Mucilage binding to ground protects seeds of many plants from harvester ants: A functional investigation

Abstract

1. The seeds of many plant species produce mucilage on their surfaces that when wetted and dried, firmly adheres seeds to surfaces and substrates. Previous studies have demonstrated that seed anchorage to the ground can reduce seed predation, although only a few species have thus far been tested.2. Here we investigated whether binding to the ground reduces seed removal by harvester ants Pogonomyrmex subdentatus, an important granivore, for 53 species with mucilaginous seeds. We also explored functional traits that associate with seed removal risk to understand the ecological and evolutionary context of this granivory resistance trait.3. Using a field cafeteria choice experiment, we compared harvester ant seed removal of wetted ground-bound seeds to dry unbound control seeds for these 53 species. We developed a simple assay to score dislodgement force. We examined whether this force, seed mass and seed mucilage production explained the interspecific variation in protection that we observed in field seed removal. We integrated these experiments with a broad scale test of correlates of seed attachment using a previously published dataset of attachment potential of mucilaginous seeds for 432 species, examining correlations of attachment potential with 13 plant traits and the climate characteristics of the species' range. 4. Binding to the ground reduced seed removal in 42 of 53 species tested. The benefit increased with seed dislodgement force, which itself increased with mucilage production, but not with seed mass. In the larger dataset, shorter plant life span, higher temperature, more solar radiation, higher humidity, fewer wet days per year and higher seed density correlated positively with the odds of seed attachment. We also found that attachment potential showed a concave down quadratic relationship with latitude, peaking at roughly 30°. No strong evidence that any of the other six predictors correlated with attachment potential was found.5. We demonstrate that protection from granivores is a widespread convergent function of seed mucilage and is associated with mucilage production. We highlight the need for increased mechanistic investigations into this common but poorly studied trait, particularly in relation to functional drivers of the broad patterns we found.

Anchorage by seed mucilage prevents seed dislodgement in high surface flow: a mechanistic investigation

“…Dislodgement force, especially that of dried mucilage was the most important predictor of dislodgement resistance (Dried mucilage dislodgement: partial R 2 = 0.26, CI 95 = [0.00012, 0.50], Wet mucilage dislodgement: partial R 2 = 0.076, CI 95 = [-0.094, 0.31]). It correlated strongly with mucilage mass, a result we also found with a different set of species and a slightly different dislodgement assay (Pan et al, 2021), suggesting that increased dislodgement force can be driven by simply increasing mucilage production. Mucilage mass may be quite variable among close relatives (Table S2).…”

“…Their mucilage composition and primary function of mucilage in nature is thus far unknown but deserves more investigation. We have found that it provides a defensive benefit against harvester ants to several Polemoniaceae species (LoPresti et al, 2019, Pan et al, 2021, though it was similarly not as protective compared to other families in those studies.…”

“…Some of the characteristics that we measured here also contribute to other beneficial effects of mucilage (e.g. mucilage mass correlates with germination under water stress conditions: Teixeira et al, 2020; dislodgement force of dry mucilage correlates with resistance to granivory: Pan et al, 2021). Additionally, it is reasonable, though as of yet untested, that these same traits contribute more to other functions: dislodgement force of wet mucilage probably drives epizoochorous dispersal (Ryding, 2001), a slower mucilage decay rate may increase survival of seeds through the gut of herbivores (Kreitschitz et al, 2021a), and faster imbibition rate could lead to better DNA repair during brief wetting periods (Huang et al, 2008).…”

“…As mucilage traits vary both within and across species, determining the functional roles of this variation can provide insight into the evolutionary pressures shaping these traits. When looking broadly, mucilage mass and dislodgement force measured across 53 plant species in LoPresti et al (2019) and Pan et al (2021) were strongly correlated among more-closely related species. However, when looking indepth at close relatives, there is often much variation (Figure 2D-E).…”

“…When wetted, mucilage absorbs water and swells, releasing a complex matrix of hydrated cellulosic, pectic, and hemicellulosic sugars (Western, 2012). This matrix may be sticky or slippery when wet, but after drying, generally anchors seeds to substrates tightly (Kreitschitz et al, 2021b, Pan et al, 2021; Figure 2C, F). Previous workers have observed its utility in anchorage to substrates (antitelochory) and noted its ubiquity among plants in highly erosive environments (Ellner & Schmida, 1981, Garcia-Fayos et al, 2013).…”