Ontogenetic change in scleral pigmentation in the bonnet macaque

In a previous Post, we have seen that baboons, in general have eyes that are inconspicuous owing to their colouration.

This generalisation does not apply to macaques (Macaca spp.), which are the closest counterparts to baboons in Eurasia. The eyes of macaques tend to be somewhat conspicuous, owing to various features of small-scale colouration on the sclera, the eyelids, and the adjacent parts of the face.

The species I examine here is the bonnet macaque (Macaca radiata, https://www.inaturalist.org/taxa/43448-Macaca-radiata) of southern India.

Two facts emerge in this species of monkey.

Firstly, scleral pigmentation is absent at birth despite being characteristic of the species.

Secondly, despite the tightness of the eyelids, the scleral pigmentation is so dark that it confers the most salient feature of the face of all ages and sexes (except the infant): dark-accentuated eyes that appear to stare. 

The following shows clearly that the sclera adjacent to the iris in infants of the bonnet macaque is unpigmented.
http://walkthewilderness.net/wp-content/uploads/2012/05/BM.jpg 
Ditto but with a hint of pigmentation starting on the lateral (as opposed to medial) side of the iris: 
http://i1.treknature.com/photos/7695/dsc_7143.jpg 

Pigmentation appears in the sclera of the bonnet macaque in young juveniles, as shown by the following.
http://thumbs.dreamstime.com/x/baby-bonnet-macaque-portrait-8766933.jpg

In young juveniles of the bonnet macaque, the eyes already assume a staring aspect accentuated by the dark sclera immediately adjacent to the iris, as shown in the following. Please note that the iris in the bonnet macaque is not particularly dark, and not dark enough to confer a stark appearance to the eyes in the absence of its dark scleral definition.
http://cdn2.arkive.org/media/ED/ED2F9E48-3448-4C62-904A-D41721DD6371/Presentation.Large/young-bonnet-macaque-head-profile.jpg

The following of a juvenile of the bonnet macaque shows the pigmented sclera.
http://fc02.deviantart.net/fs70/f/2013/009/f/f/bonnet_macaque_monkey_goa_india_by_rixresources-d5qyem6.jpg 
Ditto:
http://thumb7.shutterstock.com/display_pic_with_logo/304825/304825,1239469005,1/stock-photo-bonnet-macaque-in-bandipur-national-park-india-28318396.jpg

In adults of the bonnet macaque, there is a hint of pale eyelids, further accentuating the dark-rimmed stare. However, this is not as well-developed as in e.g. Macaca fascicularis.
http://cdn2.arkive.org/media/EC/ECB6F34D-BD9D-4B92-B541-8759DB6C3378/Presentation.Large/adult-bonnet-macaque-head-profile.jpg

In adults of the bonnet macaque, the facial skin remains pale enough that the dark sclera gives the eyes a dark-rimmed stare. However, the eyelids encompass the eyeballs too tightly to show as much of the sclera as in humans.
http://3.bp.blogspot.com/-_VmfAm7zeok/Uql03VQ_fUI/AAAAAAAADeM/mspxUe_fJhM/s1600/img-850+Bonnet+Macaque+Monkey.jpg

The following, of an adult female of the bonnet macaque, glancing sideways, shows clearly that the sclera is dark-pigmented, with no incidence of pale scleral exposure as seen in the infants above. Most of the sclera is presumably white (as in all mammals), but none of the white surface seems ever to be exposed in this species in adulthood, partly owing to the breadth of the pigmented ring adjacent to the iris and partly owing to the tightness of the eyelids.
http://walkthewilderness.net/wp-content/uploads/2012/05/BM+2181.jpg

Mature females of the bonnet macaque sometimes have a blush on the flesh-coloured bare skin of the face. However, this is not dark enough to cancel the effect of the dark sclera in accentuating the stare.
http://thumbs.dreamstime.com/z/bonnet-macaque-closeup-portrait-8747516.jpg 

The following shows a warning expression in mature females of the bonnet macaque. Although the face is as dark in this blushed mother as in any member of the species, the eyes still tend to stand out as dark-rimmed items in an accentuated stare, in which any paleness of the upper eyelids plays a negligible role (in contrast to M. fascicularis, in which the pale eyelids greatly accentuate the stare in conjunction with the dark sclera).
http://www.drkrishi.com/wp-content/uploads/Bonnet_Macaque-05.jpg 

The following shows an adult male of the bonnet macaque, proving that the dark sclera occurs likewise in the male, and that the male like the female has an essentially dark-rimmed accentuation of the stare on a pale face.
https://s-media-cache-ak0.pinimg.com/236x/dd/2b/90/dd2b9024d030098310ef22b3bcefac1e.jpg

The following again shows an adult male of the bonnet macaque. Please note the tightness of the eyelids, showing little of the sclera. What little is evident of the sclera is all dark-pigmented. In this view there is no noticeable pale display of the upper eyelids.
http://farm5.staticflickr.com/4153/4847724313_90d5431381.jpg

In the following self-asserting expression, an adult male of the bonnet macaque does seem to be showing pale eyelids, but the main impression remains of dark-rimmed eyes on an overall pale face.
https://theamazingworldofpsychiatry.files.wordpress.com/2011/03/mainbaringteeth.jpg

The following confirms the difference between mother and infant, w.r.t. the pigmentation of the sclera.
http://thumb1.shutterstock.com/display_pic_with_logo/304825/304825,1243282988,4/stock-photo-bonnet-macaque-nursing-in-bandipur-national-park-30886564.jpg
Ditto.
http://www.drkrishi.com/wp-content/uploads/Bonnet_Macaque-06.jpg

The following (which states bonnet macaque but could possibly be closely related toque macaque in Sri Lanka, in view of the dark ear pinnae) confirms the overall aspect of the face in the bonnet macaque: dark-rimmed eyes staring from an essentially pale face. What this photo-series does is to establish beyond doubt that in this species the pigmentation of the sclera is absent at birth, but develops early in life, remaining as the most conspicuous feature of the face, overall.
http://cdn1.arkive.org/media/45/45DD9C6A-5DFE-4887-82F2-FD88657CC478/Presentation.Large/bonnet-macaque-females-with-infants.jpg

A pattern possibly overlooked by all primatologists in the past is as follows.

The eyelids themselves, immediately adjacent to the eyeball, develop dark pigmentation at the same time (early in life), when the dark scleral pigmentation appears. If one looks closely at this photo-series, one can see this clearly in several photos. In the infant, the eyelids are flesh-coloured. However, in juveniles and adults, the lower eyelid in particular, between the eyelash line and the eyeball, shows a dark pigmentation, possibly no broader than 1 mm – but sufficient to accentuate the stare in conjunction with the dark sclera.

This is a noteworthy observation because

• I have never previously read of any mammal with a pale (flesh-coloured) face but dark-pigmentation on the edge of the eyelids, and
• in the normal stare, the eyelids marginally overlap the cornea.

The latter point means that, in the normal stare, the sclera is only visible laterally and medially to the iris, and the dorsal and ventral edges of the iris would lack accentuation were it not for the narrow dark rim provided by the eyelids themselves.

This eyelid darkening is extremely narrow but quite discernible. It is a case of natural ‘make-up’, adding to the already known paleness of the upper eyelid in various spp. of macaques.

Posted on July 2, 2022 10:29 AM by milewski