Annual variation in predation and dispersal of Arolla pine (Pinus cembra L.) seeds by Eurasian red squirrels and other seed-eaters

Seed predation and dispersal are key processes in the survival and distribution of plant species. Many animals cache seeds for later consumption, and, failing to recover some of these seeds, act as seed dispersers, influencing post-dispersal seed and seedling survival. Both animal and plant benefit from scatterhoarding and natural selection of seed characteristics and adaptations of seed predators (and dispersers) is one of the most important examples of co-evolution and mutualism. We studied the producer-consumer Arolla pine (Pinus cembra)-red squirrel (Sciurus vulgaris) system in a subalpine forest in the Italian Alps. Arolla pine produced large seed-crops (masting) at irregular intervals, followed by years with poor or moderate seed production. Squirrel density fluctuated in synchrony with the food resource, eliminating the time-lag normally present when resources are produced in pulses. In all years except 2009 (a mast-crop year), all Arolla pine cones were harvested (their seeds consumed and/or cached) by September to late October by different species. Both squirrels and nutcrackers (Nucifraga caryocatactes) fed on seeds, and their relative pre-dispersal predation rates (on cones in the canopy) differed between years. Overall, nutcrackers consumed more seeds between July and October than squirrels, but in 1 year squirrels took the largest number of seeds. Pre-dispersal seed predation by squirrels tended to be lower in years with large seed-crop size and there was a positive correlation, over the entire study period, between density of recovered hoards and Arolla pine seed density of the previous year. We conclude that (i) squirrels and nutcrackers are important pre-dispersal seed predators and seeds dispersers; (ii) squirrels are also post-dispersal seed predators, and (iii) the proportion of cached seeds consumed by squirrels increased with the size of the Arolla pine seed-crop, suggesting that red squirrel is a conditional mutualistic scatterhoarder of Arolla pine seeds.