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

• horns obviously longer and more curved than those of even fully mature females,
• an accentuated prepuce, with a dark tip advertising the presence of the penis (https://www.sciencephoto.com/media/1254313/view/male-sable-antelope), and
• bodies somewhat larger than those of females (https://www.ardeaprints.com/common-sable-antelope-male-female-1305709.html).

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."

Posted on November 23, 2023 05:56 AM by milewski