230 P. Mitchell et al.
stored carbohydrates. Additional factors such as biotic agents can amplify declines
in carbon balance, if carbon supply or transport is compromised through stressors
such as defoliators or wood borers (Galiano et al. 2011 ). While trees can deplete
carbohydrates during drought (Mitchell 2013 ; Hartmann et al. 2013 ; Poyatos et al.
2013 ), there is limited evidence for implicating carbon starvation solely for tree
mortality, because trees rarely exhaust measurable stores of carbon. However, given
our current knowledge of how plants store, translocate, and utilize carbohydrates
during drought (Sala et al. 2012 ), it is likely that low carbohydrate availability can
effect water transport and heighten physiological stress. This framework has helped
to stimulate much research into how primary drivers such as water deficit facilitate
the action of multiple stressors associated with plant hydraulics, carbohydrate dy-
namics, and plant defensive systems.
The other important element of McDowell’s mortality framework is that it links
exposure or the attributes of drought intensity and duration with the plant’s life-
support system (McDowell et al. 2011 ). For example, short and intense droughts
will reduce plant water balance, rapidly leading to hydraulic failure, and have little
effect on the availability of carbohydrates. Conversely, because carbohydrate uti-
lization is rate-limited through processes such as respiration, droughts that induce
extended periods of zero or negative carbon balance will deplete carbohydrates
(Mitchell 2013 ; Poyatos et al. 2013 ). Elevated temperatures may not only contribute
to heat stress and increased evaporative demand but also increase respiration and
the rate at which carbohydrates are depleted during long duration droughts (Adams
et al. 2009 ). This framework also highlights the need to understand the dynamics of
intensity and duration in defining the mechanisms underlying the observed stress.
Both of the frameworks outlined above describe interactions of multiple stress-
ors using different perspectives and levels of detail. So, how can we develop a more
generalized picture of the triggers and relationships between different factors across
the entire continuum of responses identified in Fig. 11.2? One way to view physi-
ological stress is to partition the influence of primary, secondary, anthropogenic,
and conditioning factors in influencing plant health and physiological stress (Mitch-
ell et al. 2013 ; Fig. 11.3). Primary factors such as drought tend to affect a forest
over large areas and at the regional scale can operate independently of other biotic
and abiotic factors. Secondary factors are dependent on the occurrence of primary
factors, but may be the sole source of stress or act in concert with the primary fac-
tor. These are typically biotic agents and their impact can be related to: changes in
host physiology or condition, climatic conditions, disturbance events, and food web
dynamics (Garrett et al. 2006 ). Conditioning factors include soil depth and type, the
size and age distribution of the stand and the site’s stress history. These factors have
a large influence on the spatial and temporal patterns of stress across the landscape
and can introduce considerable variation in the impacts of stress events, even within
monospecific stands. For example, meteorological drought conditions across forest
landscapes can be relatively homogenous, yet the magnitude of physiological stress
may be greater for stands on ridge top sites, where water availability is diminished
by the shallow, porous nature of the soils (Matusick et al. 2013 ). Over longer time-
scales, these conditioning factors promote adaptation within the populations. Ac-
climation is triggered by changes in physiological condition at a range of scales