Black eyes can be poisonous exclamations in orange frogs

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AT FIRST SIGHT:

Most species of frogs have prominent eyes. Despite this, frogs avoid using their eyes for communication – with ocular social signalling being rare, and the staring down of would-be predators being unknown.

It has been suggested that the bright hue of the iris in certain species of Agalychnis (Hylidae, https://en.wikipedia.org/wiki/Agalychnis) functions as flash colouration, but this is unconvincing.

The literature does mention certain species of toxic orange frogs possessing noticeably dark eyes, as if part of a possibly aposematic pattern, but this was vague and sketchy.

Even conspicuous frogs with warning colouration (i.e. aposematism) obscure their eyes with longitudinal bands of pigment on the iris and facial skin. In true toads (Bufonidae, https://en.wikipedia.org/wiki/True_toad) the eye is not crossed out by dark bands but the iris is intricately marked for camouflage. In certain frogs, even the nictitating membrane, which covers the eye in daylight, is elaborately disguised.

The only species of frogs known to use quasi-ocular signals are those that attempt to confuse predators by means of false eyespots on the hindquarters which draw attention away from the vulnerable head. These are mainly in the family Leiuperinae (https://en.wikipedia.org/wiki/Leiuperinae) in South America, although a similar pattern occurs also in a few species of Mantellidae (https://en.wikipedia.org/wiki/Mantellidae) in Madagascar and Phrynobatrachidae (https://amphibiaweb.org/lists/Phrynobatrachidae.shtml) in Africa

ON CLOSER SCRUTINY:

It is true that most animals using garish colouration to warn predators of their toxicity tend to hide their eyes despite the extreme conspicuousness of their whole bodies. This certainly applies to frogs.

However, various lineages of ‘toxic golden frogs’ are significant exceptions, with certain small species displaying an odd pattern of warning colouration: strikingly dark eyes that punctuate the uniformly orange skin.

In these species, the eyes remain fully open and dark in daylight, with no covering by nictitating membranes.

It is also noteworthy that the eyes are located on the sides of the head instead of bulging from the top of the head as is usual for frogs.

In all these independently evolved species, the eyes are darker than any other part of the body.

The most frequently photographed example is the golden poison frog (Denbrobatidae: Phyllobates terribilis https://www.inaturalist.org/taxa/21217-Phyllobates-terribilis of Colombia, reputedly the most intensely toxic of all frogs worldwide. This species has conspicuous colouration albeit also a pale green colour-morph.

A similar pattern of accentuation of the eyes can be seen in:

• the granular poison frog (Dendrobatidae: Oophaga granulifera https://www.inaturalist.org/taxa/66274-Oophaga-granulifera of central America),
• the pumpkin toadlet (Brachycephalidae: Brachycephalus ephippium https://www.inaturalist.org/taxa/24492-Brachycephalus-ephippium of southeastern Brazil),
• the golden mantella (Mantellidae: Mantella aurantiaca https://www.inaturalist.org/taxa/22009-Mantella-aurantiaca of Madagascar),
• the yellow harlequin frog (Bufonidae: Atelopus oxyrhynchus https://en.wikipedia.org/wiki/Atelopus_oxyrhynchus of Venezuela), and
• the scarlet harlequin toad (Bufonidae: Atelopus sorianoi https://amphibiaweb.org/species/82 of Venezuela).

In the case of the pumpkin toadlet, the small body may be easily overlooked despite its lurid colour, helping to explain the extraordinary anti-predator behaviours of this species, namely waving of the hands across the black eyes and alarm-vocalising even before being touched. The hands are pale orange like the rest of the skin, but reduced to two digits instead of the usual four digits in frogs

The previously overlooked ocular displays in these four families and five genera of ‘toxic golden frogs’ differ from the false eyespots previously recorded in other frogs in that they send honest, not deceptive, messages to would-be predators.

Furthermore, a converse pattern of colouration has arisen in several families of sexually dimorphic frogs.

These include the following:

• extinct golden toad (Bufonidae: Incilius periglenes, https://en.wikipedia.org/wiki/Golden_toad);
• in the Pelodryadidae, Litoria tyleri https://www.inaturalist.org/taxa/23556-Litoria-tyleri and the superspecies-complex Litoria lesueuri/jungguy/wilcoxii of eastern Australia, which has golden males and camouflage-coloured females; and
• Cophixalus saxatilis (Microhylidae, https://www.inaturalist.org/taxa/24769-Cophixalus-saxatilis).

In all these species, one sex turns vivid orange during the breeding season while the other sex remains camouflaged. In females of the golden toad (Incilius periglenes), the eye is even less conspicuous than in most bufonids.

What is revealing in the conspicuous sex is that the eye is not particularly accentuated. This presumably because the main function of self-advertisement is sexual attraction rather than the repulsion of potential predators.

In summary:
What has not been fully appreciated by biologists is that sexually monomorphic ‘toxic golden frogs’ are exceptional among frogs – with a colouration pattern that has evolved repeatedly – in displaying their real eyes to intimidate predators.

Frogs generally camouflage their eyes to avoid being spotted by predators, so it is easy to assume that no frog advertises its eyes. However, scrutiny of the colouration of the golden poison frog suggests that this species in particular hints at its toxicity with dark eyes against a bright orange body.

Posted on June 14, 2022 08:04 PM by milewski