Frost has been defined as a fundamental factor in dictating the biome boundary between Thicket and Nama-Karoo shrubland (see Image 1). The impacts of frost are numerous and have been discussed in a previous post by Dr. Robbert Duker (see Thicket restoration and frost: the forgotten enemies) , overall having detrimental impacts on photosynthetic efficiency of exposed individuals ( Duker et al. 2015).
|Image 1: Subtropical Thicket and Nama-Karoo biome boundary (photo: Robbert Duker, 2014)|
This got me thinking that the effects of frost might also extend beyond the photosynthetic machinery of Thicket species (spekboom being primary focus here) and impact the structural components as well, specifically hydraulic conduits in the stem.
At this moment I would like to take a little detour, and chat about fire or more specifically the way in which fire is proposed to kill plants and relating this to the hydraulic death hypothesis (Midgley et al. 2011). To be brief, the hydraulic death hypothesis suggests that plant mortality following intense fire events can be attributed to hydraulic failure by cavitation due to sudden water deficiencies induced by heat plumes or by what Midgley et al. (2011) referred to as run-away hydraulic damage due to leaf water deficits where stomatal response to limit water loss was lagging behind the sudden burst of heat from the fire. Whether by run-away hydraulic failure or cavitation, there where three key predictions/expectations suggesting failure in hydraulic conductivity as the prime cause for mortality. Midgley et al. (2011) described these three predictors/expectations as: (1) post-fire mortality occurred a few days after the fire event, (2) death or damaged tissue was observed forming from the base upwards, (3) the mortality correlated negatively with stem diameter as opposed to height.
|Image 2: A spekboom individual planted in a frost-prone area. (Photo: Robbert Duker, 2014)|
This fundamental idea of cavitation got me thinking about spekboom and the Thicket Nama-Karoo biome boundary. First off when water freezes it expands and crystallizes, keep this in the back of your mind while we undertake a thought experiment. Imagine a straw with the ends of the straw capped and the tube filled with water, then placing the straw in your freezer. What would happen to that straw as it freezes, it would begin to expand until it burst at any point along its length. This expanding straw metaphor is analogous to what we might expect in a plant stem comprising of hundreds and thousands of xylem vessels, little straws if you will, running the length of the stem. When frost occurs or rather the temperatures inducing frost formation, the water within these vessels freezes, crystalizes, and expands resulting in hydraulic dysfunction. There are two potential mechanisms of hydraulic dysfunction under frost, firstly, cellular puncture by water crystals resulting in cytoplasmic leakage or in the case of xylem vessels protrusions into surrounding tissue diminishing water driven potential created by intact xylem tissue. The second mechanism is expansion damage of vessel conduits preventing water mobility up the stem. Regardless of the mechanism the outcome is the same, failure in hydraulic conductivity subsequently resulting in mortality.
Bringing us back to the hydraulic death hypothesis in the case of fire there are three expectations, delayed mortality, bottom-up necrosis, and negative correlation of mortality with stem diameter as opposed to height. And while I can speak to the first two of these expectations under the hydraulic death hypothesis induced by frost conditions (see Image 2 as a summary image), the third requires some more data.
This "frost hydraulic death hypothesis" has yet to be tested explicitly but has great potential as an explanatory process beyond existing photosynthetic interference concepts explaining this biome boundary. Applying this hypothesis to other frost tolerant and susceptible Thicket species diverging in plant functional traits (e.g. wood density, SLA, turgor loss point, and xylem water potential) may highlight potential species-specific strategies to mitigating frost-water related influences, particularly hydraulic death.
Duker, R., Cowling, R.M., du Preez, D.R., van der Vyver, M.L., Weatherall‐Thomas, C.R. and Potts, A.J., 2015. Community‐level assessment of freezing tolerance: frost dictates the biome boundary between Albany subtropical thicket and Nama‐Karoo in South Africa. Journal of biogeography, 42(1), pp.167-178.
Midgley, J.J., Kruger, L.M. and Skelton, R., 2011. How do fires kill plants? The hydraulic death hypothesis and Cape Proteaceae “fire-resisters”. South African Journal of Botany, 77(2), pp.381-386.