Opinion
Aposematism: Unpacking the Defences

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Highlights

Aposematic signals advertise that animals are unpalatable or dangerous. Usually they comprise a conspicuous visual signal paired with an antipredator defence.

Ordinarily it is assumed that such signals denote unpalatability, yet we know that animals advertise many other types of defences, including stings, spines, and weaponry, as well as toxins.

Some defences are therefore overt and can be seen at a distance; others, the physiological defences, are hidden from a potential predator. Dividing defences into these categories gives surprising new insights into the evolution of aposematism.

We collate examples of defences from both invertebrates and vertebrates that are morphological, and hence obvious, or physiological and behavioural and that are hidden, and show how they are situated at different stages of the predator–prey interaction.

This new formulation of aposematic defence signalling has implications for our understanding of the evolution of signal honesty. Signals that are intimately linked to the defence are more likely to be qualitatively honest, whereas those that are hidden are open to cheating. This has implications for the evolution of Batesian and Müllerian mimicry.

Aposematic coloration is commonly considered to signal unpalatability, yet animals advertise malodour, spines, and weaponry as well as toxins, some of which can be seen at a distance whereas others are hidden from predators. Separating defences into overt and covert categories in this way and whether they act before, during contact, or following ingestion generates new insights into the evolution of aposematism. Signals drawing attention to overt defences are difficult to fake whereas signals advertising covert defences can deceive would-be predators, and those acting later in the predatory sequence are more likely to be dishonest. These two orthogonal defence categorizations help to frame where dishonest signalling occurs in nature, set limits on deception by dishonest Batesian mimics, and prompt new questions.

Section snippets

The Concept of Aposematism

Ever since Alfred Russel Wallace penned his response to Charles Darwin’s 1867 question about why nonreproductive caterpillars are brightly coloured – a letter in which Wallace recognized that conspicuous coloration advertises defences [1] – biologists have viewed warning coloration as principally signalling unpalatability. This is likely to derive from the reference to caterpillars, where unpalatability originally referred to being poisonous when ingested. Nonetheless, when Poulton [2] formally

Types of Defence

The myriad aposematic defences seen in nature, be they morphological, physiological, or behavioural 11, 12, can be divided into those constituting the least to the most intimate contact with the prey. Viewing defences through the lens of different stages in the predator–prey sequence is instructive 10, 13 because defences that operate earlier in the predatory sequence tend to be triggered and deployed more often than later ones and may be less costly (i.e., vigilance is less costly than flight

Defences Employed at a Distance before Contact

Odoriferous defences can be discerned by some predators well before they contact prey. For example, volatile irritants are produced by brightly coloured Heteroptera [20], hydrocyanide gas by gaudy polydesmid millipedes [21], and pyrazine odour by many garish insect groups 22, 23. The reek of some mephitids is unpleasant in itself and can advertise anal secretions that can be sprayed at a distance in some species (Figure 1A; [24]). Malodour is necessarily honest as the defence is the signal

Defences Employed at a Distance before Contact

Certain species advertise their ability to escape from predators by showing conspicuous colours that can be seen at a distance. For example, black flank stripes of artiodactyls may amplify the high jumps seen in stotting – a behaviour that signals an individuals’ ability to outrun a predator [31]. Such advertisements of flight speed may be open to a modicum of cheating. For example, pursuit-deterrent signals might be fakeable by low-quality individuals and between species: slow-flying beetles

Implications

Some aposematic signals are intimately tied to the defence itself, such as the echidna’s spines or the pyrazine odour of caterpillars. These signals are qualitatively honest (see [18]) and tend to be employed towards the beginning of the predatory sequence; only earlier defences can be inherently honest (Table 2). Other defences, particularly those that operate later, are not easy for a predator to assess unless it presses its attack. For example, bright-red coloration does not indicate

Concluding Remarks

Antipredator defences are extraordinarily diverse. They may be morphological, behavioural, or physiological, sometimes combined together in the same individual (see Outstanding Questions). Some of these defences, often morphological, can be seen at a distance. Colour signals associated with such defences are likely to be honest, although this requires empirical verification. Other defences, such as being poisonous, are difficult to discern accurately, raising the possibility that advertisements

Acknowledgments

We thank Kevin Arbuckle, Mike Speed, and two anonymous reviewers for helpful comments.

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