Trophic cascade driven by behavioural fine-tuning as naïve 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 behavioural 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 behavioural 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 (n = 4) were also significantly shyer than nearby, quoll-free populations (n = 3) of conspecifics. This rapid but generalised response to a novel threat was replaced over the following two years with more threat-specific antipredator behaviours (i.e. predator-scent aversion). Predator-exposed populations, however, remained more neophobic than predator-free populations throughout the study. These behavioural 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 metres. Presumably the significant and novel predation pressure induced by quolls drove melomys populations to fine-tune behavioural responses to be more predator-specific through time. These behavioural shifts could reflect individual plasticity (phenotypic flexibility) in behaviour or may be adaptive shifts from natural selection imposed by quoll predation. Our study provides a rare insight into the rapid ecological and behavioural shifts enacted by prey to mitigate the impacts of a novel predator and shows that trophic cascades can be strongly influenced by behavioural as well as numerical responses.