Research Article |
Corresponding author: Jaime Moyano ( mjaime@agro.uba.ar ) Academic editor: David Richardson
© 2019 Jaime Moyano, Mariana C. Chiuffo, Nahuel Policelli, Martin A. Nuñez, Mariano A. Rodriguez-Cabal.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Moyano J, Chiuffo MC, Policelli N, Nuñez MA, Rodriguez-Cabal MA (2019) The interplay between propagule pressure, seed predation and ectomycorrhizal fungi in plant invasion. NeoBiota 42: 45-58. https://doi.org/10.3897/neobiota.42.30978
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There are many hypotheses aiming to explain invasion success, but evaluating individual hypotheses in isolation may hinder our ability to understand why some species invade and others fail. Here we evaluate the interaction between propagule pressure, seed predation and missed mutualism in the invasion success of the pine, Pinus ponderosa. We evaluated the independent and interactive effects of propagule pressure and seed predation at increasing distances from a pine plantation. Additionally, because pines are obligate mutualists with ectomycorrhizal fungi (EMF) and pine invasions fail in the absence of their EMF symbionts, we evaluated EMF availability through a growth chamber bioassay. In this bioassay we measured root colonization by EMF with soil samples collected from the different distances from the plantation. We found that propagule pressure overwhelms seed predation only at the edge of the pine plantation, while seed predation overcomes propagule pressure at 25 m and further distances from the plantation. We also found that EMF root colonization decreases with distance from the plantation. However, pine roots were colonized up to 200 m from the plantation, suggesting that EMF may not be hindering invasion, at least not on the scale of this experiment. Taken together our results demonstrate that seed predation may be limiting the invasion of P. ponderosa in the study region as propagule pressure only overcomes seed predation at the plantation edge. Here we provide evidence of how strong biotic resistance can suppress an invasion, regardless of the variation in propagule pressure and the availability of mutualists.
Biotic resistance, granivory, invasion mechanism, mutualism, Pinus , seed dispersal
For decades, ecologists have tried to explain why some populations of introduced species become invasive while others fail to invade (
Together with strong biotic resistance and low propagule pressure, the absence of mutualistic biotic interactions (missed mutualism) is one of the most important limitations for the invasion of non-native plants (
Pines are an ideal system to study the role of propagule pressure, seed predation and missed mutualism on invasion success. The role of propagule pressure can be easily studied because non-native pines produce a large number of seeds which are wind dispersed over large areas but with the highest proportion falling near the seed source, creating a gradient of propagule pressure (
The aim of this study was to test the importance of three mechanisms (propagule pressure, seed predation and missed mutualism) in the invasion of Pinus ponderosa in north Argentinean Patagonia. Here, we evaluated seed predation with different seed availability to resemble the natural seed rain pattern at different distances from a plantation of P. ponderosa. Additionally, to test if the absence of highly co-evolved soil mutualists could account for pine invasion failure we performed a growth chamber bioassay with soil inoculum from increasing distances from the pine plantation. Specifically, we asked the following question: what is more important determining P. ponderosa invasion success, propagule pressure, seed predation, the availability of EMF symbionts or the interplay between these mechanisms? Evaluating the relative importance of different invasion mechanisms is key to identify the causes of plant invasions. Also, assessing the interaction between different mechanisms helps to understand how different processes interplay to determine invasion success or failure (
We conducted this experiment on a steppe ecosystem in North Patagonia (40°59'53"S, 71°05'13"W) because this type of ecosystem is among the most frequently invaded by non-native pines (
To evaluate the effects of propagule pressure and seed predation on seed survival, we conducted a seed predation experiment. We placed 18 transects every 50 meters perpendicular to a P. ponderosa plantation. In each transect, we installed plots at 0, 25, 50, 75, 100, 150 and 200 m from the plantation. To disentangle the effects of distance from plantation and seed availability, we used two different experimental designs with different seed densities (variable and fixed). In the "Variable density" experiment we simulated natural seed dispersion on nine transects. The purpose of the "Variable density" experiment is to evaluate the proportion of seed rain that is consumed by seed predators at different distances from the pine plantation. Since data on seed production and dispersion is not available in our study site, we obtained data from the literature (
To test if lack of ectomycorrhizal fungi is limiting P. ponderosa invasion, we conducted a growth chamber bioassay. We collected ~100 cm3 of soil from each of the seven distances (0, 25, 50, 75, 100, 150, and 200 m) from the plantation on each of the nine "Variable density" transects used for the field experiment. Soils were collected during late fall 2017, just after the peak of mushroom fruiting season. Soil samples were dug from each site using an ethanol-sterilized spoon, placed in coin envelopes, each of which was then placed into gallon bags and then stored at 4 °C to be used the next day after collection. We removed small rocks and coarse roots and we used these soils to inoculate a mix of sterilized 50:50 soil and sand that had been autoclaved twice (
To evaluate the effect of different predictive variables on seed predation we used logistic regressions. We calculated seed predation, the response variable, as the proportion of seeds that had been consumed (
To evaluate the effect of mycorrhizal inocula at increasing distances from plantation, we analyzed each response variable (survival, shoot height, biomass, and root colonization) separately. For response variables with binomial distribution (survival, and root colonization) we used GLMM fit by maximum likelihood and a logit link function (lme4 package, glmer function) (
We found that seed predation increased with distance from plantation (p = 0.0080, Fig.
Parameters of the logistic regression for seed predation of P. ponderosa at increasing distance from the pine plantation.
Fixed effects of distance from plantation, transect type and the interaction between distance and transect type. Significant effects (p < 0.05) are shown in bold letters | ||||
---|---|---|---|---|
Fixed effects | Estimate | Standard error | z | p |
Distance | 0.036 | 0.0134 | 2.656 | 0.0080 |
Transect type | -0.849 | 0.7791 | 1.090 | 0.2756 |
Distance * Transect type | -0.015 | 0.0203 | 0.731 | 0.4648 |
Random effects of the transect (n = 9). Intercepts are averaged | ||||
Random effect | Mean intercept | Standard deviation | ||
Transect | 1.475 | 0.000 |
Pairwise comparisons of seed predation levels between different distances from the pine plantation. Significant differences (p < 0.05) are shown in bold letters.
Pairwise comparison [m] | p value |
---|---|
0 vs 25 | 0.0396 |
0 vs 50 | 0.0397 |
0 vs 75 | 0.0312 |
0 vs 100 | 0.0291 |
0 vs 150 | 0.0441 |
0 vs 200 | 0.0438 |
25 vs 50 | 0.4273 |
25 vs 75 | 0.5187 |
25 vs 100 | 0.6585 |
25 vs 150 | 0.9311 |
25 vs 200 | 0.4090 |
50 vs 75 | 0.8348 |
50 vs 100 | 0.6705 |
50 vs 150 | 0.3914 |
50 vs 200 | 0.9541 |
75 vs 100 | 0.8175 |
75 vs 150 | 0.4724 |
75 vs 200 | 0.7925 |
100 vs 150 | 0.6011 |
100 vs 200 | 0.6359 |
150 vs 200 | 0.3758 |
Pairwise comparisons between propagule pressure and seed predation for each distance level from the pine plantation. Significant differences (p < 0.05) are shown in bold letters.
Pairwise comparison | Distance [m] | p value |
Propagule pressure vs seed predation | 0 | 0.0438 |
25 | 0.4090 | |
50 | 0.9541 | |
75 | 0.7925 | |
100 | 0.6359 | |
150 | 0.3758 | |
200 | 1.0000 |
EMF root colonization decreased with distance from plantation (p = 0.0139, Fig.
EMF root tips colonization on growth chamber bioassay (in black) and seed survival from predation for P. ponderosa on field experiment (in grey) at increasing distance from plantation. Dots show mean (+ SE) values for each distance.
Parameters of the logistic regression for EMF root colonization at increasing distance from the pine plantation.
Fixed effects of distance from plantation. Significant effects (p < 0.05) are shown in bold letters | ||||
Fixed effects | Estimate | Standard error | z | p |
Distance | -0.012 | 0.0050 | -2.460 | 0.0139 |
Random effects of the transect (n = 9), and the observation included due to overdispersion. Intercepts are averaged | ||||
Random effect | Mean intercept | Standard deviation | ||
Transect | 2.064 | 0.396 | ||
Observation | 2.027 | 1.554 |
Our results provide strong empirical evidence that seed predation may be the most important biotic mechanism limiting P. ponderosa invasions in this system. Seed predators consumed ca. 95% of the seeds dispersed outside the pine plantation, thereby limiting seed availability. Propagule pressure varied in a wide range, from 100 seeds/m² at the plantation edge to 2 seeds/m² at a distance of 200 m from the plantation, however, only at the plantation edge does propagule pressure overwhelm seed predation. At distances of 25 m and further from the pine plantation, seed predation overcame the influence of propagule pressure. This is particularly clear when we consider seed predation in the fixed density transects: at distances from plantation higher than 75 m seed predation was between 25% and 900% higher than propagule pressure. This survival pattern of not predated seeds suggests that P. ponderosa seedling annual recruitment is limited to the first 25 m from the seed source. Altogether, these results provide evidence of how biotic resistance from generalist natural enemies can hinder an invasion.
In this study, we found that pine seed predation probability increases with increasing distance from plantation (Fig.
Our results also show that the abundance of EMF may not be limiting pine seedling survival and growth at the distance range evaluated. We found a gradient of decreasing root colonization with increasing distance from plantation (Fig.
Our study shows that biotic resistance can be extremely important in plant invasions, even more important than the propagule pressure and the missed mutualism hypothesis. By contrast, a review of the empirical evidence for general hypothesis in invasion ecology found more support for the propagule pressure hypothesis than for the biotic resistance hypothesis in experiments with terrestrial plants (
This research was supported by Rufford Foundation grant number 23089-1 and the National Agency of Scientific and Technologic Promotion (AGENCIA) grant "PICT 2014 N° 0662 PRESTAMO BID". We thank San Ramon ranch for giving us permission to carry out our study on their property. We also thank Ariel Mayoral and Agustin Vitali for their valuable help on the field. We appreciate the help with the statistical analyses provided by Teresa Moran-Lopez and Florencia Tiribelli. We greatly appreciate the helpful comments from Dean Pearson on an earlier version of this manuscript.
Figure S1.
Data type: multimedia