“Seed masting causes fluctuations in optimum litter size and lag load in a seed predator”

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Andrew G. McAdam, Stan Boutin, Ben Dantzer, and Jeffrey E. Lane (Special Feature on Maladaptation)

The DOI will be https://dx.doi.org/10.1086/703743

Boom-bust cycles in seed production increase seed escape by inducing maladaptation in seed predators

A red squirrel in a nest with pups.
(Credit: Stephen Thomas)

Instead of producing similar amounts of seeds each year, some plant species produce very few seeds for several years followed by a bumper seed crop. This boom-bust pattern of seed production is called ‘masting’ and is thought to increase tree fitness by alternately swamping and starving seed predators. In this study, the authors proposed a new idea – perhaps masting causes natural selection on seed predators to differ between these feast and famine conditions. If this changeable selection reduces the abundance of seed predators, this could further increase the benefits of masting.

The authors tested this hypothesis using 28 years of data on North American red squirrels in the Yukon Territory of Canada. In many organisms, it is best to produce an intermediate number of offspring. Produce too many and each will be too small to survive. Produce too few and each will survive well, but there won’t be many of them. An intermediate number of offspring optimally balances these two processes. In this study, the authors found that optimum litter size in red squirrels depends on whether it is a mast year for white spruce cones, their main source of food. In bust years for cones, litter sizes of red squirrels closely match optimum litter sizes. But during mast years, when food is plentiful, the optimum litter size is much larger. Red squirrels somehow know when a mast year is coming and produce larger litters in the spring of mast years, but this increase is small compared to the large increase in optimum litter size during mast years. As a result, squirrels don’t recruit as many offspring during mast years as they would have if they had produced larger litters, which is good for tree fitness.

Following a mast year, red squirrels will store thousands of new cones in their midden, which can last for several years.
(Credit: Andrew McAdam)

So, in addition to swamping and starving seed predators, boom-bust patterns of seed production can also cause seed predators to evolve more frugal life histories that are well suited to common years of low food abundance, but are poorly adapted to less common, resource-rich mast years.


Abstract

The episodic production of large seed crops by some perennial plants (masting) is known to increase seed escape by alternately starving and swamping seed predators. These pulses of resources might also act as an agent of selection on the life histories of seed predators, which could indirectly enhance seed escape by inducing an evolutionary load on seed predator populations. We measured natural selection on litter size of female North American red squirrels (Tamiasciurus hudsonicus) across 28 years and five white spruce (Picea glauca) masting events. Observed litter sizes were similar to optimum litter sizes during non-mast years but were well below optimum litter sizes during mast years. Mast events, therefore, caused selection for larger litters (β′ = 0.25) and a lag load (L = 0.25) on red squirrels during mast years. Reduced juvenile recruitment associated with this lag load increased the number of spruce cones escaping squirrel predation. Although, offspring and parents often experienced opposite environments with respect to the mast, we found no effect of environmental mismatches across generations on either offspring survival or population growth. Instead, squirrels plastically increased litter sizes in anticipation of mast events, which partially, although not completely, reduced the lag load resulting from this change in food availability. These results, therefore, suggest that in addition to ecological and behavioral effects on seed predators, mast seed production can further enhance seed escape by inducing maladaptation in seed predators through fluctuations in optimal trait values.