Bold black-and-white in females of the southern sable antelope (Hippotragus niger niger): anti-predator warning or maternal emulation of masculinity?

For naturalists, a central puzzle of the southern sable antelope (Hippotragus niger niger) is why its fully mature females combine

  • thoroughly conspicuous colouration (on face as well as rest of figure) with
  • lethal-looking horns (sharp-pointed, and straight enough to be deployed forwards, but curved enough to be deployed against a predator on its back).

https://www.alamy.com/sable-antelope-hippotragus-niger-portrait-captive-cabarceno-park-cantabria-spain-june-image262989224.html?imageid=A8BB990A-0226-4A95-8C03-501FFAEAB05D&p=215497&pn=1&searchId=0452b29cb4460d2129648a818706996d&searchtype=0

https://www.alamy.com/sable-antelope-image472069428.html?imageid=63E4EF4B-C67D-4279-8ADA-838EB08A6134&p=1879136&pn=6&searchId=29384e0433d380722fb68e25119a69b6&searchtype=0

https://howieswildlifeimages.files.wordpress.com/2013/05/chobe-1-6_may131413.jpg

https://howieswildlifeimages.files.wordpress.com/2013/05/chobe-1-6_may1313901.jpg

The sable antelope is one of the few spp. of ruminants - a clade that comprises hundreds of spp. on various continents - that shows this combination.

(Two caveats: this applies only to the nominate subspecies of the sable antelope, and to fully mature females. In this Post I refer particularly to the subspecies Hippotragus niger niger, and to individual females older than eight years (https://www.inaturalist.org/posts/85930-hippotragus-niger-niger). However, for conciseness I will just call these 'sable antelope' and 'females'.)

At first glance, the pattern in question suggests aposematism (https://en.wikipedia.org/wiki/Aposematism), which by definition is warning colouration vs predators.

However, aposematic colouration seems far-fetched in ungulates, which rely on vigilance and fleeing as their main anti-predatory strategy.

Furthermore, this explanation would fail scrutiny in the following ways:

  • there is limited evidence that the sable antelope is apt to defend itself from predators by means of its horns, thus undermining the explanatory power of aposematism;
  • aposematism typically applies to non-apparent anti-predator defences (e.g. the venom-glands of skunks), whereas the horns of antelopes are fully apparent;
  • the colouration and horns of females emulate those of males - in which the configuration of horns and colouration are more parsimoniously explained intraspecifically, w.r.t. masculine rivalry; and
  • the sable antelope does not show particularly strong maternal protection of infants and small juveniles, which tend to lag behind their mothers at a most vulnerable time of their lives.

A subsidiary puzzle, which overlaps in the conceptual framework with the main puzzle stated above, is as follows.

There are many bovids (https://en.wikipedia.org/wiki/Bovidae) in which females resemble males, in possessing horns, in being maned and/or bearded, and in having similar colouration between the sexes.

However, in most of these, males are not immediately apparent as such, i.e. there is minimal sexual dimorphism in body size and horn size and form.

In the sable antelope, mature males differ enough from females to be easily recognisable. This is because mature males have

The implication is that the appearance and armaments of females may be emulations of masculinity. This seems as plausible as any explanation invoking anti-predator adaptations.

According to Richard Estes (https://www.sciencedirect.com/science/article/abs/pii/016815919190264X), the emulation of male appearance by female bovids may be explained by the fact that there is sexual non-segregation, throughout the year, in the spp. concerned. Territorial males would tend to ostracise male offspring at the adolescent stage. However, it is in the mothers' interests to keep their adolescent sons in the protection of the group for as long as possible.

Hence - by implication from Estes' hypothesis - females have evolved to match mature males in armaments (horns) and masculine appearance, so that they can protect the adolescents from ostracism for as long as possible.

Estes' explanation seems satisfactory for most lineages of 'plains game' in which there is so little sexual dimorphism that males can be hard to distinguish from females in the field. I refer particularly to wildebeests (https://www.inaturalist.org/observations?place_id=any&taxon_id=42279&view=species) and other alcelaphins, as well as oryxes (https://www.inaturalist.org/observations?place_id=any&taxon_id=42307&view=species).

However, this does not fully explain the odd combination of features in the sable antelope. What remains to be explained are that

  • sexual dimorphism remains great enough that, to the human eye, mature males are easily distinguished (by horn length and the black penis-marker) from mature females,
  • masculine colouration is boldly black-and-white,
  • the colouration of mature females matches the masculine boldness,
  • the horns of females are more credibly intimidating than those of alcelaphins or even oryxes, and
  • there is a particular pattern of what looks like 'badger-like warning colouration' on the face.

The anomalies shown by the sable antelope may possibly be explained by its particular habitat and foraging niche, which put a particular premium in maternal defence of adolescent sons.

The sable antelope, unlike most alcelaphins, inhabits relatively nutrient-poor savannas, in which it depends on small patches of relatively nutrient-rich soil and grasses grown to a certain height (about 0.25-1 m). It is well-known that the sable antelope is associated with edges, or 'ecotones' at various scales, rather than homogeneous vegetation.

The patchiness of foraging by the sable antelope is particularly owing to a combination of

  • fires, which occur in the dry season and tend to combust the grass once every few years in the habitat of the sable antelope,
  • interspersion of woodland with drainage lines called 'dambos' (https://en.wikipedia.org/wiki/Dambo), which tend to have clay-rich soil and to be free of trees, and on which the grasses tend to be fairly palatable, and
  • large mounds of termites, which tend to fairly nutrient-rich and exempt from the fires that sweep the matrix among the mounds, and provide particularly palatable grass in limited quantities.

What this means is that in the sable antelope, unlike most 'plains game', there may be intense competition among the sex/age classes for crucial food, localised in a generally unpalatable type of vegetation. The best grasses would tend to be taken by the territorial male, and adolescent males in particular would tend to marginalised by the masculine aggression of the territorial male.

Estes and Estes (1969, The Shimba Hills sable population. First progress report), referring to Hippotragus niger roosevelti, state on page 13:

"Sub-adult males [2-3 years old] are often found in nursery herds...Adult sable bulls thus show more tolerance than many other territorial antelopes; for instance male wildebeest are ejected from the herd as yearlings...This tolerance is promoted by submissive (= female) behaviour on the part of young males...The tolerance of males within the nursery herds until a relatively advanced age may be adapted to the frequently low population density in this species. Bachelor herds into which young males might go when evicted from the nursery herds often do not exist, which makes young males that much harder to drive from the nursery herd."

Estes and Estes, The sable in Rhodesia. Second progress report), referring to Hippotragus niger niger, state on page 12:

"Nursery herds of H. n. niger usually include one adult bull. Although more than one adult male has frequently been recorded by different observers, this is actually an unusual and temporary occurrence...in most cases the supernumerary adult males are simply sub-adults. Males are tolerated in the nursery herds up to around the age of three, by which time H. n. niger bulls are often black except for their hindlegs."

Kingdon's (2015, https://www.booktopia.com.au/the-kingdon-field-guide-to-african-mammals-jonathan-kingdon/book/9781472962447.html?source=pla&gad_source=1&gclid=Cj0KCQiAj_CrBhD-ARIsAIiMxT8O_88SxKmeKiCIx9QtJ3uKQFoCbidATl8ibTcpaImkjYzzyNrDVZAaAiHQEALw_wcB) interpretation has stood the test of time. On page 209, he states:

"Males are driven out into 'bachelor' groups at about 3 years...sable antelopes are secondarily territorial. One indication of their nomadic, open-country origins is the male's reliance on visual self-advertisement. Unlike other woodland and forest antelopes scent-marks are subordinate to the male sable's posturing's and direct herding of the females. Black colouring is both the mark of super-seniority in the colour-coded hierarchy of the female herd and also the central beacon of a defended territory. Battered bushes, dung piles and foot-scrapes in the centre of a 3 or 4 [kilometre-squared] territory may help deter other males but it is the imposition of male physical presence that dominates both hierarchy and territory."

Publicado el noviembre 23, 2023 05:56 MAÑANA por milewski milewski

Comentarios

@milewski "The sable antelope may be the only one of the hundreds of spp. of ruminants, worldwide, that shows this combination." Are there any other possible examples of ruminants which show this, even though Hippotragus niger may be the only one?

Publicado por paradoxornithidae hace 5 meses

@paradoxornithidae

Many thanks for asking.

Oreamnos americanus fails to qualify, because there is no distinct pattern on the face.

Certain oryxes may qualify. However, the horns of the relevant spp. are so long and straight that they seem not to be designed particularly for self-defence.

Oryx leucoryx - apart from this caveat re its horns - seems a particularly plausible candidate (https://www.shutterstock.com/image-photo/jerusalem-israel-october-14th-2019-arabian-1532652998 and https://www.shutterstock.com/image-photo/family-grouping-wild-arabian-oryx-maha-381993337 and https://www.pinterest.com.au/pin/arabian-oryx-and-calf-oryx-leucoryx--2674081006623252/).

Oryx gazella has conspicuous colouration (https://www.istockphoto.com/photo/south-african-oryx-in-kgalagadi-transfrontier-park-south-africa-gm1345844973-423788656?phrase=gemsbok+calf&searchscope=image%2Cfilm), but not as bold, overall, as that of Hippotragus niger niger in full maturity.

Rupicapra rupicapra seems to qualify, but only in winter coat.

https://scienceinpoland.pl/en/node/22491

https://www.istockphoto.com/photo/chamois-rupicapra-rupicapra-mother-with-young-gm1227389263-361978145?phrase=chamois+in+the+winter&searchscope=image%2Cfilm

https://www.agefotostock.com/age/en/details-photo/chamois-rupicapra-rupicapra-female-walking-in-winter-alpes-italy/SSJ-h-81078534

https://www.istockphoto.com/photo/herd-of-chamois-gm174631700-7839185?phrase=chamois+in+the+winter&searchscope=image%2Cfilm

https://www.istockphoto.com/photo/chamois-in-the-winter-vosges-mountains-france-gm870478918-145520815?phrase=chamois+in+the+winter&searchscope=image%2Cfilm

https://www.istockphoto.com/photo/chamois-rupicapra-rupicapra-adult-in-snow-france-gm1223452363-359392940?phrase=chamois+in+the+winter&searchscope=image%2Cfilm

https://www.istockphoto.com/photo/chamois-rupicapra-rupicapra-adult-standing-on-snow-gm1253817872-366279051?phrase=chamois+in+the+winter&searchscope=image%2Cfilm

https://www.alamy.com/rupicapra-is-a-genus-of-goat-antelope-called-the-chamois-they-belong-to-the-bovine-family-of-hoofed-mammals-the-bovidae-retezat-national-park-wild-image340677484.html?imageid=58C68510-503F-4D34-9E4A-C1CD58E40E81&p=407815&pn=2&searchId=c4da65e15312338e30a750d0f8536c9b&searchtype=0

https://www.freepik.com/premium-photo/chamois-deer-white-snow-winter_61673401.htm

https://www.mediabakery.com/AFS4531142-mountain-goat-gams-gams-in-winter-gams-in-the-winter-coat-gamsbrunft-chamois-chamois-in-winter-chamois-in-the-winter-coat-chamois-chamois-in.html

Publicado por milewski hace 5 meses

@paradoxornithidae

To answer your question more comprehensively:

There seem to be only two clades that offer candidates, viz. Rupicaprini and Hippotragini.

There is no doubt that rupicaprins generally have horns compatible with anti-predator defence, as opposed to ornaments for masculine sparring. And several forms have colouration stark enough to look intimidating.

However, caveats are that a) the face of Oreamnos is plain whitish like the body, and b) the body of Rupicapra loses its bold colouration in summer.

In the case of Hippotragini, females lack bold colouration overall in all spp. other than two spp. of Oryx and one sp. of Hippotragus.

In the case of Oryx, the main caveat is the length and straightness of the horns - which can best be appreciated by comparison with the more intimidating hooks of Rupicaprini.

In the case of Hippotragus, the main caveat is that, in most subspecies of H. niger, females do not attain colouration so bold that they qualify. And, even in H. n. niger, it is only fully mature female individuals that qualify.

So, if we were to take the most balanced approach, we would ask with equal curiosity why there is a combination of dangerous-looking horns (in an anti-predator context), bold overall colouration, and a boldly-coloured face in females of a) H. n. niger in full maturity, b) Rupicapra rupicapra in winter, and c) Oryx leucoryx in adolescence (when the horns are not yet full-length).

Does this make sense?

Publicado por milewski hace 5 meses

Many thanks for your detailed reply, Antoni

Publicado por paradoxornithidae hace 5 meses

Evidence of 'slack' parenting of infants in Hippotragus niger:

Reference: Estes and Estes (1969), page 15:

"Animals of the same age keep together, from young calves to yearlings and two-year-old males. From the time they join the herd [after the postnatal hiding period], calves spend more time with one another than with their mothers. A peculiarity observed in a number of different populations is that young sable calves regularly lag behind when the herd moves, sometimes not even getting up until the others are out of sight. Presumably this would enhance the vulnerability of the young to predation, and in fact the only known case of predation during our study [of H. n. roosevelti in Shimba Hills National Reserve] involved a one-month calf that was taken by a leopard in late February, when the Longo Magandi herd was on the edge of the forest."

Publicado por milewski hace 5 meses

Kingdon (2015, https://www.booktopia.com.au/the-kingdon-field-guide-to-african-mammals-jonathan-kingdon/book/9781472962447.html?source=pla&gad_source=1&gclid=Cj0KCQiA7OqrBhD9ARIsAK3UXh3GnF_j2CID1ptu2KJPN1REo7ZwSViYi1CJKhyWbXtHjnI68thhAfMaAkJgEALw_wcB) states, on page 605, about the tribe Hippotragini:

"All species are grazers, with molar teeth well suited to grinding hard grasses (Roan antelopes possess particularlybroad teeth). They have specialised in exploiting zones with an impoverished fauna and flora. Much of their range corresponds with the 'Precambrian Shield' - extensive areas of low fertility and leguminous vegetation. Their narrowed choice (even within the tropics) is due to their attachment to particular localities in which they build up intimate knowledge of large home-ranges (that may include systematic avoidance of areas with numerous predators and competitors)...Horse-like antelopes are unusual in that the females have horns as long as those of the males. Female social units tend to have closed membership. Horns provide them with the means of excluding outsiders from scarce resources and resisting any attempt by males to limit their movement or threaten their offspring."

Publicado por milewski hace 4 meses

Kingdon (2015, page 607) gives the body mass of Hippotragus niger as:
females 190-230 kg
males 200-270 kg.

Publicado por milewski hace 4 meses

Walker (1964, https://books.google.com.au/books/about/Mammals_of_the_World.html?id=16YczQEACAAJ&redir_esc=y), on page 1442, states the following about genus Hippotragus:

"The skin is thick and tough...when closely pursued, they can run as fast as 57 km per hour with great endurance...when wounded or cornered they become savage and fierce, charging and using their horns with amazing quickness and dexterity. When wounded they emit shrill, squeaking cries."

Publicado por milewski hace 4 meses

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