Investigating the “Plant Adjustment Toolkit”

 
 

A whistling-thorn acacia mounts a costly defense against a beetle larvae parasitizing its stem. Is the cost of defense paid by increasing photosynthetic productivity? If so, how does the tree handle the associated water loss?

Plants adjusting to animal interactions

How do plants get ahead in a world where animals get to move freely and plants must stay still? Animal-plant interactions can come in many forms—mutualism, parasitism, herbivory—and thus intelligence and flexibility seem like good strategies for success! (but don’t take my word for it…)

In my research, I generally use large-scale field experiments to empirically test how plant interactions with herbivores and mutualists are linked to distinct plant physiological patterns. Working with collaborators, I link plant organismal and community traits to higher-level ecological processes such as microbial community composition and apex predator success.


shrewd plants and the ants that protect them

By far, my specialty is investigating how ant-plants accommodate the contrasting costs and benefits of different ant mutualist species. The obligate ant-plant (‘myrmecophyte’) Acacia [Vachellia] drepanolobium—a.k.a, the “whistling-thorn acacia”—and four species of potential ant mutualists serve as an excellent study species for this topic, with highly variable costs (a favorite subject of my PhD advisor, Todd Palmer) and dramatic differences in defensive services by the ants, both of which are highly tractable in field experiments.

I study how these myrmecophytes change their leaf and root physiology in response to antagonistic or mutualistic interactions with animals big and miniscule. At the leaf level, the plants may adjust photosynthesis, transpiration, and water use efficiency to accommodate carbon and water needs.

My ongoing work at Mpala Research Centre investigates how trees adjust photosynthetic traits when their ant mutualist is supplanted by another ant species. Whistling-thorn acacias often grow in expansive monocultures in black cotton savannas, and we use large acacia communities as massive “petri dishes” where we can experimentally transplant ant colonies onto hundreds of similarly-sized trees spread across large (>8-ha) plots in full-factorial experiments. The KLEE project has been running at Mpala for over 25 years, and it allows us to compare the effects of these takeovers in natural conditions vs. in the absence of large herbivores (i.e., a scenario in which the benefits of mutualism with ants is sharply reduced).

We used equipment built by PP Systems to rapidly measure leaf photosynthetic parameters in the field: acacia leaves exhibit highly plastic patterns linked to both mutualist ant occupants and ungulate herbivore presence. To investigate the epigenetic mechanisms that underpin these physiological shifts, I collaborate with Dr Bridgett vonHoldt (Princeton University) to characterize DNA methylation patterns in leaf tissue, focusing on genetic sequences that are linked to fundamental photosynthetic processes like enzyme kinetics and photosystem structure and function.

heritable plant intelligence?

I am also investigating how saplings might be “primed” for the environment that their mother experienced. At the University of Nevada, Reno, we reared ca. 500 acacias from seeds collected in our full-factorial field experiment. During germination, 2/3 of our seeds were treated with zebularine, a cytosine analog that demethylates large sections of the tree genome—if DNA methylation can imbue saplings with a limited “epigenetic memory” from their mother, then zebularine functions as a “memory eraser”.

By conducting the same physiological and molecular analyses on both mature trees and saplings, we are testing if inherited epigenetic signatures can prime plant offspring with a physiology that matches their mother’s current ant mutualist, and thus may stabilize ant-plant symbiosis across generations.

“Strongly encouraging” a Crematogaster mimosae ant colony to take over a neighboring tree artificially cleared of its former Tetraponera penzigi colony. Fortunately, acacia trees are flexible and the ants can’t chew through rope.

With high winds, elephant patrols, and tricky leaf shapes, it’s not often that we record a leaf CO2-assimilation response curve with no hands!

So far from home and the mother tree, whistling acacia saplings yet produce leaves with similar photosynthetic patterns as their mother!


the belowground consequences of aboveground mutualisms

During my postdoc, I expanded my research focus to include belowground tree physiology. Primarily, we have investigated this at Ol Pejeta Conservancy, where ant mutualists have been displaced from whistling acacias by the big-headed ant (Pheidole megacephala) introduced by humans to the region in the ca. early 2000s. Big-headed ants mount an overwhelming assault on native ant mutualists and eventually leave large swathes of acacias unoccupied and unprotected (a stunning event to witness). The scenario at Ol Pejeta affords us an opportunity to study ant-plant root investment across a landscape with variable rainfall patterns, experimentally manipulated ungulate herbivory, and an 8-years-long monitoring project comparing native ant-protected and P. megacephala-occupied tree stands (see our preprint, which is updated regularly!)

My early belowground work showed that whistling acacias alter root distributions to avoid soil bioturbation by P. megacephala, and that root density appears to decline as a result of P. megacephala introduction; however, this work is lethal to the tree, which limits our ability to make long-term predictions for tree root production under different rainfall and ungulate herbivory conditions.

A whistling acacia mid-excavation: he’s dead, Jim. There must be a better way to do this…

More recently, I have led a team of collaborators to install minirhizotron tubes in the root systems of whistling acacia trees throughout Ol Pejeta Conservancy. These tubes allow us to repeatedly estimate fine root surface area of trees on both sides of the invasion front, in open and herbivore-excluded tree stands, and throughout wet and dry periods in this semi-arid savanna!