Wednesday 17 June 2020

Thirst, starve or susceptibility? Elucidating to physiological driver of canopy tree mortality in transformed arid Thicket.

by Daniel Buttner 

As we know Thicket has experienced considerable transformation shifting from a highly conserved resource sink ecosystem to an ephemeral based one (see Lechmere-Oertel et al., 2005). This change in resource dynamics has consistently been demonstrated via fence-line contrasts where extensive browsing, chiefly by goats, has degraded the landscape, removing key species contributing to both ecosystem productivity and functionality, such as the dominant succulent Portulacaria afra (spekboom) and the many "palatable" species.

While extensive work has been conducted on the overall pattern or rather impact of browsing on thicket by quantifying the loss of species as well as looking into the soil geochemical and physical properties, there is little to no physiological research, particularly drought work. This is quite paradoxical considering the general notation and subsequent recognition of thicket species as being drought tolerant, yet citing no empirical data to back up said suppositions. Irrespective of this quantitative data absence several anecdotal observations might through a "spanner in the works" of drought-tolerance assumption in thicket. Yes, the distributional range of thicket, specifically arid subtypes, appear to support this drought tolerance notion. However, much as the subtropical trees in these systems persisting beyond their respective physiological optimum, so does the question as to why in transformed arid thicket do the trees, which have escaped considerable herbivory damage  by goats are slowly beginning to vanish from these transformed landscapes. Such a disappearance would seem to contradict the notion of drought tolerance capabilities of these ancient, resource conservative trees (most commonly Pappea capensis and Euclea undulata). The expatriation has considerable repercussions for the stability and subsequent conservation efforts of subtropical thicket, particularly arid types.

I believe, or more accurately speculate, that many of the tree species are relying on a quite elusive symbiosis. What we in the Potts Research Group have come to fondly call the "Spekboom Sponge Hypothesis" (see The Spekboom Sponge Hypothesis or SSH) which posits that trees and other shrubs exploit P. afra as a physiological refugia, abstracting necessary water requirements during protracted drought (both frost drought and arid drought conditions) periods in arid Thicket. Under the SSH we might expect that thicket trees might experience greater physiological strain than those in transformed sites (spekboom the first causality to goat herbivory).

The removal of this dominant succulent has a substantial impact on the fundamental ecosystem functions, ranging from soil stabilization to gross carbon sequestration. While the role of P. afra as an ecosystem engineer is undisbuted but its relevance as a nurse plant, as suggested in Adie & Yeaton (2013), and subsequent effects as a physiological refuge from water constrained conditions remains elusive and is need of  discussion. Many studies have attempted to capture nurse plant effects or rather ascertain whether a foundational species (synonymous with ecosystem engineer) can be characterized as a nurse plant. Conventional approaches employ spatial association analyses (proximal distance between individuals to calculate a "Zone of Influence"), the second more commonly applicable approach is removal of the suspected nurse plant and document changes resident species functional traits, often phenological and health indices, with the rare appearance of a physiological metrics (see Brooker et al., 2008) to infer a reduction in stress condition of benefiters near a suspected nurse plant.

While such a removal experiment would not only be impractical but also extremely expensive to undertaken. However, in thicket we are fortunate (I use the term loose here) that goat browsing has provided us with just such an opportunity by preferentially consuming the more palatable species first, i.e. succulents, lianas and eventually spinescent shrubs, leaving only those capable of physical escape, such as the trees who's foliage exists beyond the vertical reach of goats are but the few species to have survived in these landscapes. Although, totally by coincidence have these trees escaped the first round of biophysical disturbance, yet little do they realize the second round is on its way. By removing the undergrowth, goats have unintentionally removed the majority of the Thicket canopy heightening the evaporative demand on near-surface water-soil horizons, actualizing a localized aridity gradation of  the soil matrix placing considerable physiological strain on remnant trees. The impacts of such an aridity gradient is a completely loss of the foundational microclimate needed for seedling establishment and essential for future tree recruitment success in arid thicket. The image below illustrates this quite well, with the sheer abundance of Pappea capensis skeletons outnumbers the living.

Aerial imagery taken in transformed landscape illustrating the numerous Pappea capensis skeletons (red circles) throughout indicative of future expatriation of these trees within this landscape. Note the blue circle, this individual has lost half its canopy cover with the remaining stems bleached white stems indicative of dead tissue. I suspect this individual to have surpassed a critical threshold of mortality likelihood and the foliage persisting is simply the remnant metabolic legacy of the plant, and has cascading hydraulic failures due to the inability to maintain a positive net carbon balance.

While it is quite apparent as to the outcome of goat browsing, i.e. loss of thicket wholeheartedly, the reasons for why the trees and a few spinescent shrubs (pers. obs. Carissa haematocarpa) are eventually expatriated from the landscape — the underlying physiological mechanism rationalizing their lose is yet to ascertain. From the actualization of aridity gradation transitioning between intact to transformed, many would posit drought or rather more specifically drought susceptibility, contrary to the long-held belief of drought tolerance of thicket. While I can only speculate at this moment to the hydraulic vulnerability of these trees there are shared similarities in anecdotal observations made with other classic drought based model systems, such as the Pinyon-Juniper woodlands in the USA (Mueller, et al., 2005). This classic example contrasts to dominant species as polar opposites in their respective drought response strategies and have ever since been cited as the benchmark for analogous reviews and comparative analyses for interpreting drought responses by other arid forest ecosystems or those experiencing seasonal water deficits.

Here I illustrate the strong comparative analogs using a single dominant tree species found throughout the Subtropical Thicket biome, Pappea capensis, placing it in context of the proposed hydraulic framework by McDowell et al., (2008) attributing tree mortality to two main hypotheses. The first being the hydraulic failure hypothesis, which attributes the success of a species under drought to have a well structured and supportive conductance system, enabling stomatal activity to go unimpeded during drought, thus anisohydric species where the whole-plant water potential follows closely that of soil (i.e. environment). Anisohydric species fluctuate minimally in their respective stomatal conductance ensuring carbon assimilation is not impact by drought. However, for the plant to ensure water continuity its imperative that a well supported hydraulic architecture capable of enduring extremely water potentials and potential for cavitation and subsequent emboli during protracted dry spells — anisohydric species as the risk takers and most vulnerable to hydraulic failure. Whereas isohydric species coordinate hydraulic traits to avoid the physiological strain expressed upon them during water deficiencies, maintaining whole-plant water potential at more positive pressures than those experienced those of the soil, this ensures that the plant is unlikely to experience cavitation or possible hydraulic dysfunction during drought conditions. However, by limiting or rather stringently controlling stomatal conductance these isohydric species have restricted photosynthetic activity, thus carbon assimilation. Isohydric species play it safe, as most often is the case that they are hydraulically vulnerable and thus take every effort to safeguard xylem conduits from cavitation and possible collapse. However, while attempting to avoid the hydraulic implications of drought they ran the risk of depriving themselves of necessary sugars, thus become carbon starved.

Conceptual hydraulic framework proposed by McDowell et al., (2008), illustrating the mortality trajectory of trees experiencing drought. Biotic agent susceptibility is either amplified or amplifying physiological stress.


An update of the hydraulic framework revised in McDowell (2011), which considers the dual strain placed on non-structural carbohydrates to mitigate hydraulic impairment via osmotic adjustment (production of stable solutes, e.g. proline) and having to ensure net carbon balance maintaining positive carbon turnover. This demand on carbon resources is evident by increased pest and pathogenic susceptibility. 

The carbon starvation and hydraulic failure hypotheses have been proposed the distinction isn't clear cut and is rather blurred. Both are presented as the physiological cause behind drought-induced tree mortality, differentiate on the basis of time to death. Where hydraulic dysfunction is anticipated over a series of months to years while carbon starvation is expected to occur over decades as the tree is carbon turnover is diminished progressively during drought cycles or decadal episodic events. A recent revision of the carbon starvation has additionally been proposed that illuminates hydraulic failure as more significant of the two as effecting mortality risk. McDowell (2011) revised the expectation under carbon starvation noting that during drought trees compensate for hydraulic impairment accumulating non-reactive solutes in their tissues increasing the osmotic potential and enable stomatal conductance to remain high even during water stress states prioritizing photosynthetic metabolism even during stress states. Now whether this is ineffectual photochemical quenching or interlink between nutrient assimilation, specifically nitrogen necessary for hormonal production and other signaling proteins for undertaking simultaneous responses during stressful conditions, remains speculative. However, what many researchers have reached a consensus on is the substantial effects of hydraulic impairment to the survival of trees in any environment experiencing drought or water deficit conditions.

Image of a physiologically taxed Pappea capensis situated in the transformed thicket landscape. A notable reduction in canopy foliage, not imposed by herbivory predominantly but rather as an evergreen (possible semi-deciduous) its leaves are hydraulically conservative (I speculate here no literature or data) thus are susceptible to emboli and subsequent photosynthetic impairment. (Image courtesy of Robbert Duker, May 2020)

Illustration of pest susceptibility of Pappea capensis individual in transformed site, note the numerous insects bore holes. A consequence of non-structural carbohydrate depletion reallocated for production of solutes for osmotic adjustments prioritising hydraulic conductivity over structural vulnerability and secondary metabolites preventing onslaught by pests. (Image courtesy of Robbert Duker, May 2020)

An intriguing outcome of either sequential losses in hydraulic conduits or depression of non-structural carbon turnover via stringent stomatal conductance, is the appearance of the comorbidity of increased  pest and/or pathogen susceptibility. Hence, biotic agents concurrently impact tree mortality either amplifying the physiological stress or enacted as a compounding factor. This impact strongly agrees the notion of allocation optimalty theory were carbon investment is prioritised to tissues or utilised in strategies that pose the greatest risk to survival of the plant. 

I have made several observations of pest susceptibility of the Thicket tree dominant Pappea capensis  that strongly agree with what we might expect under the hydraulic framework proposed by McDowell et al., (2008). There is a great demand for drought research both from a physiological and hydrological standpoint in Thicket as the existing climate change management outline for this biome operates under the historical notion of drought tolerant trees, yet for all we know these trees are persisting beyond their respective physiological optimum surviving within their "pseudo-realized niche" via interspecific facilitation with P. afra. Hence, the loss of this dominant ecosystem engineer has major ramifications for the sustainability of Thicket tree diversity in arid extensions of the Albany Subtropical Thicket biome. A great time to be a budding drought physiologists and Thicket ecologist, so many questions to ask and better still more experiments to run.



References:

Brooker, R.W., Maestre, F.T., Callaway, R.M., Lortie, C.L., Cavieres, L.A., Kunstler, G., Liancourt, P., Tielbörger, K., Travis, J.M., Anthelme, F. and Armas, C., 2008. Facilitation in plant communities: the past, the present, and the future. Journal of ecology96(1), pp.18-34. 

LechmereOertel, R.G., Cowling, R.M. and Kerley, G.I., 2005. Landscape dysfunction and reduced spatial heterogeneity in soil resources and fertility in semiarid succulent thicket, South Africa. Austral Ecology30(6), pp.615-624. 

McDowell, N., Pockman, W.T., Allen, C.D., Breshears, D.D., Cobb, N., Kolb, T., Plaut, J., Sperry, J., West, A., Williams, D.G. and Yepez, E.A., 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?. New phytologist178(4), pp.719-739.

McDowell, N.G., 2011. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant physiology155(3), pp.1051-1059. 

Mueller, R.C., Scudder, C.M., Porter, M.E., Talbot Trotter III, R., Gehring, C.A. and Whitham, T.G., 2005. Differential tree mortality in response to severe drought: evidence for longterm vegetation shifts. Journal of Ecology93(6), pp.1085-1093.

No comments:

Post a Comment