Abstract

Mammalian pheromones often linger in the environment and thus are particularly susceptible to interceptive eavesdropping, commonly understood as a one-way dyadic interaction, where prey sense and respond to the scent of a predator. Here, we tested the “counterespionage” hypothesis that predator and prey co-opt each other’s pheromone as a cue to locate prey or evade predation. We worked with wild brown rats (predator of mice) and wild house mice (prey of brown rats) as model species, testing their responses to pheromone-baited traps at infested field sites. The treatment trap in each of two trap pairs per replicate received sex attractant pheromone components (including testosterone) of male mice or male rats, whereas corresponding control traps received only testosterone, a pheromone component shared between mouse and rat males. Trap pairs disseminating male rat pheromone components captured 3.05 times fewer mice than trap pairs disseminating male mouse pheromone components, and no female mice were captured in rat pheromone-baited traps, indicating predator aversion. Indiscriminate captures of rats in trap pairs disseminating male rat or male mouse pheromone components, and fewer captures of rats in male mouse pheromone traps than in (testosterone-only) control traps indicate that rats do eavesdrop on the male mouse sex pheromone but do not exploit the information for mouse prey location. The counterespionage hypothesis is supported by trap catch data of both mice and rats but only the mice data are in keeping with our predictions for motive of the counterespionage.

Highlights

  • Mammalian pheromones often linger in the environment and are susceptible to interceptive eavesdropping, commonly understood as a one-way dyadic interaction, where prey sense and respond to the scent of a predator

  • In mouse-infested sites, trap pairs baited with synthetic sex pheromone components of male rats captured 3.05 times fewer mice than trap pairs baited with synthetic pheromone components of male mice (χ2 = 19.75, P < 0.0001) (Fig. 2, top), suggesting that mice avoided macro-locations indicative of rat presence

  • Traps baited with male mouse pheromone components captured 15-times more adult female mice and 2.4-times more juvenile female mice than control traps baited with testosterone alone (Fig. 3, bottom), confirming a synergistic effect of testosterone, brevicomin and thiazole on attraction of female m­ ice[22]

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Summary

Introduction

Mammalian pheromones often linger in the environment and are susceptible to interceptive eavesdropping, commonly understood as a one-way dyadic interaction, where prey sense and respond to the scent of a predator. Closely related species in mammalian communities often use similar communication s­ ignals[2] which facilitates bi-directional (interspecific) olfactory ­communication[3] and lowers the relative cost of maintaining sensory ­receptors[4] This concept appears to apply to olfactory communication signals of sympatric murine rodents, including the brown rat, Rattus norvegicus, and the house mouse, Mus musculus, because there is overlap in pheromone components of female mice and female ­rats[5,6]. While acoustic and visual signals have a fleeting presence, odors and pheromones often linger in the ­environment[25,26] This makes pheromones susceptible to inter-species ­exploitation[12,26,27] which is well known in i­nsects[28,29,30,31] but has hardly been studied in m­ ammals[4,32,33,34,35]. Whether vertebrate predator–prey interactions are informed and guided by bi-directional (mutual) eavesdropping, or “counterespionage”, on scent signals is entirely unknown, as are the underlying mechanisms

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