Physiological and behavioural effects of fruit toxins on seed-predating versus seed-dispersing congeneric rodents

Fleshy, ripe fruits attract seed dispersers but also seed predators. Although many fruit consumers (legitimate seed dispersers as well as seed predators) are clearly exposed to plant secondary compounds (PSCs), their impact on the consumers' physiology and foraging behaviour has been largely overlooked. Here, we document the divergent behavioural and physiological responses to fruit consumption of three congeneric rodent species in the Middle East, representing both seed dispersers and seed predators. The fruit pulp of the desert plant Ochradenus baccatus contains high concentrations of glucosinolates (GLSs). These GLSs are hydrolyzed into active toxic compounds upon contact with the myrosinase enzyme released from seeds crushed during fruit consumption. Acomys russatus and A. cahirinus share a desert habitat. Acomys russatus acts as an O. baccatus seed predator, and A. cahirinus circumvents the activation of the GLSs by orally expelling vital seeds. We found that between the three species examined, A. russatus was physiologically most tolerant to whole fruit consumption and even A. minous, which is evolutionarily naïve to O. baccatus, exhibits greater tolerance to whole fruit consumption than A. cahirinus. However, like A. cahirinus, A. minous may also behaviourally avoid the activation of the GLSs by making a hole in the pulp and consuming only the seeds. Our findings demonstrate that seed predators have a higher physiological tolerance than seed dispersers when consuming fruits containing toxic PSCs. The findings also demonstrate the extreme ecological/evolutionary lability of this plant-animal symbiosis to shift from predation to mutualism and vice versa.