Anthropogenic extinction of top carnivores and interspecific animal behaviour: implications of the rapid decoupling of a web involving wolves, bears, moose and ravens

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Abstract
The recent extinction of grizzly bears (Ursus arctos) and wolves (Canis lupus) by humans from 95 to 99% of the contiguous USA and Mexico in less than 100 years has resulted in dramatically altered and expanded prey communities. Such rampant ecological change and putative ecological instability has not occurred in North American northern boreal zones. This geographical variation in the loss of large carnivores as a consequence of anthropogenic disturbance offers opportunities for examining the potential consequences of extinction on subtle but important ecological patterns involving behaviour and interspecific ecological interactions. In Alaska, where scavengers and large carnivores are associated with carcasses, field experiments involving sound playback simulations have demonstrated that at least one prey species, moose (Alces alces), is sensitive to the vocalizations of ravens (Corvus corax) and may rely on their cues to avoid predation. However, a similar relationship is absent on a predator–free island in Alaska's Cook Inlet and at two sites in the Jackson Hole region of the Rocky Mountains (USA) where grizzly bears and wolves have been extinct for 50–70 years. While prior study of birds and mammals has demonstrated that prey may retain predator recognition capabilities for thousands of years even after predation as a selective force has been relaxed, the results presented here establish that a desensitization in interspecific responsiveness can also occur in less than ten generations. These results affirm (i) a rapid decoupling in behaviour involving prey and scavengers as a consequence of anthropogenic–caused predator–prey disequilibriums, and (ii) subtle, community–level modifications in terrestrial ecosystems where large carnivores no longer exist. If knowledge about ecological and behavioural processes in extant systems is to be enhanced, the potential effects of recently extinct carnivores must be incorporated into current programmes.