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.

Rewilding tropical forests: dung is the key

Rewilding means different things to different people. Basically, it involves restoring a species, or several species to an area from which they have been extirpated by humans. Conservation biologists might study the population size and distribution of the returned species, ecologists might focus on interactions between the returned species and other species, while anthropologists might investigate how humans in the area are adjusting to having a new species in their lives.  One of the most famous examples of rewilding is the return of gray wolves to the Greater Yellowstone Ecosystem in western U.S.A., which can be looked at from the perspective of how the wolf populations are doing numerically, how they affect their prey (elk) or their prey’s prey (willow and aspen in the case of elk), and how they affect ranchers in the surrounding areas.

Conservation ecologists have begun a major rewilding program in Tijuca National Park in Brazil, introducing agoutis in 2010 and brown howler monkeys (Alouatta guariba clamitans) in 2015. Howler monkeys were extirpated from this park over a century ago, so ecologists worried that the monkeys might interact with the remaining species in unexpected ways.  For example, this forest hosts several species of invasive fruit trees, such as the jackfruit (Artocarpus heterophyllus). Luisa Genes and her colleagues were concerned that howler monkeys might eat fruits from these trees, and poop out the seeds in new forest locations, causing the invasive species to spread more rapidly.

GenesHowler1

Introduced howler monkey holding the second baby born to her in the forest. Credit: L. Genes.

Even a disturbed rainforest such as Tijuca National Park hosts a large number of plant species, so the interactions can be complex and difficult to study.  As is so often the case in ecology, one very important complex of interactions involves poop.  Specifically, howler monkeys eat fruit off of trees, and poop the seeds out, usually at a new location, effectively dispersing the seeds.  But there is a second link in this seed dispersal interaction.  Twenty-one species of dung beetles use howler monkey poop for food for themselves and their offspring, breaking off small sections into balls and rolling the balls to a new location.  This process of secondary dispersal is nice for the beetles, but also for the seeds within the balls, which can now germinate in a new location without competing with the large number of seeds in the original howler monkey pile.

RafaelBrixDungBeetles

Two dung beetles battle over a dung ball. Credit: Rafael Brix.

Genes and her colleagues were interested in two basic questions.  First, were the howler monkeys eating fruit from a few select tree species, or were they eating from many different types of trees, thereby dispersing seeds from many species?  Before releasing the monkeys (two females and two males), they attached radio transmitters to the monkeys so they could easily track them, and note what they ate.  Based on 337 hours of observation, the howler monkeys ate fruit from 60 different tree species out of 330 possible species in the forest (18.2%).  This is an underestimation of actual howler monkey contribution to seed dispersal, because the researchers observed the monkeys for a relatively brief time, and fruit consumption by the monkeys should increase over time as the population of monkeys (and possibly tree diversity), continues to increase.

bugio reintroduzido no PN Tijuca 2015

Male howler monkey released in 2016.  Note the radio transmitter on its right rear leg. Credit: L. Genes.

The second question is whether secondary dispersal by dung beetles was reestablished following reintroduction of howler monkeys.  To answer this question quantitatively, Genes and her colleagues set up an experiment that used plastic beads of various sizes instead of seeds. The researchers set up circular plots of 1m diameter with 70 grams of howler monkey poop in the middle.  Each pile was mixed with seeds (actually beads) of four different sizes (3, 6, 10 and 14 mm diameters) to mimic the range of seed sizes. The researchers measured secondary seed dispersal by returning 24 hours later and counting the remaining beads, reasoning that the rest had been moved by dung beetles (along with the poop) to a new location.

Genes and her colleagues discovered that the median rate of seed dispersal (bead removal) was 69% with larger seeds being moved at a significantly lower rate than smaller seeds.  Thus secondary seed dispersal by dung beetles was still operating in this ecosystem even after howler monkeys had been absent for over 100 years.

GenesdFig2

Removal rate of beads (seed mimics) from dung piles by dung beetles in relation to bead size.  Different letters above treatments indicate statistically significant differences between treatments. 

Overall, ecological interactions among howler monkeys, plants, and dung beetles were rapidly reestablished once howler monkeys were reintroduced to the community.  There are plans to introduce five more howler monkeys this year, which should further increase beneficial seed dispersal, and hopefully allow plant diversity to increase as well.  One problematic observation was that howler monkeys also ate invasive jackfruit, which could promote its dispersal within the community.

Luciano_Candisani_38-1

Luisa Genes monitors howler monkeys in the forest. Despite its apparent lushness, the forest still lacks many species and interactions that you would expect to find in an intact forest. Credit: L. Candisani.

The researchers discovered only 21 species of dung beetles, which was somewhat lower than other studies have found.  It is probable that conversion of this land into farmland in the 19thcentury led to the decline and/or demise of some dung beetle species.  With reintroduction of howler monkeys, and the passage of time, Genes and her colleagues expect that this rewilding effort should lead to a more robust ecosystem, with increased howler monkey populations supporting high dung beetle abundance and diversity, and more effective dispersal of many plant species. To understand the overall impact on forests, the researchers recommend that future studies should compare seedling survival and forest regeneration in areas where howler monkeys were reintroduced to areas where howler monkeys are still missing.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Genes, L. , Fernandez, F. A., Vaz‐de‐Mello, F. Z., da Rosa, P. , Fernandez, E. and Pires, A. S. (2019), Effects of howler monkey reintroduction on ecological interactions and processes. Conservation Biology, 33: 88-98. doi:10.1111/cobi.13188. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2019 by the Society for Conservation Biology. All rights reserved.

Changing climate promotes prolific plants and satiated consumers

Plants in Sweden can have a difficult life, but climate change has provided a more benign environment for some of them, including the white swallow-wort, Vincetoxicum hirundinaria. This perennial herb grows in patches in sun-exposed rocky areas, in forests located below cliffs, and along the edges of wooded areas. The plant forms clumps that are heavily laden with flowers in June and July, and creates pod-like fruits in July and August

Solbreck1AB

Vincetoxicum hirundinaria growing in rocky outcrop (top photo). Vincetoxicum pods releasing their wind-dispersed seeds (bottom photo).

Christer Solbreck has had a lifelong interest in insect populations, and he has been following the insects that eat Vincetoxicum’s seeds for the past 40 years. As he described to me, surprisingly few population ecologists actually measure the amount of food available to insects. I should add that very few people have the resilience to study the same population of insects for 40 years, either. And interestingly, though this paper discusses the effect of a changing climate on seed production and seed predation, it was not Solbreck’s intent to consider climate change as a variable when he began, as climate change was not a concern of most scientists in the 1970s.

But climate change has happened in southeastern Sweden (and elsewhere), and has affected ecosystems in many different ways. Ecologists can quantify climate change by describing its effect on the vegetation period, or growing season (days above 5°C), which has increased by about 20 days since the mid 1990s.

Solbreck2B

Length of growing season (vegetation period) in southern Sweden.

During the same time period the abundance of Vincetoxicum has increased sharply.

Solbreck2Ayes

Vincetoxicum abundance, measured as area of the research site covered, during the study.

You will note that “Vincetoxicum” has the word “toxic” in its midst; the seeds are toxic to most consumers, and are important food sources for only two insect species. Euphranta connexa females lay eggs in developing fruits of the host plant, with the emerging larva boring through the seeds and killing most of them. Lygaeus equestris is an all-purpose seed predator; both larvae and adults suck on flowers, on developing seeds within the fruits, and on dry seeds they find on the ground up to a year later.

solbreck1c.png

Euphranta connexa female lays eggs in an immature seed pod.

Solbreck1D

Lygaeus equestra larva feeds on a fallen seed.

Solbreck teamed up with biostatistician Jonas Knape to analyze his data. From the beginning of the study, Solbreck suspected that annual variation in weather – particularly rainfall – might influence Vincetoxicum seed production, and consequent population growth of the two insect species. They discovered something quite unexpected; the dynamics of seed production shifted dramatically in the second half of the study, alternating annually from very high to very low production over that period. This dynamic shift coincides with the extension of the growth season as a result of climate change.

Solbreck2Cyes

Seed pod abundance by year.

The researchers argue that there is a non-linear negative feedback relationship of the previous year’s seed production on the current year’s seed production. Negative feedback occurs when an increase in one factor or event causes a subsequent decrease in that same factor or event. In this case, an increase in seed production uses up plant resources, leading to a decrease in seed production the following year. But the effect is non-linear, and does not come into play unless Vincetoxicum produces a huge number of seeds, as shown by the graph below,

Solbreck3yes

Seed production in the current year in relation to seed production in the previous year. Note that both axes are logarithmic. The curve represents the expected seed pod density generated by the statistical model, with the shaded area representing the 95% credible intervals. Open circles are data for 1977-1996, while closed circles are data for 1997-2016.

The researchers also found that high rainfall in June and July increased seed production.

So how do these wild fluctuations in seed production affect insects and the plant itself? One important finding is that in high seed production years, the proportion of seeds attacked by insects plummets because the sheer number of seeds overwhelms the seed-eating abilities of the insect consumers. Ecologists describe this phenomenon as predator satiation.

Solbreck4yes

Seed predation rates in relation to seed pod density.  Note that both axes are logarithmic. The curve represents the expected predation rate generated by the statistical model, with the shaded area representing the 95% credible intervals. Points are E. connexa predation rates while triangles are combined predation by both insect species.

As a result of predator satiation, there were, on average, seven times as many healthy (unattacked) seed pods in 1997-2016 than there were in 1977-1996. Presumably, this increased number of healthy seeds translates to an increase in new plants becoming established in the area. An important takehome message is that the entire dynamics of an ecosystem can change as a result of changes to the environment, in this case, climate change. More long-term studies are needed to evaluate how common these shifting dynamics are likely to become in the novel environmental conditions we humans are creating.

note: the paper that describes this research is from the journal Ecology. The reference is Solbreck, Christer and Knape, Jonas (2017), Seed production and predation in a changing climate: new roles for resource and seed predator feedback?. Ecology, 98: 2301–2311. doi:10.1002/ecy.1941. 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.