Tuesday, 2 February 2016

The Puff Adder is not a Phew Adder: The case of the odourless snake

Writing about olfaction in English is complicated by the fact that the verb smell is both transitive and intransitive. So, if we say a snake does not smell, the meaning can be either that the snake emits no odour or that the snake cannot detect odours. This post is entirely about the former sense, do particular snakes emit so little odour that they are undetectable by other animals.

Recent research1 in South Africa has shown that dogs and meerkats cannot be trained to detect the Puff Adder (Bitis arietans) by scent. By contrast, dogs and meerkats can be trained to recognise the scent of five other species of snake. The important difference between the snakes is that the Puff Adder is an ambush predator; the others tested are foraging predators.

Embed from Getty Images: Puff Adder on the savannah

So far, so good. The first question to consider how the Puff Adder achieves an odourless state, as judged by the scenting abilities of dogs. By contrast with the scent from live snakes, dogs could be trained to detect the odour of recently shed skin of the Puff Adder. The authors make the point that Puff Adders are known to move to a new ambush position after shedding their skin and that typically they defaecate at the site of shedding before moving. Questions that spring to mind are: are the outer layers of the skin impermeable to volatile compounds? Is there a period after shedding when Puff Adders are detectable by smell? What is happening in the respiratory tract; an obvious site for the emission of volatile compounds? In this connexion I am not sure I go for the authors’ suggestion that ambush predators may have a lower rate of metabolism and body temperature and, therefore, a lower rate of production of volatiles; I am not convinced that the difference would be sufficient to account for the experimental findings with trained dogs and meerkats as the detector system.

The second question is: given that foraging snakes can be detected by their scent, is there a metabolic cost to being odourless? Is energy needed to use metabolic pathways that do not produce, say, ketones, that appear in the breath of mammals?

The third question is what is the Puff Adder and, probably, the Gaboon Viper using chemical crypsis to hide from. The authors assume throughout that it is to hide from predators. They make the point that their own observational studies suggest that Puff Adders are not easily detected by their known predators: canids, mongooses and genets. In addition, animals from the study population have low (about 50%) annual survival rates. They argue the case for strong positive selection pressure for ‘adaptations that provide even minor reductions to the production of metabolic volatiles (either from the organism itself or its microbiota) or their persistence in the air plume’.

The fourth question I would have asked had I refereed the paper is whether we should also consider any advantages of chemical crypsis to the Puff Adder not as potential prey but as a predator. Does being odourless enable ambush predators an advantage in terms of getting their next meal? If a small rodent could detect a smelly snake in ambush mode might it not stay out of range of the venomous strike? Chemical crypsis could be highly advantageous to the snake lying in ambush. A clue presented but not commented on by the authors in this context is that observational studies indicated that Puff Adders are not easily detected by some rodent species, with rats (Rattus spp.), snake food by any other name, given as one example.

Whatever the proximate and ultimate mechanisms of this particular example of chemical crypsis, the authors have opened up a fascinating field in the evolution of deception.

Miller AK, Maritz B, McKay S, Glaudas X, Alexander GJ. 2015. An ambusher’s arsenal: chemical crypsis in the puff adder (Bitis arietans). Proceedings of the Royal Society B 282: 20152182. doi.org/10.1098/rspb.2015.2182