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.


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.

Monday, 6 April 2020

Frost synonymous with fire? The hydraulic death hypothesis in Thicket

by Daniel Buttner

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).

Abrupt biome  boundary observed between Spekboom-dominated Thicket and Nama Karoo shrubland. (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.

Image 3: Frost damage of a single spekboom individual transplanted into a frost-prone area at study site. Notice the damage is from the bottom progressing upwards conforming to the second expectation of the hydraulic death hypothesis (photo: Robbert Duker, 2014).

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.

Tuesday, 18 February 2020

The loss of thirst-refugia and implications for thicket restoration

by Alastair Potts

In a previous post (The flattening of the waterscape and unrecorded loss of thirst-refugia: how does this affect plant biodiversity? ), I discussed how the area that is readily accessible to animals has increased dramatically because a fundamental resource ​— water ​— has been homogenised across the landscape (by humans).

A major driver of this homogenisation process is the advent of fencing the landscape to control both domestic and wild animals. This has a long, and relatively recent, history with many fences being put up from the 1950s onwards using government farming subsidies. However, if animals are going to be kept on a parcel of land, there has to be water. And thus, fencing went hand-in-hand with building dams, waterholes and watertroughs (initially windmill-driven). Every parcel of land had to have at least one water point.

Fast forward a few decades to the present where many farms have been consolidated or repurposed into larger farms ​— usually resulting in the removal of inner boundary fences ​— we have larger parcels of land, but watering points are very rarely removed. Thus, herbivores have greater freedom to roam the landscape, but their densities can remain high because of the short-distances to available water.

Here we need to jump briefly to a different topic ​— high failure rates of restoration initiatives in the subtropical thicket using Portulacaria afra (commonly known as "Spekboom"). We have demonstrated that part of this is due to planting in the wrong parts of the landscape (e.g. in frost zones; Duker et al. 2015a,b). But there is a strong herbivory component to this failure ​— although this has not been directly measured, but field observations suggest that this is a very important part of the puzzle.

Herbivory can come in the form of domestic or wild herbivores. Farmers may keep some stock animals on degraded land ​— but their effect on growth and survival of planted spekboom can be devastating. What is the primary reason why limited stock can be kept on degraded land? ​— the presence of a water point.

Dr Robbert Duker and Dr Marius van der Vyver (both excellent thicket ecologists) report high densities of Greater Kudu retarding the growth rate of spekboom planted in the great Thicket-Wide Plot experiments and neighbouring intact thicket. I suspect the increased densities of Greater Kudu across the subtropical thicket is cause for alarm ​— this is not in line with how this ecosystem worked previously. For example, Jack Skead records that the first sighting of Greater Kudu in 300 years in the Steytlerville area was in 1956 ​— Kudu were unknown in this region before and yet their densities are so high now that driving at night is considered dangerous as the chance of hitting a Kudu is quite high.

And these Kudu are also found in very degraded areas (note that most fences are not barriers to Kudu who readily leap >2 m). Why? The availability of water.

Thus, if we are to give restoration efforts the best chance at succeeding, we need to try and increase the thirstscape ​— to do this, we need to close watering points! There will be areas that are have natural water points (i.e. near rivers), so don't target these for restoration. Thus, any analysis of spekboom restoration potential for the Eastern Cape landscapes should include the waterscape. Target areas that are away from natural or anthropogenic water sources, or include the shutdown of anthropogenic water sources as part of the restoration toolset.

Duker, R., Cowling, R.M., du Preez, D.R., Potts, A.J., 2015a. Frost, Portulacaria afra Jacq., and the boundary between the Albany Subtropical Thicket and Nama-Karoo biomes. South African Journal of Botany 101, 112-119.
Duker, R., Cowling, R.M., du Preez, D.R., van der Vyver, M.L., Weatherall-Thomas, C.R., Potts, A.J., 2015b. 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, 167–178.

Monday, 17 February 2020

The Spekboom Sponge hypothesis

By Alastair Potts

We know that Portulacaria afra, commonly known as "Spekboom" (and the focus of much misguided hype around carbon sequestration), is an ecosystem engineer in its native range in the Eastern Cape province (and the Little Karoo of the Western Cape). 

An ecosystem engineer is any organism that significantly contributes to the creation, modification or destruction of a habitat. In this case, P. afra, increases the water availability in the landscape (van Luijk et al. 2013) for other subtropical thicket tree species that would not normally be able to survive in that landscape (Wilman et al. 2014). It does this by increasing the rainwater infiltration and creating a thick mulch leaf litter (Lechmere-Oertel et al., 2008) which traps water and decreases evaporation.

Our research group was recently in the field exploring how this dynamic helps subtropical trees ​— i.e. what effect does having P. afra around a tree help its water dynamics. Our focus species was Pappea capensis (Jacket-Plumb) and we were measuring the tension of the water column in trees that were either emerging from Spekboom clumps or were in herbivore-degraded parts of the landscape, and therefore standing alone.

Examples of Pappea capensis trees that we assessed for water pressure potential (a measure of plant water stress). Trees were on the same slope and within ~200 meters of one another. Exposed trees occurred lower on the slope where overbrowsing by goats and sheep has removed P. afra. The exposed trees have likely been in this state for >50 years. 
What we found was unsurprising...
The mean water pressure potential (uMPA= mean MPa of 3 replicates per plant) of trees of Pappea capensis occurring alone or within a clump of P. afra (Exposed: n=9, In-clump=11). {Don't ask about the difference in sample size! All I can say, this measurement mission was done between 12h00 and 15h00 with our highest temperature of 47°C ​— our brains were a tad fried}. More negative values means greater water stress!

Thus, the subtropical trees within a P. afra clump, in general, had significantly lower tension (more +ve values on the figure) on their water column than those on exposed slopes without P. afra. {Note: these are preliminary results that require replication ​— that's up to Daniel B.}

But, while we were waiting around for the poor sod who was fetching the latest samples (we tag-teamed as to who had to venture forth from our basecamp — the centre of large P. afra clump — to collect the next sample) ​— we decided to also measure the water tension in P. afra. We were expecting it to be quite a bit lower, but it was consistently around -0.83 to -0.96 MPa.

This is quite a difference in water pressure potential between the succulent P. afra and canopy tree P. capensis. Which got us thinking...! What if P. afra increased water availability in the landscape more than simply by increasing infiltration and decreasing evaporation? If the roots of P. capensis and P. afra grew close together (i.e. touching), then the difference in water pressure potential might be enough for the tree to suck water out of the succulent!

We call this the "Spekboom Sponge" hypothesis: specifically, as trees become more stressed and the tension on their water columns increased, that they might ​— at some point ​— be able to suck water out of P. afra. 

P. afra is able to suck up a lot of water during a rainfall event ​— data from Dr Kathleen Smart's PhD found that P. afra increased its stem diameter by 5-7% post rainfall (×1.05-1.07 of original size). Based on the size of the stems she was analysing (ø: 84.5 & 145.5 mm),  that's ~0.4-0.8 mm³ per cm of stem. The subtropical trees do not have this same ability, and cannot store much water in their stems, and are thus largely reliant on soil moisture for their physiological requirements {ref needed}. Thus, the P. afra, may provide the surrounding plant community with additional water via touching roots systems as the environment becomes drier and drier.

This is quite an exciting hypothesis, as it suggests that P. afra may be more than just an ecosystem engineer but also a "nurse plant" for subtropical trees during the common droughts and generally low rainfall conditions experienced by arid and valley subtropical thicket in the Eastern Cape landscapes.

And of course, Daniel B. (the Duracell Bunny in our research group) found this paper within hours of our return from the field:
"Nurse shrubs can receive water stored in the parenchyma of their facilitated columnar cacti" by Alicia Montesinos-Navarro and colleagues published in the Journal of Arid Environments in 2019.
In this paper, these researchers demonstrate that the columnar cacti, Neobuxbaumia tetetzo, provides water to neighbouring shrubs, Mimosa luisana. 

We'll be testing this hypothesis in the coming year using the same methods as Montesinos-Navarro et al. We'll provide an update as to what we find.

Alastair out...

Update: 20-Feb-2020. After chatting to Ed February, we're also going to be looking at leaf SLA of trees in and out of P. afra clumps as well as leaf δ13C to determine if there have been long-term water contraints (beyond short hot and dry periods, like our pressure chamber measurement mission).

Update: 22-May-2020. Thanks Daniel for picking that I don't know how to convert PSI to MPA! Excuse the crazy readings in the previous figure version...!

Lechmere-Oertel, R.G., Kerley, G.I.H., Mills, A.J., Cowling, R.M., 2008. Litter dynamics across browsing-induced fenceline contrasts in succulent thicket, South Africa. South African Journal of Botany 74, 651-659.
Montesinos-Navarro, A., Verdú, M., Querejeta, J.I., Valiente-Banuet, A., 2019. Nurse shrubs can receive water stored in the parenchyma of their facilitated columnar cacti. Journal of Arid Environments 165, 10-15.

van Luijk, G., Cowling, R.M., Riksen, M.J.P.M., Glenday, J., 2013. Hydrological implications of desertification: Degradation of South African semi-arid subtropical thicket. Journal of Arid Environments 91, 14-21.
Wilman, V., Campbell, E.E., Potts, A.J., Cowling, R.M., 2014. A mismatch between germination requirements and environmental conditions: Niche conservatism in xeric subtropical thicket canopy species? South African Journal of Botany 92, 1-6.

Friday, 27 September 2019

The flattening of the waterscape and unrecorded loss of thirst-refugia: how does this affect plant biodiversity?

The Impala Lilies (Adenium multiflorum) in my parents' garden flowered this year. This little happening led me down a train of thought that ended in a shattering conclusion: the greatest threat to plant diversity is how man has homogenized water across the landscape, or rather created a uniform waterscape. 

Oh wow, so how did I get there? A little bit of background is required. Firstly, my parents “garden” is no garden at all — their backdoor opens onto the African savanna of the lowveld. {I remember returning home on one occasion to find the back door out of use as a pride of 15 lions had killed a waterbuck on the path from the car to the house.} The plants growing there are those that have always been there and are subject to all the nibbles and chomping of all the animals that nibbled and chomped them for millennia past. Except….

Except for three Impala Lilies, which are indigenous to the Lowveld, but had never been seen on the farm. My mother has a fondness for this particular plant species, hence a break in tradition of keeping the garden wild, she planted these few plants. And they have suffered ever since. The impala and kudu share an inordinate fondness for these three plants — enjoying the leaves as fast as they were produced. 

In the more than fifteen years that these poor little plants eked an existence, and I never seen them flower. Not until this year. This year, I found happy Impala Lilies full of leaves and a display that lit up the winter bush drabness. What had changed? Well, after years of worrying after her little plants, and coaxing them back to life after each mauling by a hungry antelope, she finally decided to keep the animals out for good, so she caged them in (the plants that is). Free from hungry mouths, these plants thrived in their captivity.

A simple observation. No animals meant happy plants. But hang on, Impala Lilies are indigenous to the Lowveld. They’ve evolved in a landscape full up with many different plant eaters. So they should be able to easily withstand herbivory. But. But, I’d never seem them on the farm. Certainly not because the environment was wrong — my mother’s plants certainly attest to how much they enjoy the soil and the rain. But, I’m certain that it is because there are too many hungry mouths to feed, and any other Impala Lilies that may have been on the farm never had a human mother-hen to protect them. I think that this plant species, and many others, have been eaten out existence — what scientists term “local extinction”.

Oh, but I hear your thoughts: “that is the obvious result of overstocking, putting too many game animals onto the land, you silly people”. No, the reserve follows strict scientifically-based and monitored stocking densities, and the plant community, or the biomass of greenery, is healthily intact. There is enough food, barring natural droughts, for all the animals and then some. This is not a management or science problem. Or at least, not directly.

What those Impala Lilies showed me, was that they needed to be away from herbivores. Far away. But where is this in the large expanse of the reserve? Nowhere. Because what used to be refugia — places where plants are protected from plant-eaters — no longer exist. 

Almost all of the large herbivores in the African savanna need two things: food and water. Plants grow across the landscape, but in prehistory water was restricted to river courses, often in ephemeral rivers, or small seasonal pans. Large grazers and browsers, especially those that occur at a high density (and thus consume a lot of plants) can on!y do so within foraging distance of water. In prehistory, the closest water source to my mothers Impala Lilies would have been a small river over 15 km away. But now there are at least five dams and water holes within 3 km. And I can think of areas that may have been tens of kilometres, maybe even hundreds, away from water. These areas could only support few animals. But the plants! The plants don’t need to be near a river or any other surface water. They tap into underground water or water stored in the soil. 

Thus, there is probably an entire guild of savanna plant species that only ever experienced the mildest of the herbivore munchies. In scientific terms, we could say that the waterscape was highly heterogenous — there were many areas with surface water, but large areas with none, or almost none. These low points in the waterscape would have been home to a few animals like roan, sable, eland and tsessebe with the rare movement of the animals that make larger herds through their midst. {And interestingly, the increase in waterpoints has been blamed for the decline in the antelope mentioned above ​— read "The Riddle Of The Rare Antelope"}

By putting in boreholes, and creating a new surface water point, humans have encouraged the expansion savanna herbivore populations into the thirsty plant refugia. And although the herbivore-resistant plants do just that, resist, survive and flourish, those like the Impala Lilies start to fade a disappear under onslaught of continuous bites.

This idea of the role of waterscape refugia in protecting plant biodiversity also explains something that I found decidedly odd in another African system, the subtropical thicket of the Eastern Cape. Thicket is home to elephants, where they are the primary agent of disturbance (unlike savannas, where fire could be said to be the dominant reset button in the system). And Thicket can support an incredibly high biomass of elephants — the tree species are especially robust to mega-herbivore hunger, far more so than their savanna counterparts who lose large limbs and whole trunks to elephant ministrations. But there are also a host of plant species that seem to get systematically removed from the landscape once elephants are introduced. Aloe africana is an example. An aloe that is endemic to small part of the subtropical thicket and yet it is very susceptible to elephants and other large herbivores (like the Greater Kudu). So, how can this be? Well, water used to be really scarce in this basin. There are major rivers, running from the escarpment across the narrow strip of coastal lowlands and into the sea. But these are far apart. In prehistory, there would have been vast areas of Thicket that would have been far from water, and thus rarely visited by elephants. (Elephants are a keystone species in Thicket as they open paths that other animals can traverse — No elephants, no paths. No paths, no other herbivores, or at least very few). Ask the Addo ecologists and they’ll tell you that their biggest way to control elephant densities is to open and close water holes. Their management strategy is largely based on controlling water availability. 

Nonetheless, there remains far more surface water for roving herbivores in Addo, and across the rest of the country, than there ever has been. In the Karoos (both Succulent K. and Nama K.), I predict that scores of plant species have been lost as the thirsty plant refugia was quenched by boreholes and watering troughs. As I said above, the herbivore resistant community remains, but we lose species that relied on being in that part of the landscape where animals rarely travelled. 

The levelling out of the waterscape is likely the greatest threat to plant biodiversity. Creating herbivore-free fenced areas — much larger versions of my mother’s caged Impala Lilies may be what we need to preserve those plant species who relied on the thirst refugia to survive herbivory. 

A parting thought… All of those nature reserves where we imagine the ecosystem and biodiversity to be in some sort of prehistory balance — think again. The waterscape has been homogenized in these reserves, and we may be unaware of those plant species that are being lost from the communities as the munching mouths of herbivores move in.

Finally in Flower: My mother's Impala Lily (Adenium multiflorum) in flower after being protected from herbivory. This species can withstand a level of browsing, but then only grows as a small stunted shrub. When free from browsing, it can form a tree up to 3 m tall (often seen in Kruger Park camps). It grows from a rootstock that enables it to often resprout after damage. But continuous browsing can kill a plant.

Thursday, 9 August 2018

The Fynbos Forum Turns 40 — But the Conservation Fight is Far From Over

By Alastair Potts

I've attended many of the Fynbos Forums over the years. It's a fantastic place where scientists, managers, government officials, and NGOs get to meet and share ideas about the Cape Floristic Region. Overseas researchers, e.g. from the US or Europe, are blown away by this conference concept. The Forum can be seen as a think-tank for research and conservation. Many ideas generated at the Forum have gone on to grow into major globally recognised initiatives (e.g. the Working for Water program).  These successes have been documented by Caroline Gelderblom & Julia Wood in their recent book "The Fynbos Forum: Its Impacts and History" (Available for free download in coming months).

The Forum has always had an upbeat vibe as it is where all those at the frontline of the conservation battle get to meet, share war stories, the successes, the losses, and all the interesting facts that we continue to learn about nature. 

This year felt different. Very different. In reviewing the amazing work of dealing with alien invasive plant species (the biggest threat to Fynbos!), the continued glaring omission of pine trees in the biocontrol list is devastating. Pine trees have escaped plantations, gone feral in the Fynbos, and are marching on unabated. (The reason for this is the plantation industry's fears around biocontrol affecting their plantations).

But these policy-level problems have been around for a long time. But this year, the problems were more personal, more devastating to the psyche. Those at the conservation frontline are hurting. There were many stories, and I list a few below for a feeling of them...

  • A site monitored by the CREW due to its rare plants was bulldozed by order of a local council in the Western Cape to make a parking lot for a water collection point. The bulldozers worked carefully around the large information signs explaining the unique heritage of the site. When confronted, the council apologised, and is "restoring" the veld, but the damage is irreversibly done. It is likely that these plant populations have been lost for good.
  • The City of Cape Town's biodiversity management department has put in years of effort and energy to conserve important open spaces in the City. The City of Cape Town is largely built on lowland Sand Fynbos, and this vegetation type is nearly extinct within the City's footprint — this is an incredibly rich vegetation with many endemics (most of which are now extinct). The biodiversity management department would always have an uphill battle against the needs of a growing city compared with the generally globally unique situation of incredibly high levels of biodiversity that is also spatially restricted. But the water crisis has brought on a mass flouting of environmental regulations and resulted in the ruining of many sites and threatening of plant species. But more worrying is the growing land appropriation question. There are land grabs in the city, and these naturally focus on the open undeveloped areas — but these are the exact same pieces of land that the biodiversity team have spent years in obtaining and managing for conservation. With single swoops, these areas are invaded and shacks are built on them. Evictions are nearly impossible as this is politically-sensitive topic, and what politician is going to stick his or her neck out to evict illegal land grabbers "for a few plants". The twin onslaughts are juggernauts that are impossible to stop. So while the City deals with the water crisis, and our Nation deals with the land crisis, we're losing our natural heritage.
  • There are also development plans for Kenilworth racecourse which is driven by the government, despite the obvious and documented conservation of the racecourse.  
  • Phosphate mining has reached the border of the West Coast National Park, and there are moves afoot to de-proclaim sections of the Park to allow the miners in...
  • The scuttlebutt is the Dr Guy Preston (Deputy Director General in the DEA) is being sued in his personal capacity by trout enthusiasts for his work on trying to get trout out of South African rivers where they are causing harm. Trout, an alien and invasive fish species, has caused huge amounts of biodiversity harm to the unique fauna of Cape rivers and there is a strong environmental case for their removal. But to attack conservationists in their personal capacity sets a worrying precedent for those who are willing to stand up against the "mighty" (the trout associations are backed by big money as is the case for most of those involved in major despoiling the environment!).
With all of these frontline stories shared at the Forum, it was apt that the concept of "ecological grief" has just been defined and Rupert Koopman shared this at the Forum. As Neville Ellis and Ashlee Cunsolo write..
"Research shows that people increasingly feel the effects of these planetary changes and associated ecological losses in their daily lives, and that these changes present significant direct and indirect threats to mental health and well-being. Climate change, and the associated impacts to land and environment, for example, have recently been linked to a range of negative mental health impacts, including depression, suicidal ideation, post-traumatic stress, as well as feelings of anger, hopelessness, distress, and despair."
Those in the conservation sector aren't in it for the money. The aren't in it for the fame. They're there because they can see the tidal wave of destruction that humans are unleashing and they know what it means. They are not "doing it" for us, but for future generations who are going to look back in despair at what our century destroyed. They can see the long view, the big picture, which gets lost in the day to day need to "make" money, whatever the cost.

Our environment needs help, but our conservationists also need help. This is not a war they can win on their own. And it is a war that is going on in your back yard, no matter where you live.

Glenn Moncrieff shared the following quote during his keynote address by Gus Speth (a leading US environmentalist):
I used to think that top environmental problems were biodiversity loss, ecosystem collapse and climate change. I thought that thirty years of good science could address these problems. I was wrong. The top environmental problems are selfishness, greed and apathy, and to deal with these we need a cultural and spiritual transformation. And we scientists don’t know how to do that.” - Gus Speth
Although the Fynbos Forum has been an amazingly successful think-tank for scientific and conservation issues, as well as making substantial progress highlighting the value of biodiversity to politicians and the public, there are still missing elements. The psychologists, the advertisers, the graphic designers, the famous, and the trend setters need to become part of the Forum's fellowship. It is no longer about what we know, but rather how we can capture minds across all walks of life. A difficult task given the pressing issues facing the world (the gross inequality in South Africa being especially prominent), and it is a task that both scientists and conservation managers are poorly equipped to do. We need to re-think who can really have the biggest impact on conserving biodiversity.

Imagine if Schalk Burger were to adopt a plant species and he took part in surveying it each year... :)

Thursday, 2 August 2018

The origins of flammable vegetation

by Alastair Potts

Examples of plant communities that require fire for sustained existence are found around the world. In South Africa, both fynbos and savanna ecosystems need fire at some point for their component species to either complete their life history cycle or reduce competition with other plants. Thus, some vegetation types have  traits that make them more flammable than others (think of fynbos [e.g. small leaves = "fine" fuel] versus forest [e.g. large leaves = "coarse" fuel]).

However, the evolution of these flammable traits at a community level is an evolutionary conundrum. In a seminal paper published in 1970, Robbert Mutch from the U.S. Department of Agriculture (Forest Service), proposed that...
"Fire-dependent plant communities burn more readily than non-fire-dependent communities because natural selection has favoured the development of characteristics that make them more flammable."
 A straightforward argument on the surface. But as dip a bit deeper into this idea, problems arise. This has primarily to do with what is the biological unit that is being selected?

Mutch opens his paper with the following bold proposition...

"If species have developed reproductive mechanisms (underground rhizomes, root sprouting, serotinous cones) and anatomical mechanisms (thick bark, epicormic sprouting) to survive periodic fires, then fire-dependant plants might also possess characteristics obtained through natural selection that actually enhance the flammability of these communities." [emphasis added]
Thus,  he suggests in a vague way that plant communities, and not species, are the units under selection. This type of argument is known as "group selection"; this type of selection has experienced extreme criticism in the literature, as altruistic behaviour where, in its extreme form, an individual sacrifices itself "for the good of the species" does not make evolutionary sense: if any individuals evolve that do not behave altruistically, then they will have a higher likelihood of passing on their genes in a population of altruistic kamikazis — and thereby such defectors will, over generations, come to dominate the population.

What is additionally interesting is that group selection usually applied to a group within the same species. However, almost all flammable vegetation types are comprise a highly diverse suite of species which have flammable traits. So even arguments of "kin selection" (i.e. sacrificing individuals do pass on their gene via relatives who survive), which is another angle of group selection, still fail to explain such behaviour.

Enter the "kill-thy-neighbour" hypothesis proposed by Bond and Midgley in 1995. This hypothesis that
"...flammability may enhance inclusive fitness if the resulting fires kill neighbouring less flammable individuals and also open up recruitment possibilities".
They also state that
"Alteration of the fire regime through the evolution of flammability, even in a single species contributing heavily to fuel loads,would result in the selective exclusion or admission of other species to an ecosystem depending on the compatibility of their pre-existing traits with fire."
Yet how does this hypothesis apply within a flammable fire-driven community? [Note: flammability and fire-surviving traits need to be considered separately]. If flammable traits are costly to maintain (e.g. dead branch retention), then defectors (in this case, species with low flammability but fire-surviving traits [either of the current individual or of seeds]) should come to dominate the community and thereby decrease its overall flammability. This would allow the invasion of other species that were previously excluded by fire; for example, remove fire from fynbos vegetation and forest species invade and ultimately transform the vegetation into a forest community.  Thus, flammable species need to remain dominant components of the community, and non-flammable defectors a minority component. Thus, from the Bond and Midgley model, we can predict that there should be a combination of flammable and non-flammable fire-adapted (or pre-existing fire survival traits) species.

But this is where the "kill-thy-neighbour" model ends. It still does not adequately explain how flammability and the necessary post-fire seedling advantage could co-evolve. This is where I think there is a geological explanation for the origin of flammable vegetation with fire-adapted traits, but that is a blog for another day...