We investigated the problem of the optimal persistence of a chemical s
ignal as an evolutionary game between conspecifics when such signals c
an be exploited by natural enemies. We used a plant-herbivore-parasito
id system as a model to determine the optimal decay rate of a contact
pheromone used by a herbivore to signal the presence of an herbivore's
egg to the marking female and conspecifics. These pheromones are also
exploited by a specialized parasitoid of the herbivore offspring. We
used a series of models with increasing complexity to elucidate the op
timal decay rates of marking pheromones. As long as the mark had no as
sociated costs, the population evolved towards the lowest possible dec
ay rates, independent of herbivore oviposition response towards marked
sites. When marking behaviour had some associated cost, increasingly
higher decay rates evolved with physiological cost of marking and incr
easing levels of parasitoid attack. However, the degree of change depe
nded on competition for, and the probability of re-encounters with, ex
ploited oviposition sites. Additionally, we tested the effect of the t
ime of onset of parasitoid attack (representing early instar to late i
nstar parasitoids) on the evolution of optimal decay rates and found d
ecay rates to decrease in a non-linear fashion with increasing time la
g between herbivore egg deposition and parasitoid attack. We discuss o
ur findings with respect to chemical communication and signals in gene
ral that might be exploited by natural enemies, and stress the importa
nce of an evolutionary ecological perspective towards an understanding
of signal quality.