11 Combined Stresses in Forests 229
and a small number of observations involving fungal infection ( unpublished data).
The majority of die-off events associated with biotic agents occurred at sites where
mean annual temperature was < 20 °C, a pattern suggesting a greater likelihood of
drought–biotic agent interactions in relatively cooler environments. It is impor-
tant to note that this survey only involves die-off events that were characterized as
episodic; relatively sudden incidences of canopy collapse and mortality during or
directly after a drought event. As we discuss in this chapter, protracted tree declines
are almost always associated with biotic agents as tree health is diminished over
several years or decades, exposing them to greater incidence of infection or attack.
Studies of protracted forest decline from many different ecosystems demonstrate
that a complete etiology of these types of stress involves a consideration of climatic,
soil, stand dynamics, physiological, genetic, and ecological factors and their distri-
bution through time and space (Mueller-Dombois 1986 ; Manion 1981 ; Landsberg
1983 ). Manion ( 1981 ) presented the concept of a decline syndrome that involved
three or more sets of factors to explain the complex interactions of biotic and abi-
otic factors. The first set of factors is termed predisposing; those long-term factors
that are relatively static, such as climate, site conditions, and genotypic/phenotypic
traits Manion ( 1981 ) suggested that predisposing factors weaken a plant growing
in a particularly hostile location. The second set of factors, termed inciting, induces
short-term stress on trees associated with events such as insect defoliation, frost,
drought, or air pollution. It is assumed that these events result in drastic injury to the
plant. The third set of factors is termed contributing factors, tending to operate over
the long term, because they persist on the host for extended periods. While infesta-
tion by contributing agents such as canker fungi, bark beetles, or viruses is often
thought to be the key agent inducing dieback or mortality, they may merely occur in
association with stress caused by predisposing and inciting factors. Manion’s model
provides a useful approach for clarifying the contribution of different factors when
there are multiple biotic agents present during protracted forest decline.
Episodic or acute stress arises from relatively discrete events that induce short-
(minutes to days) and long-term (months to years) responses involving plant defens-
es, productivity, and survival. One prominent framework describes severe drought
events that are associated with tree mortality and forest collapse (McDowell et al.
2008 ). McDowell and colleagues proposed two interrelated pathways through
which tree water and carbon balance influence the process of tree death (McDowell
et al. 2008 , 2011 ). One physiological pathway resulting in mortality is termed hy-
draulic failure. This is caused by severe declines in tree water balance that produce
large tensions on the water column in the xylem, and cavitation involving entry of
air into the water-transport system (Tyree and Sperry 1988 , 1989 ). The process of
cavitation is well documented and is thought to result in cell death through dehy-
dration (Brodribb and Cochard 2009 ). Alternatively, carbon starvation is a process
involving the exhaustion of available carbohydrates. The exhaustion of carbohy-
drates comes about through an imbalance between carbohydrate supply from pho-
tosynthesis, and demand from growth and respiration (McDowell et al. 2008 ). This
pathway for mortality during drought has been postulated, because water deficit can
reduce photosynthesis via stomatal closure, while respiration continues to deplete