Bluff- and baffle-displays in lizards, part 1: several overlooked aspects of the aberrant skink Tiliqua rugosa

(writing in progress)
  
Is Australia the continent with the most false threats by lizards?
 
There are several excellent and clear examples, among various families of Australian lizards, of false aposematism (without definite mimicry as in the sense of having a particular model species) and false threatening behaviour.

The lizards involved are rather common ones familiar even to suburban Australians in several metropolitan areas, so nobody thinks much of the phenomenon. The agamid Pogona has an erectile ‘beard’ which looks menacing but the lizard is not venomous except by the most stretched of definitions.

When Pogona barbata ups the level of threat, it opens its mouth to show a conspicuously yellow interior to the mouth.

This looks menacing, but it is bluff. Then there’s the well-known case of the frilled lizard (Chlamydosaurus), which I’ve illustrated in recent emails about neck length.

Moving on to the Scincidae, a similar type of threat is used by members of two genera (Tiliqua and Hemisphaeriodon): they open the mouth to show a lurid and alarming tongue, but neither does this signify real danger (for there is no venom) nor does the display mimic any particular model, the sinister quality being extremely generalised in the sense of confusing the potential predator with bravado rather than announcing ‘I am a snake’, which is obviously untrue. In the case of hatchlings/juveniles of two genera of skinks related to Tiliqua, namely the aforementioned Hemisphaeriodon and also Cyclodomorphus, there are ominous-looking collar markings suggesting a snake even though the animal is obviously legged.

Turning to the legless lizards (the purely Australian familiy Pygopodidae, which are closely related to geckos but have taken a serpentine body form), at least two genera mimic snakes in the most general way, either behaviourally or in colouration, by having dark markings on the collar and sticking out a tongue which looks nothing like a snake’s tongue but, once again, has alarm value because of a kind of confusing/bluff effect.

And then of course we have several species of Varanus, which seem to display more in Australia than their congeners do on other continents (e.g. standing bipedally on the hind legs and puffing up the throat while sticking out the tongue.

The tongue is, indeed, a common theme in all these forms although the form of the tongue is variable and the whole effect is never particularly convincing in its emulation of snakes.
 
Although this false aposematism/generalised bluff display/confusing nebulous threat pattern is common in Australia, it is uncommon on other continents.
 
One possible case if the ant-eating specialist in North America, Phrynosoma.

This aberrant but harmless iguanid is really odd in squirting blood from the corners of its eyes when harrassed. But it does not pretend in any way to be snake-like and apart from the colour of the blood it has no particular warning colouration.

And chameleons certainly do flatten their bodies and open their mouths and hiss, which is bluff because they are harmless.

But as in the case of Phrynosoma there is no real morphological feature comparable to the beard of Pogona, the neck-frill of Chlamydosaurus, the tongue of Tiliqua or Pygopus, and the tonal contrast on the neck of at least four genera, that shows a specialisation and commitment to false threats.

The general theme is similar, but I can’t think of other lizards, in Eurasia, Africa, or South America, that use this kind of pretence.

Is Australasia will prove to be the world centre of this kind of deception in lizards? I think Varanus may conform to the pattern and that the conspicuousness of Varanus varius may turn out to be based on similar bluff, with no venom to back it up even in juveniles.
 
My explanation:
Australia is big enough to have considerable threats to lizards from predators (which would not apply to smaller islands).

However, the predators are thin enough on the ground that the rate of encounters between potential predator and lizard prey is limited. Also, some of the potential predators are rather unintelligent (e.g. Dasyuridae, other reptiles).

This means that a generalised morphological+behavioural bluff pattern, that would not work in a hectic environment such as Africa, can work in Australia. In Africa, a lizard encountered by a predator really has only two options: flee or fight.

In Australia, there is an additional option, which is to stand and bluff.

It’s noteworthy that most of the species I’ve mentioned above here are rather slow as lizards go. Tiliqua rugosa is, indeed, in some ways the closest thing in Australia to a terrestrial tortoise.

These lizards could not have survived until now were it not that many of the potential predators encountering them must have been confused enough about their identity to feel that it just wasn’t worth the bother of pressing home an attack.
 
Agamidae: Pogona barbata:
http://en.wikipedia.org/wiki/Eastern_bearded_dragon#mediaviewer/File:Pogona_barbata-03.JPG

http://en.wikipedia.org/wiki/Eastern_bearded_dragon#mediaviewer/File:Eastern_Bearded_Dragon_defence.JPG

Scincidae: Tiliqua rugosa:
http://en.wikipedia.org/wiki/Tiliqua_rugosa#mediaviewer/File:Tiliqua_rugosa.jpg
 
Scincidae: Tiliqua occipitalis:
http://jordan7herps09.blogspot.com.au/2010/05/blue-tongued-skink.html

Scincidae: Hemisphaeriodon gerrardii adult:
http://ih1.redbubble.net/image.9299360.1036/flat,550x550,075,f.jpg

Scincidae: Hemisphaeriodon gerrardii, juveniles with snake-like markings on the nape:
http://farm7.static.flickr.com/6062/6115930090_17e17b3d3c_m.jpg

Pygopodidae: Delma torquata:
http://www.arod.com.au/arod/pictures/squamata/pygopodidae/delma/Delma-torquata-thumb.jpg

Pygopodidae: Pygopus lepidopodus:
http://farm9.static.flickr.com/8361/8444338130_671d74633b_m.jpg

Pygopodidae: Pygopus nigriceps:
http://cdn1.arkive.org/media/18/181ABB16-3CF6-46A1-A5B8-F928551D0801/Presentation.Large/western-hooded-scaly-foot-male.jpg

One of the common lizards, surviving even in outer suburbia in Australia, is the shingleback Tiliqua rugosa (Scincidae).

Many naturalists in Australia are familiar with this lizard. However, it is odder, and more remarkable, than realised.
 
Firstly, this is the closest thing to a land tortoise over much of southern Australia. It is armoured, and slow-moving, with an exceptionally short tail for a skink (incapable of autotomy), and is partly plant-eating.
 
I am unsure how it survives fire, because it certainly lives in fire-prone vegetation. It is certainly too slow to flee.
 
But what is noteworthy is that this is an extreme lizard in terms of its reproduction.

Tiliqua rugosa is it monogamous. Furthermore, the precocial offspring are gestated with a true placenta, similar to those of mammals. This, in a perverse way, represents the ‘opposite’ direction of adaptation from the marsupials with which it coexists.

There are even hints of an unusual level of parental care for a lizard.

Although one could ponder why this lizard is somewhat mammal-like, I’m focussing more here on the relevance to land tortoises, pointing out that in order to be anything like a ‘fill-in’ for the missing land tortoises on this continent, a tortoise-equivalent lizard seemingly has to be extreme in more ways than simply its body form: even the dynamics of its reproduction are extreme.
 
Secondly, an odd thing about T. rugosa, as you can see from a photo below, is its threat display.

It opens its large mouth while raising its head towards its potential attacker, and puts out a lurid tongue, producing a purple-and-pink colour display which is certainly ominous-looking although there is no great tonal contrast involved. The implication is that this defensive display is directed mainly against predators with colour vision, by day.

The thing is that there is no special defensive capability to back up the threat; the shingleback is essentially harmless although of course like any lizard it can bite. So we can’t call this display aposematic, but what should be call it instead? Nobody seems to have thought of that question before although this species is so well-known.
 
Please note the following source: http://adc.library.usyd.edu.au/view?docId=shesyst/xml-main-texts/shesystv3.xml;database=;collection=;brand=default;;query=tiliqua
  
http://australianmuseum.net.au/Shingleback-Lizard

http://en.wikipedia.org/wiki/Tiliqua_rugosa#mediaviewer/File:Shingleback-sa.jpg

http://www.wildherps.com/images/herps/standard/05110725PD_Shingleback.jpg

http://en.wikipedia.org/wiki/Tiliqua_rugosa

More explanation of the peculiarly Australian syndrome of specialisation for bluff vs predators in lizards:
  
The photos below illustrate in more detail the pattern of specialised bluff vs predators, which I find to be best developed in Australia although there are also a few examples in semi-arid Asia.
 
Although the basic pattern of colouration may seem similar between the gila monster of North America and some species of Tiliqua in Australia, the banding is more vivid/bold in the venomous North American lizard than in the harmless Australian lizards.

In fact, all the bluffing lizards of Australia have essentially inconspicuous (cryptic/disruptive, i.e. mainly camouflaged) patterns. This is important because it gives the bluff additional force when the display is suddenly produced by an otherwise inconspicuous and slow-moving lizard.
 
In this series of photos, the most important point to note is the size and protrusibility of the tongue in Australian Tiliqua, and the fact that there is nothing about the foraging ecology or society of Tiliqua that could possibly explain the oddness of such a tongue in morphological terms.

Compare this with the gila monster: the tongue is protruded but I don’t think that this tongue is necessarily specialised for display. It’s possibly the tongue that the gila monster needs for eating, and it’s simply deployed in a corollary/subsidiary way for anti-predator display in order to give additional emphasis to a dispaly of genuine aposematism.
 
It is in these sorts of distinctions that the oddness of the familiar Australian pattern has been ‘hiding in plain sight’.
 
The following photo shows the gila monster, Heloderma suspectum, of North America. This lizard is different from all Australian lizards because it is genuinely venomous, and its colouration is genuinely aposematic.

The tongue is protruded falsely in the sense that the tongue is itself harmless, but the overall threat indicated by conspicuous markings and behaviours is genuine. This is NOT the syndrome that occurs in Australia, although to the naive eye it may be confused with it.

There is actually no lizard anywhere in Australia that is analogous with the gila monster.
 
http://www.animalsdo.com/wp-content/uploads/2014/10/gila-monster.jpg?ff2483

Good illustration of fine line between camouflage colouration and aposematism, illustrated by genuinely venomous lizard:
  
The gila monster (Heloderma suspectum) is genuinely venomous, and its whole-body colouration marginally qualifies as aposematic.

There is no lizard in the world that has an unambiguously aposematic whole-body colouration as seen in some frogs (e.g. Dendrobatidae), salamanders (e.g. Ambystoma tigrinum in the adult, not larval, stage) and snakes (e.g. the various ‘coral snakes’).

Indeed, the lack of aposematic colouration is a noteworthy feature of lizards. However, the gila monster (which is only one of two species in its genus, the other species having essentially camouflage colouration which is just not conspicuous enough to be called aposematic) is THE exception.

The point of my showing the photo below is to emphasise that the basic pattern here remains partly consistent with camouflage.

The gila monster retains the sort of banding/spotting that can hide the animal in its typical habitat. However, once the lizard is spotted by a predator, it just looks a bit too garish/boldly marked for comfort, i.e. it arouses suspicion along the lines that a skunk does.

In particular, it’s worth noting the parallel pattern on the head between the gila monster and various mustelids including the honey badger, with a pale crown and forehead offset by dark muzzle, tantamount to a kind of criminal mask.
 
assessment of the Australian pattern of anti-predator bluff in lizards, which involves unambiguously inconspicous whole-body colouration combined with a posturally/behaviourally dependent exposure of certain morphologically specialised, ‘falsely aposematic’ features such as the tongue.

The bottom line is that, although the gila monster can and does display posturally/behaviourally, it looks fairly suspect and sinister even when it lies there doing nothing – and that is a true hallmark of whole-body aposematism.

Truly aposematic animals can make themselves look even more alarming by means of postural/behavioural display (as indeed exemplified by the handstands and tail-wavings of the spotted skunk), but the point is that they look dangerous even when they do nothing at all.

Such a thing cannot be said of any Australian lizard, whether in false aposematism or true/honest aposematism.
 
http://www.unco.edu/biology/faculty_staff/mackessy/Photo%20Gallery/lizards/Heloderma%20suspectum.jpg

In Australia and neighbouring islands of Indonesia (e.g. the Moluccas) there is a genus of extremely large skinks, Tiliqua, most or all of which have a lurid tongue that they stick out when displaying to a potential predator.

This tongue is not only oddly coloured but it seems far too large for its main evolutionary function to be eating or social (intraspecific) interactions. This is a morphological specialisation for bluff, accompanied by a behavioural specialisation for anti-predator display.
 
Scincidae: Tiliqua:
http://helios.webcity.com.au/~chi19603/wp-content/uploads/2012/04/Animalia_Reptilia_Squamata_Sauria_Scincidae_Tiliqua_TiliquaScincoides_0011.jpg
 
Scincidae: Tiliqua:
http://render.fineartamerica.com/images/images-print-search/images-medium/eastern-blue-tongue-skink-threat-display-michael-and-patricia-fogden.jpg

http://render.fineartamerica.com/images/images-print-search/images-medium/eastern-blue-tongue-skink-threat-display-michael-and-patricia-fogden.jpg

Scincidae: Tiliqua rugosa:
http://creagrus.home.montereybay.com/trip-SAuz09/Shinglb-th17Nv09Waik2492w.jpg

Scincidae: Tiliqua rugosa:
http://www.ryanphotographic.com/images/JPEGS/Tiliqua%20rugosa,%20shingleback%20lizard%20showing%20tongue%20low%20res.jpg
 
Scincidae: Tiliqua rugosa:
http://www.ryanphotographic.com/images/JPEGS/Tiliqua%20rugosa%20Shignleback%20lizard%20displaying%20tongue%20low%20res.jpg
 
Scincidae: Tiliqua rugosa:
http://cache2.asset-cache.net/gc/475166037-stump-tailed-skink-in-threat-display-with-gettyimages.jpg?v=1&c=IWSAsset&k=2&d=ICzUBzSY7ASYrYXW6WLOogpn3tKkh6EqwkPOUq%2F59zGeF2Hx5uH4qbDtrI5R%2Bxu7BEu8GrqrG9vLxp1T4wZfjg%3D%3D

Scincidae: Tiliqua rugosa:
http://1.bp.blogspot.com/_jVcOg_5E02U/TLy4adK0LxI/AAAAAAAADU0/stLEjSiotbc/s320/Sleepy+Lizard+Threat+Display.jpg

to be continued in https://www.inaturalist.org/journal/milewski/68689-bluff-and-baffle-displays-in-lizards-part-2-callisaurus#...

(writing in progress)

Posted on July 16, 2022 05:20 AM by milewski