Mechanism of Red Spruce Winter Injury

Red spruce winter injury is the reddening and mortality of the foliage in late winter followed by its abscission in late spring (DeHayes 1992). Injury is caused by freezing and is likely the result of various stresses, including low temperatures (DeHayes and others 1990), freeze-thaw cycles (Hadley and Amundson 1992, Lund and Livingston 1998), and rapid freezing (Perkins and Adams 1995). The current-year foliage of red spruce is more vulnerable to injury than older foliar age classes or foliage from sympatric species because it is less cold tolerant (DeHayes and others 1990). In addition, certain anthropogenic inputs such as acidic or prolonged N deposition can further reduce foliar cold tolerance and increase the risk of freezing injury (Schaberg and DeHayes 2000). Heavy foliar loss and potential bud mortality due to winter injury disrupts the carbon economies of trees, leading to growth declines and potential mortality (DeHayes 1992, Lazarus and others 2004). Winter injury was linked to the widespread decline of red spruce observed in the Northeastern United States from the 1960s through the 1980s (Friedland and others 1984, Johnson 1992), and severe winter injury events persist within the region (Lazarus and others 2004).

Beginning in the late 1980s, a series of studies were published showing that acid mist exposure significantly reduced the cold tolerance of red spruce current-year foliage, increasing the risk of foliar winter injury, (e.g., DeHayes and others 1991, Fowler and others 1989, Vann and others 1992). The physiological mechanism for this acid-induced reduction in cold tolerance remained unresolved, however, until a new method for measuring Ca specifically associated with cellular membranes was used in conjunction with controlled acid mist exposure experiments. Using these new methods for measuring membrane-associated Ca (mCa), a series of experiments documented that acid mists preferentially leached mCa from the outside of mesophyll cells, whereas other cations and forms of Ca were leached less, presumably because they were concentrated within the protective membrane barrier of cells (DeHayes and others 1999, Jagels and others 2002, Jiang and Jagels 1999, Schaberg and DeHayes 2000,Schaberg and others 2000). Furthermore, these studies showed that this loss of mCa destabilized membranes, depleted a source of Ca needed for stress signaling, reduced foliar cold tolerance, and predisposed trees to the secondary freezing injury responsible for decline (DeHayes and others 1999, Schaberg and DeHayes 2000, Schaberg and others 2000). Later work verified that soil-based Ca depletion initiated the same mechanistic sequence of physiological disruptions documented for foliar Ca leaching (Schaberg and others 2002).