Pollination and seed dispersal mutualisms support a large amount of biodiversity and productivity in terrestrial ecosystems (Janzen 1985). However, both the plants and animals that participate in these mutualisms are facing global declines due to anthropogenic perturbations such as climate change, habitat destruction, and invasive species (Traveset & Richardson 2006, 2014, Tylianakis et al. 2008, Potts et al. 2010, 2016, Wotton & Kelly 2011, Aslan et al. 2013, Neuschultz et al. 2016). Though mutualism research has historically focused on understanding stable coexistence at high density, characterizing the dynamics of mutualisms at low density is a current conservation priority (Latty & Dakos 2019). Recent work has tended to model pollination and seed dispersal mutualisms as one phenomenon, that of food resources provided by plants exchanged for reproductive services provided by animal consumers (Holland & DeAngelis 2010, Revilla 2015). However, animal-pollination and seed dispersal affect different stages of plant reproduction, and thus are likely to have different dynamics when plants or animals are at low density (Bronstein 2015, Beckman et al. 2020).
Here, we develop and analyze simple two-species models of pollination and seed dispersal mutualisms. By incorporating more detail in plant reproductive biology than previous consumer-resource approaches, we identify important differences in the dynamics of these mutualisms at low density and the likely ecological scenarios under which these dynamics would occur. For example, both pollination and seed dispersal mutualisms exhibit a threshold under which partners whose populations are dependent upon the mutualism for growth collapse even if initially highly abundant. However, animal-pollinated plants are uniquely subject to a form of Allee threshold under which they can become too rare to attract sufficient pollinator visits to achieve outcrossing, causing population collapse.
Critically for management, the “threshold effects” in both types of mutualism occur because one species is too low in density to provide sufficient benefits to its partner, causing that partner’s population to decline. The low-density species continues to benefit from the mutualism, but its increase in density cannot occur fast enough to save the system from collapse. When the benefits are food rewards (i.e., animals consuming nectar, pollen, seeds, fruit, etc), the threshold is not in population density per se, but rather in the density of rewards provided. The timeline of collapse varies based on the system, but understanding the dynamics of collapse can suggest management strategies that may otherwise be counterintuitive, such as supplementing benefits (e.g., food) to a high density (but declining) population when its partner is at low density.
This work advances the study of mutualism by characterizing the differences between pollination and seed dispersal mutualisms both biologically and mathematically. Additionally, we shift the focus of theoretical contributions in mutualism from stable coexistence (which has been long established, if not well-known in broader community ecology) to the unique and troubling dynamics at low density which are extremely relevant to modern ecosystems.
Citation: Hale, K. R. S., Maes, D.P., & Valdovinos, F. S. (2022). Simple mechanisms of plant reproductive benefits yield different dynamics in pollination and seed dispersal mutualisms. American Naturalist 200(2):202–216. https://doi.org/10.1101/2021.05.05.442848
Abstract: Pollination and seed dispersal mutualisms are critical for biodiversity and ecosystem services yet face mounting threats from anthropogenic perturbations that cause their populations to decline. Characterizing the dynamics of these mutualisms when populations are at low density is important to anticipate consequences of these perturbations. We developed simple population dynamic models detailed enough to distinguish different mechanisms by which plant populations benefit from animal pollination or seed dispersal. We modeled benefits as functions of foraging rate by animals on plant rewards and specified whether they affected plant seed set, germination, or negative density dependence during recruitment. We found that pollination and seed dispersal mutualisms are stable at high density but exhibit different dynamics at low density, depending on plant carrying capacity, animal foraging efficiency, and whether populations are obligate on their partners for persistence. Under certain conditions, all mutualisms experience destabilizing thresholds in which one population declines because its partner is too rare. Plants additionally experience Allee effects when obligate on pollinators. Finally, pollination mutualisms can exhibit bistable coexistence at low or high density when plants are facultative on pollinators. Insights from our models can inform conservation efforts, as mutualist populations continue to decline globally.
Note the correction: In the caption of Figure 1, the parameter f should be 0.5 in all cases. This value is correct in the included Mathematica code.
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