageid=98C0297C-DE45-4087-86E4-70065AAFA3C9&p=167000&pn=1&searchId=93599c4de3243ce8afad2bbc76259296&searchtype=0).

The upper lip of giraffes is, together with the tongue, adapted for the selection of shoots on trees and shrubs (https://stories.sandiegozoo.org/2018/06/14/we-have-lip-up/ and https://www.naturepl.com/stock-photo-south-african-giraffe-giraffa-camelopardalis-giraffa-exhibiting-nature-image01515042.html and https://www.flickr.com/photos/fwooper7/15389557385 and https://twitter.com/blankparkzoo/status/1012701100686770178).

The difference in the width and flexibility of the gape between hippotragin and alcelaphin bovids is evident when the animals are fleeing:

• in the former, the mouth sometimes noticeably opens, presumably in order to breathe as rapidly as possible (https://www.alamy.com/stock-photo-gemsbok-antelope-oryx-gazella-running-kalahari-desert-south-africa-55200475.html and https://www.kimballstock.com/preview.asp?db=a&image=AFW+29+MH0019+01 and https://www.vecteezy.com/photo/706299-running-gemsbok-antelope and https://www.pinterest.com.au/pin/antlers-vs-horns--542683823834285982/ and https://www.shutterstock.com/image-photo/oryx-calf-running-jumping-green-field-1505844341 and https://www.dreamstime.com/herd-beautiful-very-secretive-roan-antelope-herd-beautiful-very-secretive-roan-antelope-running-image125214407), whereas
• in the latter, I have yet to see evidence that the mouth opens even in duress while running.

Posted on December 1, 2023 05:44 AM by milewski