Overcoming prey naiveté: Free‐living marsupials develop recognition and effective behavioral responses to alien predators in Australia

• Published in: Global change biology 2019-05, Vol.25 (5), p.1685-1695
• Main Authors: Bytheway, Jenna P., Banks, Peter B.
• Format: Article
• Language: English
• Subjects: adaptation; Allopatry; Animal behavior; Anti-predator behavior; antipredator behavior; Behavioural responses; eco‐evolutionary experience; Foraging; Foxes; Frameworks; Indigenous species; invasive alien species; Isoodon macrourus; Mammals; Native organisms; Odor; Odors; Odour; predator recognition; Predators; Prey; prey naiveté; Recognition; Sympatric populations; Vigilance; Vulpes vulpes
• ISSN: 1354-1013; 1365-2486
• DOI: 10.1111/gcb.14607

Naiveté in prey arises from novel ecological mismatches in cue recognition systems and antipredator responses following the arrival of alien predators. The multilevel naiveté framework suggests that animals can progress through levels of naiveté toward predator awareness. Alternatively, native prey may be preadapted to recognize novel predators via common constituents in predator odors or familiar predator archetypes. We tested predictions of these competing hypotheses on the mechanisms driving behavioral responses of native species to alien predators by measuring responses of native free‐living northern brown bandicoots (Isoodon macrourus) to alien red fox (Vulpes vulpes) odor. We compared multiple bandicoot populations either sympatric or allopatric with foxes. Bandicoots sympatric with foxes showed recognition and appropriate antipredator behavior toward fox odor via avoidance. On the few occasions bandicoots did visit, their vigilance significantly increased, and their foraging decreased. In contrast, bandicoots allopatric with foxes showed no recognition of this predator cue. Our results suggest that vulnerable Australian mammals were likely naïve to foxes when they first arrived, which explains why so many native mammals declined soon after fox arrival. Our results also suggest such naiveté can be overcome within a relatively short time frame, driven by experience with predators, thus supporting the multilevel naiveté framework. We asked how naiveté changes for mammal prey in Australia where alien predators are linked to >20 mammal extinctions. We found that bandicoots in areas where foxes have never occurred show no recognition responses to cues of alien fox presence and appear to be naïve to the predation threat posed by foxes upon first encounter. In contrast, bandicoots in areas where foxes have been abundant for >100 years showed recognition and appropriate antipredator behavior (increased vigilance and avoidance) towards fox odor. These results suggest that naiveté can be overcome within a relatively short time‐frame, driven by eco‐evolutionary experience with predators.