Trophic Cascade Driven By Behavioral Fine-Tuning As Naive Prey Rapidly Adjust To A Novel Predator

The arrival of novel predators can trigger trophic cascades driven by shifts in prey numbers. Predators also elicit behavioral change in prey populations, via phenotypic plasticity and/or rapid evolution, and such changes may also contribute to trophic cascades. Here, we document rapid demographic and behavioral changes in populations of a prey species (grassland melomys Melomys burtoni, a granivorous rodent) following the introduction of a novel marsupial predator (northern quoll Dasyurus hallucatus). Within months of quolls appearing, populations of melomys exhibited reduced survival and population declines relative to control populations. Quoll-invaded populations were also significantly shyer than nearby, quoll-free populations of conspecifics. This rapid but generalized response to a novel threat was replaced over the following 2 yr with more threat-specific antipredator behaviors (i.e., predator-scent aversion). Predator-exposed populations, however, remained more neophobic than predator-free populations throughout the study. These behavioral responses manifested rapidly in changed rates of seed predation by melomys across treatments. Quoll-invaded melomys populations exhibited lower per-capita seed take rates, and rapidly developed an avoidance of seeds associated with quoll scent, with discrimination playing out over a spatial scale of tens of meters. Presumably the significant and novel predation pressure induced by quolls drove melomys populations to fine-tune behavioral responses to be more predator specific through time. These behavioral shifts could reflect individual plasticity (phenotypic flexibility) in behavior or may be adaptive shifts from natural selection imposed by quoll predation. Our study provides a rare insight into the rapid ecological and behavioral shifts enacted by prey to mitigate the impacts of a novel predator and shows that trophic cascades can be strongly influenced by behavioral as well as numerical responses.