The snake hiss: potential acoustic mimicry in a viper-colubrid complex

Abstract

Examples of acoustic Batesian mimicry are scarce, in contrast to visual mimicry. Here we describe a potential case of acoustic mimicry of a venomous viper model by harmless viperine snakes (colubrid). Viperine snakes resemble vipers in size, shape, colour, pattern, and anti-predatory behaviours, including head flattening, false strikes, and hissing. We sought to investigate whether hissing evolved as part of, or separately to, the viper mimic syndrome. To do this, we recorded and analysed the hissing sounds of several individual asp vipers, viperine snakes, and grass snakes (a close relative of viperine snakes that hisses but does not mimic the asp viper). Frequencies consistently ranged from 40 to 12 000 Hz across species and individuals. All vipers (100%) and most viperine snakes (84%) produced inhalation hissing sounds, in comparison to only 25% of grass snakes. Inhalation hissing sounds lasted longer in vipers than in viperine snakes. The hissing-sound composition of grass snakes differed significantly from that of both asp vipers and viperine snakes; however, the hissing-sound composition between viperine snakes and asp vipers was not statistically distinguishable. Whilst grass snake hissing sounds were characterized by high frequencies (5000-10 000 Hz), both vipers and viperine snake hissing sounds were dominated by low frequencies . A principal component analysis revealed no overlap between grass snakes and vipers, but important overlaps between viperine snakes and vipers, and between viperine snakes and grass snakes. The likelihood that these overlaps respectively reflect natural selection for Batesian mimicry and phylogeny constraints is discussed.

Revisiting the fear of snakes in children: the role of aposematic signalling

“…Further, it is often believed that snakes flatten their head in a triangular shape to appear more formidable and deter potential predators. Yet, viper mimics clearly flatten their head to deceive predators by appearing as a true viper, not necessarily as a large snake2320. Hence, a possibility exists that snakes have exploited the recognition by mammals (including humans) and birds21 of danger signalling: most snakes (harmless or venomous) adopt a triangular head pose when threatened because the shape is perceived as potential danger by predators (i.e.…”

“…Warning signals may be (or combine) patterns, colours, shape, behaviour, odours and sounds1617. Harmful snakes and their mimics boast aposematic signals such as bright colours18, rattle or hissing sounds1920, dorsal zigzag patterns2122 and shaping into or accentuating the triangular shape of their head when threatened23. It was shown that plasticine models of snakes displaying a dorsal zig-zag pattern or a triangular head shape are less likely to be attacked by predators2122.…”

Multi-trait mimicry of ants by a parasitoid wasp

“…Studies of mimicry have focused on characters that are easily observable to the human eye, but as we have shown mimicry may involve more subtle morphological, behavioural, olfactory and acoustic signals. Another case of multi-trait mimicry was recently found in a viperine snake ( Natrix maura ) that mimics the venomous asp viper ( Vipera aspis ) in terms of body size, shape, colouration, patterning and acoustic emissions 39 .We expect that the phenomenon of multi-trait mimicry, as observed in G. agilis and Natrix maura , might be much more common among animals than has been thus far realized.…”

Ecological significance of dorsal polymorphism in a Batesian mimic snake

“…We acknowledge that our results on attacks are based on plasticine models, and those on fleeing distance of live individuals are derived from a rather small sample size, which makes it advisable to discuss these issues under alternative hypotheses. The Batesian mimesis of the viperine snakes on vipers do not limit to the zigzag dorsal pattern, and includes other behavioral aposematic traits such as coiling, striking, snorting, and head triangulation ( Rollinat 1934 ; Aubret and Mangin 2014 ). However, as we used the same cast (that was not coiled neither showed head triangulation) for the 3 types of models ( Figure 2 ), we deduce that the higher frequency of bird attacks to bilineata and control models was exclusively the consequence of the differences in dorsal design among models.…”

“…The elaborate and consistent set of morphological and behavioral traits of most European viper species has been copied by the inoffensive viperine snake Natrix maura (Linnaeus 1758) ( Rollinat 1934 ) as defensive mimicry. This water snake is distributed by the Western Palaearctic and mimics morphological and behavioral traits of European vipers with which it coincides geographically to some degree, for example, Vipera aspis (Linnaeus 1758), V. latastei Boscá 1878, and V. seoanei Lataste 1879 ( Aubret and Mangin 2014 ; Santos et al 2014 ). For example, N. maura exhibits a zigzag dorsal pattern (hereafter zigzag) formed by a wide and dark dorsal band, zigzag shaped, from the neck to the tail, which contrasts with lighter background body colors.…”