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). 

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).

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(EMF_P/EMF_A), where EMF_P is seedling biomass with EMF present , and EMF_A 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).

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.

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.