Changes in colouration in the spotted hyena, from infancy through adolescence to maturity

@tonyrebelo @jacqueline_llerena @jeremygilmore @ludwig_muller @maxallen @douglasriverside @doug263 @devbagdi @davidbygott @matthewinabinett @zarek @beartracker

First, let me introduce readers to the cervical flag of the spotted hyena (Crocuta crocuta, https://www.inaturalist.org/taxa/41886-Crocuta-crocuta), which is a pale, spotless panel on the side of the neck (https://www.gettyimages.com.au/detail/photo/young-cheetah-eating-sausage-on-grassy-field-royalty-free-image/1352760448?adppopup=true and https://www.gettyimages.com.au/detail/photo/spotted-hyena-in-the-maasai-mara-national-reserve-royalty-free-image/1223215569?adppopup=true).

This will feature prominently in this Post, about the previously unexplained ontogenetic changes in colouration in the spotted hyena.
 
There is no sexual dimorphism in colouration in this species. This is unsurprising, because there is - as far as I know - no sexual dimorphism in the colouration of any fissiped (https://en.wikipedia.org/wiki/Fissipedia) carnivore other than the lion (Panthera leo).

In general, fissiped carnivores are sexually monomorphic with respect to colouration. It is true that the spotted hyena has a remarkably ‘sexist’ society. However, this does not extend to colouration.
 
The ontogenetic changes in the colouration of the spotted hyena (https://www.gettyimages.com.au/detail/news-photo/spotted-hyenas-with-babies-in-the-grassland-of-the-masai-news-photo/1052873046?adppopup=true) exceed those in most other carnivores, including other hyenids.
 
The three other species of hyenids all have similar colouration as infants and adults. So, the spotted hyena is odd in both its sexual biology and its colouration.
 
A few canids, such as the dingo (Canis familiaris dingo), show minor ontogenetic change in colouration (see https://www.inaturalist.org/journal/milewski/56704-juvenile-makeup-as-a-distinctive-feature-of-the-dingo#).

Felids also show some ontogenetic changes in colouration. However, these are mainly in juveniles being more spotted than adults, in species that have lost their spots as adults, e.g. lion and puma (Puma concolor). The major changes in the cheetah (Acinonyx jubatus) are unique (see https://www.inaturalist.org/journal/milewski/54808-protective-mimicry-in-the-cheetah-part-1#).
 
In the spotted hyena, the neonate is uniformly dark. At this stage, it remains underground for most of the time.

Soon, the pelage pales on the temples (https://www.gettyimages.com.au/detail/photo/spotted-hyena-with-cub-royalty-free-image/522010418?adppopup=true). This pale spreads on to the neck, while the rest of the body remains so dark that the spotting cannot yet be easily discerned.

Next, the body becomes spotted, leaving a pale cervical flag spotless. The muzzle and feet tend to remain dark.

In the adult but not fully mature coat, the feet lose their darkness.

Finally, in full maturity even the cervical flag is lost, and the spotting fades, over the whole body.

The tail tassel remains dark (https://www.gettyimages.com.au/detail/photo/spotted-hyena-masai-mara-preserve-kenya-royalty-free-image/522275794?adppopup=true) throughout the sequence. The raising of the tail thus provides a caudal flag.
 
This ontogenetic sequence is basically one of progressive fading. However, this change from intensely pigmented to somewhat depigmented is anatomically complicated. Furthermore, there is an as yet uninvestigated possibility of patterns in ultraviolet.

The loss of the cervical flag, and most of the darkness of the spotting, is more a case of the fur becoming threadbare with age, than an actual change in pattern. However,

• the complexity of this whole sequence remains odd among Carnivora, and
• the patterns differ from those in the coexisting species, the cheetah.

Here, I document these patterns, and I try to explain them. Since other hyenids lack these changes, the social complexity and peculiarity of the spotted hyena are presumably responsible. But, according to which rationale?
 
Perhaps one can invoke a particular aspect of the society of the spotted hyena. This is a kind of ‘aristocracy’, a system whereby hierarchical rank tends to be inherited.

The spotted hyena combines gregariousness with selfishness (a lack of apparent altruism, relative to canids and felids). The only aspect departing much from this selfishness is maternal behaviour. It is thus possible for rank to be passed from mothers to daughters/sons.
 
I suggest that the causal link between ‘aristocracy’ and ontogenetic change in colouration deserves more investigation.
 
Wherever it occurs in mammals, juvenile colouration tends to protect offspring from attack. This is by means of either

• camouflage (probably true for most fissiped carnivores in which juveniles have distinctive colouration), or
• emphasis of submissive cues that ‘switch off’ adult aggression, playing on ‘maternal’ or ‘paternal’ instincts.

The ontogenetic changes in colouration in the spotted hyena are too complex to be satisfactorily explained simply as camouflage.

So, I reason that part of the explanation may be some sort of ‘appeal’ to adults on the part of juveniles, i.e. some sort of reminder of their vulnerability.
 
Bearing in mind the selfishness of the spotted hyena, I am not suggesting that juvenile colouration directly mollifies the behaviour of adults, regardless of relationships, on the basis of protective instincts as such. Instead, I suggest that it works via the mother's retribution on those that mistreat her offspring, or fail to let it participate in eating at the kill. This would facilitate the inheritance of rank.
 
For offspring to inherit rank from their mothers would be meaningless, unless their mothers are prepared to defend that rank when tested. But because the species has such a selfish psyche, the mother relies partly on a mechanism, using colouration, of stimulus that

• brings out the most of her limited altruism, and
• does not presume any altruism on the parts of others (including the aunts, father, and sibling of the juvenile/adolescent in question).

An important aspect of my rationale is that the ontogenetic changes in the colouration of the spotted hyena are directed towards neither adults in general (unlike the wolf, Canis lupus), nor other predatory species (unlike the cheetah). Instead, they are hypothetically directed only towards the mother (through maternal instinct), and via the mother (through the mother's projection of her intimidatory powers on to her offspring).

And I suggest that this ontogenetic sequence is, in a sense, the mark of an aristocratic society.

The caudal flag does not warrant particular explanation, because it is relatively simple in function. However, the following are my thoughts on the cervical flag.

In a way, the whole ontogenetic sequence in the spotted hyena revolves around the cervical flag - if one incorporates the pale temples of infants into this feature.

The cervical flag, loosely defined, first appears on the sides of the head infants, at which stage they are offset by the general darkness of the colouration.

Later, the feature shifts on to the sides of neck, forming a spotless, pale panel (https://www.gettyimages.com.au/detail/photo/spotted-hyaena-khwai-concession-okavango-delta-royalty-free-image/530315530?adppopup=true). This may be more conspicuous in the eyes of Carnivora than in human eyes, because of a possible ultraviolet component.

The spotless panel on the neck shows noticeable contrast with the spotted body on one side, and with the dark face on the other side (depending on perspective).

A main function of the spotting, which is best-developed in half-grown juveniles, is to hide individuals from other members of their own species - as opposed to hiding them from prey animals.

The cervical flag persists through adolescence, when full body size has been reached. This works, because offspring still benefit from maternal support (mainly indirect, via the hierarchical society) at this late stage.

In full maturity, both the cervical flag and the general spotting fade. This is because hierarchical rank is now (fairly permanently) established, and mature individuals hunt mainly by methods other than stalking prey.
 
The following four photos recapitulate the ontogenetic shift in a posterior direction, of the cervical flag in the loose sense.

The flag first appears just in front of the ears: https://www.gettyimages.com.au/detail/photo/playing-hyena-royalty-free-image/1073470626?adppopup=true.

Then it spreads to most of the neck: https://www.gettyimages.com.au/detail/photo/cub-hyaena-royalty-free-image/998722048?adppopup=true.

Then it disappears from the head, with the highlight now located on the side of the neck just in front of the scapula/shoulder: https://www.gettyimages.com.au/detail/photo/spotted-hyena-runs-across-grass-in-sunshine-royalty-free-image/1149822396?adppopup=true.

Finally, it disappears altogether: https://www.shutterstock.com/image-photo/hyena-165692117.

FURTHER ILLUSTRATIONS OF THE ONTOGENETIC PROGRESSION

NEONATE
The neonate is blackish.

https://www.gettyimages.com.au/detail/photo/mum-hyena-with-baby-in-the-burrow-royalty-free-image/1404372958?adppopup=true
https://countrylivingsa.blog/2014/10/12/raising-a-spotted-hyena-part-2/
scroll in https://africafreak.com/baby-hyena
https://www.dreamstime.com/spotted-hyena-mom-carrying-her-cub-spotted-hyena-mom-crocuta-crocuta-carrying-her-baby-maasai-mara-national-reserve-image169886860
scroll in https://www.animalfactsencyclopedia.com/Baby-hyena.html
https://www.bing.com/images/search?view=detailV2&insightstoken=bcid_rxiqRUJ9N2wEqw5pjXB31976hzID......Y*ccid_GKpFQn03&form=ANCMS1&iss=SBIUPLOADGET&selectedindex=0&id=1154706572&ccid=GKpFQn03&exph=337&expw=600&vt=2&sim=11
https://icanhas.cheezburger.com/tag/hyena 
https://www.earthtouchnews.com/cute-and-cool/cute/tough-week-this-trio-of-hyena-cubs-will-help/
https://www.istockphoto.com/photo/chilling-on-mum-gm1279438383-378051229?phrase=hyena%20cub
https://www.gettyimages.com.au/detail/news-photo/spotted-hyena-crocuta-crocuta-with-young-pup-masai-mara-news-photo/1140447552?adppopup=true

INFANT
The first parts of the infant to become pale are the temples, and the anterior bases of the ears.

http://www.zooborns.com/.a/6a010535647bf3970b0120a69553c7970b-pi
http://www.zooborns.com/.a/6a010535647bf3970b019b0076b572970c-800wi
https://www.gettyimages.com.au/detail/photo/hyaena-cubs-royalty-free-image/117082594?adppopup=true
https://www.gettyimages.com.au/detail/photo/hyena-mother-and-pup-close-up-of-meerkat-kruger-royalty-free-image/1368461634?adppopup=true
https://www.gettyimages.com.au/detail/photo/playful-spotted-hyena-cubs-in-masai-mara-royalty-free-image/1353040220?adppopup=true

YOUNG JUVENILE
Then, this pale spreads to the neck, before much spotting appears on the body. A poorly-defined facial mask may be present (https://www.gettyimages.com.au/detail/photo/hyena-in-kenya-africa-royalty-free-image/97362201?adppopup=truehttps://www.gettyimages.com.au/detail/photo/spotted-hyena-pup-royalty-free-image/534972438?adppopup=true and https://www.gettyimages.com.au/detail/news-photo/young-spotted-hyena-in-the-kalahari-news-photo/948060918?adppopup=true).

https://www.istockphoto.com/photo/young-spotted-hyena-kruger-national-park-gm1363154160-434829831?phrase=hyena%20cub
https://www.istockphoto.com/photo/spotted-hyena-cub-south-africa-gm173158002-20414739?phrase=hyena%20cub 
https://www.istockphoto.com/photo/young-hyena-stock-photo-gm1259441961-369066369?phrase=hyena%20cub
 
JUVENILE TO ADOLESCENT
The spotting on the body appears, complete with the spotless cervical flag. The legs tend to remain dark. This colouration, which is essentially adult except for the dark feet, lasts over a wide range of ages from what looks much like an infant to what looks much like an adult.

http://40.media.tumblr.com/6acbeeef30c0573b87eeb86c5fbc84d6/tumblr_n464rqfnUk1qg94lno1_1280.jpg
https://i2.wp.com/www.ejphoto.com/images_ZA/ZA_SpottedHyena02.jpg
http://www.columbusmagazine.nl/images/user_images/341a8/341a8.jpg
https://www.gettyimages.com.au/detail/photo/portrait-of-deer-standing-on-road-royalty-free-image/1304949709?adppopup=true

ADULT
Once adulthood is reached, the darkness on the feet pales. However, the cervical flag remains.
 
http://jon-atkinson.com/Large%20Images%205/Spotted%20Hyena.JPG
https://www.istockphoto.com/photo/spotted-hyena-gm155430962-20379748

FULLY MATURE TO ELDERLY
With age, even the cervical flag becomes indistinct, as the general spotting fades, whether or not the pelage acquires a 'threadbare' appearance.
 
https://www.masterfile.com/image/en/614-03902377/spotted-hyena-in-desert
https://www.picfair.com/pics/02205508-gevlekte-hyena-spotted-hyena-crocuta-crocuta
https://www.shutterstock.com/image-photo/lone-spotted-hyena-crocuta-known-laughing-488457259
https://es.123rf.com/photo_144893060_spotted-hyena-in-profile-trotting-across-grass.html
https://www.gettyimages.com.au/detail/news-photo/tanzania-serengeti-spotted-hyaena-news-photo/453278972?adppopup=true
http://www.etoshanamibia.info/wp-content/uploads/2013/09/Spotted-Hyena-1024x682.jpg 
http://cache2.asset-cache.net/gc/80361065-spotted-hyena-walking-africa-gettyimages.jpg?v=1&c=IWSAsset&k=2&d=kuQaqGtiSadGjG747L1ZsWwRhG%2B2ta87B4w%2BcpLLUmjxeOzDiSwl%2BtJ0IQ%2BaZY7h
http://previews.123rf.com/images/EcoSnap/EcoSnap0607/EcoSnap060700008/459520-Spotted-hyena-walking-Kalahari-South-Africa-Stock-Photo.jpg
https://www.gettyimages.com.au/detail/photo/22_01_28_spotted_hyena-royalty-free-image/1372422723?adppopup=true

ILLUSTRATIONS OF CERVICAL FLAG
https://www.inaturalist.org/observations/47769154
https://www.gettyimages.com.au/detail/photo/hyena-hunting-at-wild-royalty-free-image/1346329228?adppopup=true
https://www.gettyimages.com.au/detail/photo/spotted-hyena-runs-across-grass-in-sunshine-royalty-free-image/1406324743?adppopup=true
https://www.gettyimages.com.au/detail/news-photo/spotted-hyaena-in-south-luangwa-national-park-in-eastern-news-photo/458431976?adppopup=true
https://www.gettyimages.com.au/detail/news-photo/spotted-hyena-in-the-serengeti-national-park-tanzania-news-photo/143078177?adppopup=true

ILLUSTRATIONS OF CAUDAL FLAG
https://www.alamy.com/stock-photo-spotted-hyaena-displaying-excited-behaviour-amboseli-national-park-144192057.html
https://twitter.com/hyenaproject/status/828293819904950273
https://animalcorner.org/animals/spotted-hyena/
https://www.alamy.com/a-lioness-panthera-leo-runs-away-with-its-tail-up-wide-eyed-and-mouth-open-as-four-spotted-hyena-crocuta-crocuta-chase-after-it-in-dry-yellow-gra-image233183023.html
https://www.gettyimages.com.au/detail/photo/22_01_28_spotted_hyena-royalty-free-image/1372422733?adppopup=true
https://www.gettyimages.com.au/detail/news-photo/hyenas-crocuta-crocuta-with-a-carcass-stolen-from-a-lioness-news-photo/1371857439?adppopup=true
https://www.gettyimages.com.au/detail/photo/spotted-hyena-running-royalty-free-image/591073024?adppopup=true
https://www.gettyimages.com.au/detail/photo/two-hyena-approaching-a-zebra-royalty-free-image/847644612?adppopup=true

ILLUSTRATIONS OF CAUDAL AND CERVICAL FLAGS IN SAME SPECIMEN
https://www.gettyimages.com.au/detail/photo/spotted-hyenas-royalty-free-image/1304722945?adppopup=true
https://www.gettyimages.com.au/detail/photo/spotted-hyena-running-royalty-free-image/593271578?adppopup=true

Publicado el julio 18, 2022 10:46 MAÑANA por milewski