Abstract

Pain, though unpleasant, is adaptive in calling an animal’s attention to potential tissue damage. A long list of animals representing diverse taxa possess venom-mediated, pain-inducing bites or stings that work by co-opting the pain-sensing pathways of potential enemies. Typically, such venoms include toxins that cause tissue damage or disrupt neuronal activity, rendering painful stings honest indicators of harm. But could pain alone be sufficient for deterring a hungry predator? Some venomologists have argued “no”; predators, in the absence of injury, would “see through” the bluff of a painful but otherwise benign sting or bite. Because most algogenic venoms are also toxic (although not vice versa), it has been difficult to disentangle the relative contributions of each component to predator deterrence. Southern grasshopper mice (Onychomys torridus) are voracious predators of arthropods, feeding on a diversity of scorpion species whose stings vary in painfulness, including painful Arizona bark scorpions (Centruroides sculpturatus) and essentially painless stripe-tailed scorpions (Paravaejovis spinigerus). Moreover, southern grasshopper mice have evolved resistance to the lethal toxins in bark scorpion venom, rendering a sting from these scorpions painful but harmless. Results from a series of laboratory experiments demonstrate that painful stings matter. Grasshopper mice preferred to prey on stripe-tailed scorpions rather than bark scorpions when both species could sting; the preference disappeared when each species had their stingers blocked. A painful sting therefore appears necessary for a scorpion to deter a hungry grasshopper mouse, but it may not always be sufficient: after first attacking and consuming a painless stripe-tailed scorpion, many grasshopper mice went on to attack, kill, and eat a bark scorpion even when the scorpion was capable of stinging. Defensive venoms that result in tissue damage or neurological dysfunction may, thus, be required to condition greater aversion than venoms causing pain alone.

Highlights

  • The discipline of toxinology is characterized by a number of heuristic dichotomies.Poisons, for example, are toxins that must be ingested, inhaled, or absorbed through the skin to harm their targets, while venoms inflict damage by being injected via a bite or a sting [1,2]

  • The diversity of the natural world, is unlikely to be fully captured by simple dichotomies, so we should not be surprised that some cone snails [10], assassin bugs [19], and no doubt many other species produce both predatory toxins and defensive toxins, and deploy them selectively in the appropriate contexts of feeding vs. deterrence

  • Our use of southern grasshopper mice feeding on AZ bark scorpions provided a conservative test of the hypothesis, as the mice have evolved resistance to the algogenic components in the scorpion’s venom; a sting that can cause intense pain that lasts for hours in humans generates only a few seconds of mild irritation for a grasshopper mouse [52]

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Summary

Introduction

The discipline of toxinology is characterized by a number of (at least partially) heuristic dichotomies.Poisons, for example, are toxins that must be ingested, inhaled, or absorbed through the skin to harm their targets, while venoms inflict damage by being injected via a bite or a sting [1,2]. Venoms, implicated in a range of functions from being antimicrobial [3] to aiding in intrasexual combat [4], are typically classified as serving either to increase the feeding efficiency of the venomous animal or in deterring that animal’s own enemies; i.e., in the binary roles of predation or defense [5,6,7,8,9] These dual selection pressures have been compared broadly across taxonomic groups, with predation frequently cited as driving venom evolution and venom variability in cone snails [10,11]. Venoms used to deter a potential predator, in contrast, typically cause immediate, intense pain at the site of the bite or sting [1,5,9,20], leading the predator to drop or otherwise disengage from the prey, enhancing the prey’s probability of surviving the encounter [21,22,23]

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