Savanna plant survival: hanging out in the right crowd

Tyler Coverdale first visited the Mpala Research Centre in Laikipia, Kenya in 2013, and immediately became painfully aware of the abundant spiny and thorny plants that cover the savanna.  Spines help defend the plants from voracious elephants, giraffes and numerous other herbivores that depend on vegetation for their sustenance.


Camels browsing on  Barleria trispinosa at Mpala Research Centre, Kenya. Credit Tyler Coverdale.

Acacia trees such as Acacia etbaica (left foreground below) dominate the landscape, and may be associated with smaller shrubs, such as Barleria trispinosa. In the photo below, there is one B. trispinosa plant immediately below (on the right side) the acacia tree, and a second B. trispinosa plant to its right, more out in the open.  Coverdale realized that being situated immediately below a spiny acacia tree might be advantageous to B. trispinosa, which could be protected from the ravages of elephants and giraffes by the acacia thorns .

MRC landscape

Credit: Tyler Coverdale.

As you might guess by its name, B. trispinosa is itself a very spiny plant, which should help protect it from browsers.  Nonetheless, it still gets eaten, so Coverdale and his colleagues explored whether being under acacias would reduce how much it, and two other related species, got browsed.

Barleria trispinosa

Barleria trispinosa out in the open. Credit: Tyler Coverdale.

The first study was observational – a survey of the damage three species of Barleria suffered when they were under (associated with) acacia trees vs. unassociated with acacia trees. For each Barleria species, the researchers haphazardly chose 10 stems from eight associated and eight unassociated plants, and measured the proportion of these stems that showed physical evidence of being browsed.  As the figure below shows, browsing was sharply lower for each species when it was associated with an acacia plant.


Percentage of stems damaged by browsers for three Barleria species in relation to whether they were associated or unassociated with an acacia tree.* indicates significant differences between means in all figures.

The understory plant community associated with acacias is much denser than the plant community out in the open, so the researchers wondered whether it was the acacia itself, or the other plants associated with it, that were providing protection. They set up an experiment using focal B. trispinosa plants with four treatments (A) unmanipulated control, (B) overstory removal, (C) overstory + understory removal, (D) a procedural control with overstory + understory removal, with the focal plant enclosed in a metal cage to protect it from predators (see Figure below).


Coverdale and his colleagues ran the experiment for one month.  They discovered that removing overhanging acacia branches sharply increased herbivory, but the additional removal of understory neighbors had little additional effect.  Both the unmanipulated controls and procedural controls were unaffected.


Change in % of stems browsed for (A) unmanipulated control (left bar), (B) overstory removal (second from left bar), (C) overstory + understory removal (second from right bar), (D) a procedural control (right bar).  Different letters above bars indicate significant differences between the mean values.

The researchers then investigated how useful these spines are to unassociated B. trispinosa plants. They set up another experiment with four types of spine treatments: (A) unmanipulated controls, (B) 50% spine removal, (C) 100% spine removal, (D) procedural control with 100% spine removal + enclosure within a predator-proof cage. These cages were vandalized shortly after the experiment was set up, so the researchers chose eight plants from a nearby plot (that had all predators excluded for a different experiment) as their procedural control. They discovered that spines are very useful to protect against predators in unassociated B. trispinosa.


Change in % of stems browsed for (A) unmanipulated control (left bar), (B) 50% spine removal (second from left bar), (C) all spines removed (second from right bar), (D) procedural control (right bar).

If you were a plant living under the protection of an acacia tree, it would make sense for you to reduce your investment in thorns, so you could allocate more resources to growth and reproduction.  Does Barleria do this?


Several lines of evidence indicate that all three Barleria species reduce their investment in spines when associated with an acacia. First, a survey of spine density shows a reduced number of spines for all three species when they were associated with acacia trees (top graph).  Second, the spines that are present are significantly shorter in Barleria species associated with acacia trees (middle graph).  In a final survey, Coverdale and his colleagues cut all of the spines off of associated and unassociated Barleria.  For each plant, the researchers calculated the dry weight of spines and of all the other plant tissue.  For each Barleria species, the defensive investment – the ratio of spines to total mass, was substantially reduced in acacia-associated plants in comparison to unassociated plants (bottom graph).

Lastly, can plants react adaptively to browsing?  In other words, will understory plants produce more thorns if they are browsed?  To explore this question, the researchers used scissors to simulate moderate (25%) or heavy (50%) browsing.  They discovered a significant increase in spines produced by unassociated plants one month after clipping. Ecologists call this an induced defense. This induced defense is strongly suppressed in plants that have lived under the protection of acacia trees – in fact there was no significant response to experimental browsing in acacia-associated B. trispinosa plants. The researchers don’t know how long this suppression of induced responses persists. Would browsing induce increased spine growth in B. trispinosa six months, a year or two years after its protective acacia tree died?

Coverdale and his colleagues conclude that the overall benefit of association is positive to the plant populations.  Their studies show better survival and higher reproductive rates of acacia-associated understory plants. There is probably a cost associated with too many offspring competing for resources within a small area, as seedlings tend to grow within 1 meter of their parents.  However the reduction in defense costs probably overrides this cost of competition, leading to increased population size.  The researchers suggest a long-term study of population growth rates for acacia-associated and unassociated plants for several different species to see how general these effects are, and to explore whether other factors, such as soil moisture and nutrient levels influence the allocation and induction of defensive structures such as spines and thorns.

note: the paper that describes this research is from the journal Ecology. The reference is Coverdale, T. C., Goheen, J. R., Palmer, T. M. and Pringle, R. M. (2018), Good neighbors make good defenses: associational refuges reduce defense investment in African savanna plants. Ecology, 99: 1724-1736. doi:10.1002/ecy.2397. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Seaweed defense – location, location, location.

If you’re ever feeling sorry for yourself, you should know that things could have been much worse; you could have been the brown seaweed, Silvetia compressa. So many problems!  Ocean waves come crashing over you, threatening to pull you off your life-sustaining substrate.  Ocean tides recede, exposing you to harsh sun and dangerously dry conditions. Perhaps worst of all, the fearsome predator Tegula funebralis eats away at your body, and you are powerless to defend yourself from its savage ravages.


Tegula snails chomp away on Silvetia seaweed in northern California. Credit: Emily Jones.

As it turns out, Silvetia is not so powerless after all.  After being partially grazed by Tegula, the seaweed can induce defenses that reduce its palatability.  From prior work, Emily Jones noticed that seaweed from northern California shorelines was much more sensitive to grazing than was seaweed from southern California shorelines.  It took fewer grazing snails to elicit palatability reduction in northern Silvetia than it did in southern Silvetia. She decided to focus her PhD work with Jeremy Long on documenting these geographic differences, and figuring out why they exist.


Emily Matthews (near) and Grace Ha (far) survey snails and seaweed in a northern California site. Credit: Emily Jones.

Environmental conditions vary along the California coast.  Northern seaweed populations experience cooler temperatures (air ~5-20 °C; water ~10-12 °C) and more nutrients (nitrate levels up to 40 umol/L) than do southern populations (air 5-37 °C; water ~14-20 °C; nitrate levels < 2 umol/L). In addition, Jones and Long surveyed Tegula abundance at three northern California and three southern California sites, counting every snail in 20 quadrats placed in the low, mid and high intertidal zone at each of the six sites (360 0.25 X 0.25m quadrats in total) .  They discovered that seaweed was much more likely to encounter Tegula along northern coastlines.


Percent of plots with Tegula snails in northern sites (Stornetta, Moat Creek and Sea Ranch – blue bars) and southern sites (Coast, Calumet and Cabrillo – orange bars). High, Mid and Low refer to location within the intertidal zone (high is closest to shore and regularly exposed at low tide).

Given these differences in snail abundance, we can now understand why Silvetia is more sensitive in its northern range to Tegula grazing.  But how strong are these differences in sensitivity? Jones and Long developed a simple paired-choice feeding preference assay to test for differences in palatability. At each location (north and south), the researchers gave test snails a choice between feeding on seaweed that had been previously grazed by either 1, 4, 7, 10 or 13 Tegula snails, or to feed on seaweed with no grazing history.  The test snails grazed for five days, and the researchers measured the amount of seaweed consumed for each group. They discovered that even a little bit of previous grazing (the 1-snail treatment) made northern test snails prefer non-grazed northern Silvetia, while only high levels of previous grazing (the 10 and 13-snail treatments) had similar effects on southern snails tested on southern Silvetia.


Amount of previously-grazed and non-grazed Silvetia eaten by Tegula in paired choice tests. (Top) Northern Selvetia, (Bottom) Southern Silvetia. Error bars are 1SE. * indicates significant differences in consumption rate.

These findings raised the question of whether the cooler and more nutrient-rich environmental conditions at the northern site were somehow causing this difference in consumption of previously-grazed seaweed.  The researchers designed a series of common garden experiments at the Bodega Marine Laboratory, in which seaweed from both locations were tested in the same environment.  Silvetia was exposed to grazing by two snails, or by no snails for 14 days. When test snails were given the choice of non-grazed or previously-grazed northern Silvetia, they much preferred eating non-grazed Silvetia. In contrast, they showed no preference when given a similar choice between non-grazed or previously-grazed southern Silvetia. This indicates that seaweed from the north are responding more to grazing by reducing palatability than are seaweed from the southern locations.


Amount of previously-grazed and non-grazed northern and southern Silvetia eaten by Tegula in paired choice tests.

In theory, there could be a tradeoff between induced defenses, such as reduction in palatability in response to grazing, and constitutive defenses, which an organism expresses all of the time.  Examples of constitutive defenses are thorns or spines in plants, and cryptic coloration or body shape in many insects.  Jones and Long found no evidence for such a tradeoff; in contrast southern Silvetia actually had lower levels of constitutive defenses, as both northern and southern Tegula strongly preferred eating southern Silvetia in paired choice tests.


Amount of northern and southern Silvetia eaten by northern and southern Tegula in paired choice tests.

These geographic differences in seaweed sensitivity to grazing are probably due to long-term differences in environmental history.  Southern Silvetia seaweeds live in stressful conditions (high temperatures and low nutrients), and the physiological cost of mounting an induced defense against low and moderate levels of grazing may be too high to be worthwhile. We also don’t know what the overall grazing rates are in the north versus the south, and importantly, how variable the grazing rates are in each location.  Highly variable grazing rates would select for a strong set of induced responses, which could be turned on and off as needed, allowing seaweed, or any plant, to defend itself against new or more hungry herbivores moving into their environment.

note: the paper that describes this research is from the journal Ecology. The reference is Jones, Emily and Long, Jeremy D. 2018. Geographic variation in the sensitivity of an herbivore-induced seaweed defense. Ecology. doi: 10.1002/ecy.2407. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.