A new feature of adaptive colouration in ungulates: the fibular flag, part 1: Raphicerus (Bovidae)

@capracornelius @tandala @oviscanadensis_connerties @jeremygilmore @paradoxornithidae @beartracker @jacqueline_llerena @henrydelange @tonyrebelo @koosretief @justinhawthorne @ludwig_muller @happyasacupcake @marcelo_aranda @enricotosto96 @diegoalmendras @michaelweymann @jakob @jwidness @grinnin @karoopixie @davidbygott @dejong @gigilaidler @jason_van_den_berg @michalsloviak @nyoni-pete

Please see https://www.inaturalist.org/journal/milewski/70293-the-bambis-part-9-bleezes-flags-and-semets-in-the-bovid-genus-raphicerus#.

INTRODUCTION

Dear reader, here is a glimpse deep into the secret world of intraspecific communication in two
species of bambis.

Members of the antilopin genus Raphicerus are not gregarious. However, they tend to be monogamous.

Furthermore, adult females consort with their offspring, at least until weaning.

Therefore, there is frequent contact among individuals in the 'societies' of Raphicerus, despite the impression that these animals are 'solitary'.

Because bambis are small-bodied enough to hide for most of the time, their intraspecific communications tend to be secretive.

One way to monitor each other's whereabouts, as they forage in the mornings and evenings, is to 'flash' parts of the body that are small and low enough not to be noticed by scanning predators, but pale/bright enough to be conspicuous at fairly close range, at least when moved.

And this brings us to something that zoologists and naturalists may have overlooked.

It seems possible that grysboks (Raphicerus melanotis and Raphicerus sharpei) mediate such social monitoring, at least in part, by means of a certain part of the body that nobody has paid attention to: the inner surface of the hindleg, just above the hock (https://en.wikipedia.org/wiki/Hock_(anatomy)).

The pelage of the inner surface of the upper hindleg is oddly pale in these species.

Raphicerus melanotis:

http://cameratrap.mywild.co.za/p/cape-grysbok.html

https://www.inaturalist.org/observations/26439871

https://www.inaturalist.org/observations/102342423

Raphicerus sharpei:

https://www.inaturalist.org/observations/9522907

https://stock.adobe.com/search?k=grysbok&asset_id=466446249

Scroll in https://africawild-forum.com/viewtopic.php?p=234341#p234341

By comparison, this same surface is not anomalously pale in the third member of the same genus, namely Raphicerus campestris.

The following show subspecies campestris of R. campestris, which coexists with R. melanotis but prefers more open vegetation (also see comment below for many more illustrations):

https://www.inaturalist.org/observations/107377965

https://www.inaturalist.org/observations/106332311

https://www.inaturalist.org/observations/50746594

https://www.inaturalist.org/observations/129193891

https://www.inaturalist.org/observations/122610678

https://www.alamy.com/stock-photo-steenbok-raphicerus-campestris-walking-in-shrubbery-south-africa-western-76154029.html?imageid=D54D52A6-FFDA-4FBE-9283-9390D08886ED&p=1142662&pn=1&searchId=b33750fe1700c0af1e7d56e14ee9b7da&searchtype=0https://es.123rf.com/photo_171698571_alert-steenbok-carnero-capturado-temprano-en-la-ma%C3%B1ana-en-el-parque-nacional-karoo-cabo-occidental.html?vti=n84f9ofebt93ncyyzk-1-81

The following shows that, in some individuals of R. campestris campestris, there is white on the inner, upper surface of the hindleg, but this does not extend to the vicinity of the hock: https://www.inaturalist.org/observations/60722940.

COINING A NEW TERM: 'FIBULAR FLAG'

In the context of adaptive colouration, a flag is defined as a relatively small-scale pattern that becomes conspicuous, at the scale of the whole figure, when activated by movement.

A typical location for flags, in ungulates, is the hindquarters, particularly the tail. And the functions of caudal flags include social and sexual signalling, and the announcement of anti-predator alarm to conspecifics, or the potential predators, or both.

What has been previously overlooked is that, in certain secretive species of ruminants with small tails, the location of flags on the posterior of the figure may have been shifted from the tail to another, more subtle and intriguing, location, namely the hind leg above the hock.

INTERPRETATION OF FIBULAR FLAG IN RAPHICERUS

In Raphicerus, certain species/subspecies have more countershading (https://en.wikipedia.org/wiki/Countershading) than others.

This countershading is by definition located on the ventral parts of the figure, and the inner surfaces of the upper limbs.

However, on closer examination, there is a significant anomaly.

Countershading - which, by definition, works best when a bright sun is high in the sky- is best-developed in tropical and subtropical subspecies of Raphicerus campestris. It is least-developed in Raphicerus melanotis, which is restricted to the temperate zone

On this basis, one would expect the inner surface of the upper hind leg to be pale in R. campestris, vs not pale in R. melanotis.

However, in reality it is the opposite that is true. Raphicerus melanotis has a pale inner surface on the upper hindleg, whereas R. campestris tends not to have this.

Please scroll to the 11th photo in https://www.africawild-forum.com/viewtopic.php?t=527&start=20 for a particularly clear view of the fibular flag in Raphicerus sharpei.

The fibular flag in R. melanotis and R. sharpei is presumably activated when the animal walks, and it should be particularly visible in the oblique light of evenings and early mornings - when much of the foraging takes place.

The paleness, in R. melanotis, of the inner surface of the hind leg, is puzzling if interpreted simply from the viewpoint of countershading in aid of crypsis. This is because this part of the anatomy

is paler than the ventral surface of the torso, despite the fact that it
is not normally visible enough, in the standing figure, to need disguising.

I therefore tentatively suggest that this pale feature functions as a flag, during walking/asymmetrical standing in suitable illumination.

This fibular flag, I hypothesise, aids social monitoring by means of a signal low-profile enough to remain congruous with the furtive habits and overall inconspicuousness of the species concerned.

A similar rationale may possibly apply to an even smaller area of anomalously pale pelage in R. sharpei, which likewise transgresses countershading. This is located on the front surface where the foreleg joins the torso.

The anterior feature can perhaps be called an 'anterior axillary flag'.

https://www.flickr.com/photos/44691276@N06/8250863085

https://es.123rf.com/photo_110620408_sharpe-grysbok-in-kruger-national-park-south-africa-specie-raphicerus-sharpei-family-of-bovidae.html

https://www.alamy.com/stock-image-sharpes-grysbok-raphicerus-sharpei-male-adult-south-africa-mpumalanga-161763316.html?imageid=6332CFDE-0830-42B2-8ED6-8113A09A06AE&p=546796&pn=1&searchId=bb39c60edd2f811fc9c03d99a5112e0b&searchtype=0

to be continued in https://www.inaturalist.org/journal/milewski/84573-a-new-feature-of-adaptive-colouration-in-ungulates-the-fibular-flag-part-2-alces-alces-cervidae#...

Posted on 27 September, 2022 18:15 by

milewski

Comments

This is an interesting article, I hope it might stimulate people to look more closely at the behaviour of these animals. I have concern, however, about your term "fibular flag". You write "nobody has paid attention to: the inner surface of the hindleg, just above the hock" but the fibula is on the OUTER (lateral) part of the hindleg, not the inner (medial), thus the bone nearest the inner hock is the tibia. Regards, Peter

Posted by nyoni-pete 7 months ago

@nyoni-pete

Hi Pete, Many thanks for your careful reading of this Post, and your perspicaceous critique of the term 'fibular' in this context. You may well be right.

In reply, let me first 'steel-man' your argument, before defending my choice.

The choice of 'fibular', rather than 'tibial', is inept for the following reasons: the fibula is, in the relevant mammals, a) a bone so small as to be vestigial, and b) located at the proximal side of the limb segment in question, i.e. near the knee, not near the hock.

Does this adequately paraphrase your critique? (I could not verify that the fibula is located laterally to the tibia in ungulates or canids.)

Now for my counter-argument:

The flag in question is a feature of the medial/posterior aspect of the limb segment in question (purely medial in Raphicerus, but extending to posterior in e.g. Alces). It would be correct to describe this feature as 'tibial', because the tibia is the dominant bone for the whole limb-segment concerned. However, this inevitably introduces confusion, because 'tibial' could refer to the anterior/lateral aspect - and by default might be assumed to refer to this aspect. Various mammals do have anomalous features of colouration on the anterior/lateral aspect of the limb-segment in question. Two examples that come readily to mind are Damaliscus pygargus (https://www.flickr.com/photos/ucumari/30293536817 and https://shakati.wordpress.com/2020/12/13/bush-facts-34-blesbuck/) and Muntiacus muntjak (https://www.shutterstock.com/image-photo/muntiacus-muntjak-feas-barking-deer-called-1450933313 and https://www.shutterstock.com/image-photo/indian-muntjac-muntiacus-muntjak-called-southern-1262737519 and https://www.shutterstock.com/image-photo/southern-red-muntjac-muntiacus-muntjak-kaho-1152378773 and https://www.shutterstock.com/image-photo/muntjac-crossing-370311422 and https://www.flickr.com/photos/berniedup/6963743562), in which the front of the limb-segment in question is anomalously white (inexplicable according to countershading). The obvious choice of terms for these features would be 'tibial', because they lie right over the tibia. Were we to have applied the term 'tibial' to the medial/posterior surface, we would have a dysfunctional ambiguity. Hence, although I acknowledge that 'fibular' is far from ideal, I suggest that it is the better choice for what we see in e.g. Raphicerus and Alces. The advantage of the fibula, outweighing its shortcomings, is that it is located posterior to the tibia.

Your further thoughts?

Posted by milewski 7 months ago

I'm not sure exaxtly what you want me to look at, but from your link https://veteriankey.com/the-hind-limb-2/ at 6.1.3 "On the lateral distal part of the tibia, recall the presence of the lateral malleolus as the remnant of the fibula in the distal crus." So domestic ungulates, at least, have a very reduced fibula, reduced to remnants proximal and distal. The distal remnant is found near the hock, as the LATERAL malleolus -on the lateral not medial side. The youtube clip at 2.30 gives exactly the same information, the distal end of the fibula is the lateral malleolus.

Posted by nyoni-pete 7 months ago

I stand corrected about the lateral position of the remnant of the fibula near the hock. So, your critique seems valid. However, the problem of ambiguity would remain, not so?

Posted by milewski 7 months ago

Just a couple of points and then I'm off to bed! I can assert that the fibular is lateral to the tibia in all mammals I know and also in birds (I taught veterinary students for 30+ years). I agree that to use the term "tibial flag" could be misleading because around the hock the tibia is the only bone cranial, medial and caudal (I'm using veterinary terminology here - the corresponding human terms are anterior, medial and posterior.) I'm not sure what to suggest as a replacement - perhaps medial hock, although many/most people wouldn't know what is a "hock". Alternative "medial ankle". The fibular flag has a nice "ring" to it but is not anatomically correct.

Posted by nyoni-pete 7 months ago

@nyoni-pete @matthewinabinett

I agree.

The basic problem is that the anatomical lexicon for the various surfaces of the body is limited, causing us to name this surface according to 'the nearest bone'.

This is too much of a stretch, but how else can we proceed?

Perhaps I can elaborate w.r.t. Alces (https://www.inaturalist.org/journal/milewski/84573-a-new-feature-of-adaptive-colouration-in-ungulates-the-fibular-flag-part-2-alces-alces-cervidae).

The basic pattern of interest in Alces is that a conspicuously pale surface occurs on the posterior surface of the hindleg (https://www.inaturalist.org/observations/165808747 and https://www.inaturalist.org/observations/22730337).

This seems analogous with the conspicuous pale seen on the rump/buttocks/haunches/tail in other large ungulates (https://www.adfg.alaska.gov/index.cfm?adfg=muledeer.main).

The pale feature in question, according to subspecies and individuals of A. alces, wraps on to the medial surface of the limb segment in question, and also in some cases on to the lateral surface, and on to the hock and beyond.

However, the essential point of interest is that it is a) located in a posterior position in the figure (https://www.alamy.com/stock-photo-moose-from-behind-142718462.html), b) high enough to be noticeable above snow/water/scrubby stems (https://www.inaturalist.org/observations/116521066 and https://www.inaturalist.org/observations/73167063), and c) unexplained by countershading.

The functional significance, in terms of adaptive colouration, is that Alces is advertising itself, but in a 'semi-covert' way. I hypothesise that it is not advertising its posterior enough to be conspicuous to scanning predators, but it is facilitating monitoring among conspecifics.

So, the principle seems similar to that seen in Raphicerus, not only grysboks but also the steenbok, which likewise has a 'mid-level' pale feature (please see 'buttock flags' in https://www.inaturalist.org/journal/milewski/70293-the-bambis-part-9-bleezes-flags-and-semets-in-the-bovid-genus-raphicerus#).

Clearly, the pale feature in Alces deserves a name. However, there is no name, veterinary or otherwise, for the surface in question. It involves the hock but is not centred on the hock; and much of its significance is that it originates not on the buttocks, but lower down.

Given this gap in the lexicon, we can understand why the conspicuously pale feature I refer to has hardly been mentioned, anywhere in the literature on Alces, despite being the single most striking aspect of the colouration of the largest deer in the world. Those studying Alces have had a 'blind spot' for an obvious feature, as if to exemplify the principle that, until one has a word for a phenomenon, that phenomenon hides in plain sight.

Posted by milewski 7 months ago

@nyoni-pete @muir

I find it remarkable that, in the most detailed and comprehensive account of Alces alces, the most striking feature of the adaptive colouration of the species is not even mentioned.

https://archive.org/details/mammalianspecies-154

Posted by milewski 7 months ago

A story I learned this summer is moose hair, moose flies and roundworms: https://www.inaturalist.org/observations/173161280

Is there evidence from other bovids to suggest that moose coloration might be related to avoiding/minimizing biting flies/parasites?

Posted by muir 7 months ago

@muir

Many thanks for this intriguing idea.

https://www.adfg.alaska.gov/index.cfm?adfg=wildlifenews.view_article&articles_id=920

If the parasites depend on molt for the skin of the moose to be suitably exposed, would the colouration of the pelage really matter?

In view of the close-up photos you link here:

I note that the short pelage on the posterior surface of the upper leg in this individual is pale brown rather than whitish, i.e. it is not pale enough to be conspicuous. In your opinion, is this lack of whitishness because a) the hairs are still so short, after molt, that the dark skin is showing through to some degree, or b) the hairs themselves are pigmented enough to be pale brown, rather than whitish?

Posted by milewski 7 months ago

Have you ever seen any mention.... sorry, I have not.

Posted by muir 7 months ago

The following shows that Redunca fulvorufula fulvorufula lacks a fibular flag, but instead may have an anterior axillary and/or radial flag, consisting of conspicuous white on the inner surface of the upper foreleg:

https://www.inaturalist.org/observations/176381734

Also see https://www.inaturalist.org/observations/176653212

The following shows that Pelea capreolus lacks a fibular flag:

https://www.conservationphotography.co.za/image/I0000EfpiZ3AaWlE

Posted by milewski 7 months ago