Invading pines get help

What makes for a successful invasion?  Is it better to invade with a small, fast moving force or a large, but less mobile force?  Should the invaders be capable of operating independently, or should they have partners (or make partnerships easily) with the existing population? Should resources be allocated to defending the individuals that make up the invasion force, or instead be allocated to recruiting large numbers of less-well-defended invaders?  While military strategists are confounded by these questions, pine trees have solved them. The solution is:

Z-score = 23.39 – 0.63(SM)1/2 -3.88(JP)1/2 -1.09(SC)

This equation was derived about 25 years ago by Marcel Rejmánek and David Richardson who wanted to know what plant attributes were associated with whether pine trees invaded new areas successfully.  They contrasted 12 species that had made successful invasions with 12 species who were primarily noninvasive, and derived the z-score as a quantitative measure of what attributes the invasive species shared.  A higher z-score was correlated with higher invasiveness.  Qualitatively, this equation tells us that invasiveness is correlated with small seed mass (SM), a short juvenile period (JP) and a short interval of time between large seed crops (SC). 

Pine seeds vary in size and number across species. Credit: Jaime Moyano.

Shift to the present time (or at least the recent past). Jaime Moyano and his colleagues were puzzling over whether it was better for these invaders to be capable of operating independently, or whether they should depend on partners.  Ecologists had assumed that independence was a good idea for invaders, and had framed an “ideal weed hypothesis” that plant species that depend on mutualisms are less prone to invade.  Common mutualisms for plants include association with pollinators, seed dispersers and fungi (mycorrhizae).

Pinus contorta (lodgepole pine) invades a forest near Christchurch, New Zealand. Credit: Martin Nuñez.

Moyano and his colleagues tested a prediction of the ideal weed hypothesis by going through the literature to see whether pine species seedlings with higher invasiveness are less dependent on mutualisms with ectomycorrhizal fungi (EMF).  EMF are an association between plant roots and fungi in which the fungal hyphae form a sheath around the root’s exterior and suck up nutrients which they may share with the plant. To test this prediction, the researchers compiled a database of 1206 data points in 34 species based on studies where researchers evaluated how pine seedlings grew with and without EMF inoculation. For each study, they calculated an effect size of EMF as equal to the ln(EMFP/EMFA), where EMFP is seedling biomass with EMF present , and EMFA is seedling biomass with EMF absent.  So a higher effect size indicates that EMF improves seedling growth.

All the pieces were together – all that was left was to do the analysis.  The prediction of the ideal weed hypothesis was that the most invasive species – the species with the highest Z-score – would be expected to have the lowest EMF effect size (be less dependent on mutualism).  The researchers discovered…exactly the opposite.  In general, invasive pines depended heavily on EMF mutualisms to aid seedling growth, while non-invasive pines were less likely to benefit from the services of EMF (top graph below).

EMF effect size in relation to invasiveness (Z score) (top graph). EMF effect size in relation to seed mass (bottom graph).

In addition, the researchers discovered that species with smaller seeds benefitted more from EMF (bottom graph above).  Initially, they were puzzled by these findings that conflicted with conventional expectations.  But then it started making sense…

Parental investment theory tells us that parents have a limited amount of resources that they can allocate to their offspring.  Given this limitation, some plant species make a small number of large seeds that are endowed with large stores of nutrients that the baby can use while germinating and a thick seed coat to protect it.  The downside of this approach is that the large seed might not disperse very far from its parent and may get shaded out by it.  Other plant species make large numbers of very small seeds that are very poorly supplied with nutrients.  The upside of this approach is that the seeds can be blown to new locations that might be ripe for germination (pine seeds are equipped with wings that facilitate traveling in the breeze when released).  The downside of this approach is that germinating seeds might run out of nutrients before they establish themselves.  This selects for a strong dependence on quickly establishing mutualisms to facilitate nutrient intake from the environment. All pines trees ultimately establish EMF, but the smaller-seeded most invasive plants benefit more from EMF early in development, and thus can travel long distances and still get enough nutrients to invade new habitats.

Lodgepole pines invade a forest in Patagonia. This species produces numerous tiny seeds and is highly invasive. Credit: Martin Nuñez.

The question then becomes, how generalizable are these results to other species and other types of mutualisms? The pattern of large seeds showing decreasing response to EMF has been found in some plant families but not others. There are not a lot of data on the relationship between plant invasiveness and their dependence on other types of mutualisms such as pollinators and animal seed dispersers. Moyano and his colleagues caution us that many factors are involved in biological invasions, which makes it very difficult to anticipate which species will be successful invaders.  

note: the paper that describes this research is from the journal Ecology. The reference is Moyano, J., M. A. Rodriguez-Cabal, and M. A. Nunez. 2020. Highly invasive tree species are more dependent on mutualisms. Ecology 101(5):e02997. 10.1002/ecy.2997. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2020 by the Ecological Society of America. All rights reserved.

Hot ants defend plants from elephants

I’ve lost a lot of sleep over ants.  As a spider researcher, I often placed ants on spiderwebs to lure my spiders out of their underground retreats and onto their webs. The problem was that these harvester ants (Pogonmyrmex species) were fierce, so to minimize damage to myself, I was forced to capture them in the very early morning, when they and (alas) I were very sluggish.

acacias_thorn copy

Swollen thorn (domatia) that serves as living quarters for acacia ants. Credit: T. Palmer.

Todd Palmer has worked with ants for many years, including research on ant-plant mutualisms in which acacia trees provide domatia (swollen thorns) as ant living quarters and extrafloral nectaries as ant food, while ants provide protection from herbivores such as elephants, kudus and steenboks.

Similar to my efforts with ants and spiders, Palmer wanted to reduce ant-induced damage to himself and his colleagues, so he often took advantage of early morning ant sluggishness for purposes of manipulating acacia trees. On the other hand, if he wanted to study aggressive responses, he learned that mid-day was best. Recognizing the daily patterns of ant activity got Palmer, Ryan Tamashiro (Palmer’s undergraduate research student) and Patrick Milligan (Palmer’s graduate student) thinking about how these different levels of activity would influence herbivores, many of which tend to be most active during dawn and dusk when temperatures are low and ants are relatively sluggish.

Elephant side

Elephants are major herbivores that can cause enormous damage to acacia trees. Credit: T. Palmer.

Four species of ants live in domatia on branches of Acacia drepanolobium, the dominant tree species at Mpala Research Centre in Laikipia, Kenya.

Acdr habitat

A grove of Acacia drepanolobium. Credit: T. Palmer.

In order of relative abundance, the ant species are Crematogaster mimosae (52%), C. sjostedti (18%), Tetraponera penzigi (16%) and C. nigriceps (15%).  Previous research showed that C. mimosae and C. nigriceps are the two most effective acacia defenders.

Cnigriceps copy

Crematogaster nigriceps on an acacia tree. Credit: T. Palmer.

Ants are poikilotherms, whose body temperature, and presumably their activity levels, fluctuate with environmental temperature.  As these ants live in acacia branches, the first order of business became to determine how branch temperature fluctuated with time of day during the 21 days of data collection.  Not surprisingly, branch temperature peaked at mid-day, and was lowest at dawn and dusk (temperatures were not measured during the night).

TamashiroFig S!

Variation in branch surface temperature with time of day. Horizontal bars are median values; boxes are first and third quartiles.

Tamashiro, Milligan and Palmer next asked how ant activity level related to branch temperature.  Different ant species don’t get along so well, so each tree hosted only one ant species.  For each tree surveyed, the researchers counted the number of ants that passed over a 5 cm branch segment during a 30 second time period (they did this twice for each tree),  The researchers discovered a strong correlation between branch surface temperature and baseline ant activity, with C. mimosae and C. nigriceps showing greatest activity levels at all temperatures, which increased sharply at higher temperatures.

TamashiroFig 1a

Ant activity levels in relation to branch surface temperature. Shaded areas are 95% confidence intervals for each species.

Do higher temperatures cause a stronger aggressive response to predators or other disturbances? Tamashiro and his colleagues tested this by rapidly sliding a gloved hand over a 15 cm segment of a branch three times and then resting the gloved hand on the branch for 30 s.  They then removed the glove and counted the number of ants that had swarmed onto the glove.  Again, C. mimosae and C. nigriceps showed the strongest aggressive response, which increased sharply with temperature

TamashiroFig 1b

Aggressive swarming by ants in relation to branch surface temperature. Shaded areas are 95% confidence intervals for each species.

While a gloved hand is a nice surrogate for predators, the researchers wanted to know how the ants would respond to a real predator, and whether the response was temperature dependent.  At the same time, they wanted to determine whether the predator would change its behavior in response to changes in ant defensive behavior at different temperatures.  They used eight somali goats (Capra aegagrus hircus) as their predators, and C. mimosae as the focal ant species for these trials.

Cpl. Paula M. Fitzgerald, USMC - United States Department of Defense

Somali goats in Ali Sabieh, Djibouti. Credit: Cpl. Paula M. Fitzgerald, USMC – United States Department of Defense.

The researchers chose eight trees of similar size for their experiment, and removed ants from four of the trees by spraying them with a short-lived insecticide, and preventing ant recolonization by spreading a layer of ultra-sticky solution (Tanglefoot) around the based of each treated tree.  Goats were allowed to feed for five minutes.


Number of bites (top graph) and time spent feeding (bottom graph) by goats in relation to branch surface temperature. Shaded area is 95% confidence interval.

Tamashiro and his colleagues measured the number of bites taken (top graph) and the amount of time spent feeding (bottom graph) at different branch temperatures.  Both measures of goat feeding were not influenced by branch temperature if there were no ants on the trees (blue lines and points).  But if ants were present (red lines and points), goat feeding decreased sharply with increasing branch temperature, presumably reflecting more aggressive ant defense of the plants.

These findings have important implications for acacia trees, which are a critical species in the sub-Saharan ecosystem.  Previous research has shown that elephant damage is strongly influenced by the number of swarming ants on a particular tree; a greater number of swarming ants are associated with less elephant damage. Many vertebrate browsers feed throughout the day, but may feed preferentially at dawn and dusk, when temperatures are cooler and ant-defense is weakest. Browsing is particularly problematic for acacia saplings, which are usually attacked by small-bodied vertebrates such as steenbok, which forage primarily at night when ants are least active.  Thus the effectiveness of ant defense may be compromised by mismatches between vertebrate activity periods and ant activity periods.

note: the paper that describes this research is from the journal Ecology. The reference is Tamashiro, R. A., P. D. Milligan, and T. M. Palmer. 2019. Left out in the cold: temperature-dependence of defense in an African ant–plant mutualism. Ecology 100(6): e02712. 10.1002/ecy.2712 . Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.



Fires foster biological diversity on the African savanna

As an ecology student back in days of yore, I was introduced to the classic mutualism between ants and swollen-thorn acacia trees. In this mutually beneficial relationship, ants protect acacia trees by biting and projecting very smelly substances at hungry herbivores, and by pruning encroaching branches of plant competitors. In return for these services, acacia trees provide the ants with homes in the form of swollen thorns, and in some cases also provide food for their defenders.


Swollen thorns of Acacia drepanlobium occupied by C. nigriceps. Credit: Ryan L. Sensenig.

I always assumed there were limits to what these ants could do. I knew that elephants were a constant problem for trees trying to get established on the African savanna. I figured, wrongly, that ants could not do much to counter a determined thick-skinned elephant. But as Ryan Sensenig describes, ants will swarm any intruding elephant, rushing into the elephant’s very sensitive trunk and mouth, biting it and, in some cases, exuding a chemical compound that is very offensive to an elephant’s keen sense of smell. So don’t mess with these ants if you can help it!


The Laikipia Plateau has one of the few growing elephant populations in East Africa. Credit: Ryan L. Sensenig.

Fires play an important role in savanna ecosystems, killing many trees before they can get established, and creating a mosaic of burned and unburned areas which vary in grass quality and quantity, and in the abundance of acacia trees (and other species as well). Recently burned grasslands tend to be lower in grass abundance and higher in grass nutrient levels. In a previous study of controlled burns, Sensenig and his colleagues showed that larger animals, such as elephants, tended to graze in unburned areas, which had more grass – albeit of lower quality. Returning seven years after the burn, he was surprised to find that elephants, which eat both trees and grass, had shifted to the burned sites in preference to unburned sites. He thus wondered whether fire was having an impact on the ant-acacia mutualisms that defend acacias from elephants and other large herbivores.


Sunset strikes an Acacia xanthophloea on Mpala Research Centre in Laikipia, Kenya. Credit: Ryan L. Sensenig.

Ants do not share trees. In Mpala Research Centre in the Laikipia Plateau of Kenya, there are four mutually-exclusive species of ants that live in Acacia drepanolobium trees: Crematogaster sjostedti, C. mimosae, C. nigriceps, and Tetraponera penzigi.

Sensenig and his colleagues wanted to know whether the controlled burns had a long-lasting effect on ant species distribution on acacia trees. The researchers surveyed 12 plots that had been burned seven years previously and an equal number of unburned plots to see how burns affected which ant species were present.


Goshen College research students estimate ant densities on Acacia drepanolobium trees in the Kenya Longterm Exclosure Experiment. Credit: Ryan L. Sensenig.

They found that C. nigriceps was more common in acacias from burned areas while the other three species were more common in trees from unburned areas.


Why were there more C. nigriceps ants in previously burned areas? One explanation is that perhaps C. nigriceps is better at avoiding getting burned by fire, or else is better at recolonizing after a fire. To look for species difference in response to fire, the researchers simulated fires by burning elephant dung and dried grass in 3-gallon metal buckets, creating a small sustained smoke source. They stationed observers every 50 meters along a 500 meter transect for the first experiment, and a 1.8 km transect for the second experiment. They then measured ant-evacuation rate by counting the number of ants moving down the trunk. There were some very pronounced differences, with C. nigriceps having the highest evacuation rate, C. mimosae also showing a strong smoke response, and the other two species showing little evidence of any response.


Evacuation rate for each species in response to smoke.

C. mimosae generally prevails when it battles a colony of C. nigriceps. These results indicate that the subordinate C. nigriceps is able to maintain its presence in the community, in part, by taking advantage of its superior performance when it encounters a fire. The researchers also found some evidence that C. nigriceps is better at recolonizing after a fire than is C. mimosae. So despite being the subordinate species, C. nigriceps is abundant in this ecosystem.

Returning to those elephants, the researchers describe one final experiment in which some plots had a series of fences that excluded herbivores, while other plots were open to herbivores, including elephants.


In this experiment, as well, there were burned and unburned plots. In general, there were more ants present when herbivores were present, as the trees invested more in swollen thorns and in ant food (in the form of nectar) to attract protective ants. In addition, ants were more abundant in unburned plots than in plots that had been previously burned, with the exception of C. nigriceps when herbivores were excluded.

Ecologists have long known that fire maintains savanna ecosystems by preventing the grasslands from being overgrown by trees. This study shows that fires shift ant community structure in favor of the subordinate ant species (C. nigriceps), resulting in a higher diversity of ant species overall. The researchers suggest that if fires become more common in savannas, elephants may become more attracted to acacias that harbor a reduced (or nonexistent) cast of defenders, which could lead to a further reduction in the abundance of acacia trees and their mutualistic ants.

note: the paper that describes this research is from the journal Ecology. The reference is Sensenig, R. L., Kimuyu, D. K., Ruiz Guajardo, J. C., Veblen, K. E., Riginos, C., & Young, T. P. (2017). Fire disturbance disrupts an acacia ant–plant mutualism in favor of a subordinate ant species. Ecology, 98(5), 1455-1464.Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.

Nitrogen nurses

Alfred Lord Tennyson puzzled over the conflict between love as a foundation of Christianity, and the apparent violence of the natural world.

Who trusted God was love indeed

And love Creation’s final law

Tho’ nature, red in tooth and claw

With ravine, shriek’d against his creed

The good poet would be relieved to learn that modern ecologists have uncovered a softer, gentler side of the natural world – facilitative interactions, in which one species (the facilitator) helps out a second species. In many, but not all, cases, the second species also helps out the first species. Ecologists describe these mutually-beneficial interactions as mutualisms. As an example, Mimosa luisana is a mutualist with Rhizobium bacteria, providing the bacteria with root nodules to live in and carbohydrates as an energy source, while receiving ammonia (NH3) that the bacteria fix (convert) from atmospheric N2. A second type of mutualism, a mycorrhizal association, is a very common facilitative interaction between plants and fungi, which grow alongside or within the plant roots. In many mycorrhizal associations, the plant provides carbohydrates to the fungi, which import and share nutrients and water.

Mimosa plant

Mimosa luisana. Credit: Leticia Soriano Flores, algunos derechos reservados (CC BY-NC)

Alicia Montesinos-Navarro and her colleagues, and researchers before them, noticed that in arid and semi-arid environments, plant-plant facilitation was most common between two plant species that were structurally and functionally very distinct, and that tended to be very distantly related to each other. In particular, M. luisana tends to associate with many different species of plants, including many cacti that look nothing like it, and are very distantly related. M. luisana is called a nurse plant, because other species tend to grow under its branches, which shade the soil and reduce water loss from evaporation. Recent work by Montesinos-Navarro and her colleagues showed another benefit of nursing – some plants receive nitrogen from these nurse plants via the network of mycorrhizal fungi.

Traditionally, ecologists have argued that associations between distantly-related plants occur because the plants have very different ecological niches, using different resources in different ways, so they are not competing with each other. Montesinos-Navarro and her colleagues argue that a second process might be important in this and other systems. Close relatives of M. luisana might tend to have high nitrogen levels and thus not benefit from nitrogen transfer from the nurse plant, while more distantly-related plants might tend to have lower nitrogen levels and thus benefit from any nitrogen arriving from M. luisana. They explored this hypothesis in the semi-arid Valley of Zapotitlan in the state of Puebla, Mexico.


Study site dominated by the columnar cactus Neobuxbaimia tetezo, Credit: Alicia Montesinos-Navarro.

Measuring nitrogen transfer from the nurse plant to the recipient is not the world’s easiest task. Fortunately there is a rare form or isotope of nitrogen, 15N, which can be distinguished from the more common 14N. The researchers soaked M. luisana leaves in urea that was made up of primarily 15N, and the leaves took up the urea. Consequently, any exported nitrogen would contain a disproportionately high concentration of 15N, resulting in high 15N levels in the recipient plant. They then measured 15N levels in 14 different species of plants that used M. luisana as their nurse. The researchers were able to test two hypotheses. First, they could see whether close relatives to M. luisana tended to have higher N-levels than more distantly related species. Second they could see whether distant relatives tended to receive more nitrogen from nurse plants than did close relatives.


Mimosa luisana branch taking up 15N-labeled urea. Credit: Alicia Montesinos-Navarro.

The graph below summarizes the results. The y-axis measures how much the 15N level in the facilitated species increased by the end of the experiment (15 days). The x-axis measures the evolutionary relationship between M. luisana and the facilitated species – more precisely how long ago the two species shared a common ancestor. Lastly, the size of the dot measures the initial difference in leaf N-levels between M. luisana and the facilitated plant.

Ecology Fig 2

Influence of evolutionary relationship between M. luisana and the facilitated species (x- axis) and nitrogen gradient – the initial difference in nitrogen levels between the two species (size of dots) on the amount of nitrogen imported by the facilitated species.

Several trends are evident. First, close relatives of M. luisana tended to have similar leaf nitrogen values to M. luisana (medium sized dots), while distant relatives tended to have much less nitrogen than M. luisana (largest dots). Second, the most distant relatives tended to have the greatest increase in their 15N levels, which indicates that they received the greatest nitrogen export from their nurses.

One question is how the nitrogen is transported. Montesinos-Navarro and her colleagues describe how they treated soil with a fungicide, presumably killing the mycorrhizae, which resulted in a substantial reduction in nitrogen transport. This suggests that the mycorrhizal network is important for nitrogen transport. But more pressing is what do the nurse plants get out of the relationship. The researchers suggest that the recipient plants may provide M. luisana with either water or phosphorus, both of which may be in short supply in arid environments.

This study indicates that we need to look beyond traditional niche theory, and may need to  dig deeper to understand the structure of plant communities, and how facilitative interactions can explain the coexistence of very distantly related plants.

note: the paper that describes this research is from the journal Ecology. The reference is MontesinosNavarro, A., Verdú, M., Querejeta, J. I., & ValienteBanuet, A. (2017). Nurse plants transfer more nitrogen to distantly related species. Ecology, 98(5), 1300-1310. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.