The role of parasitoids in a nursery-pollinator system: A population dynamics model

Highlights

• Our model simulates a complex biological system with different ecological interactions.

• The nursery pollination system simulated predicts the role of the parasitoids.

• A predatory species in a mutualist-antagonist system acts as a regulatory mechanism.

• It is important to differentiate the role of both sexes of a nursery pollinator.

Abstract

A nursery pollinator system comprises a plant and an insect pollinator which uses the reproductive structures of the plant to guard its eggs and serve it as food for the larvae. This kind of systems usually includes a third party, one or more species of parasitoids, that inject their eggs inside the larvae of the pollinating-seed predator to feed on them from the inside out. Here we build a model based on differential equations that replicates this system, first by showing the dual role of the pollinating-seed predator, which behaves both as a mutualist and as antagonist for the plant. We show that the system is more stable with the presence of the parasitoids; the stationary solutions with them significantly favor the plant population size with minor effects for the population of the pollinating-seed predator. By modeling both sexes of the nursery pollinator separately, we also highlight the role that male adults can have to compensate the costs and benefits of the interaction with plants, and thus to contribute to the stability of such mutualisms.

Introduction

Probably the most paradigmatic mutualistic system is pollination (Toby Kiers et al., 2010, Holland et al., 2002), in which the flower visitors obtain trophic resources (nectar, pollen, oils, etc.) and the plant obtains reproductive benefits through pollen dispersal and seed production. A special case of pollination, called nursery pollination, is reported when one pollinator species uses the fertilized flowers as hatching nests for its eggs, and the developing seeds serve as a food resource for its larvae. Therefore, the pollinating-seed predator obtains plant food resources for both its adult and larval stages, depriving the plant of part of the reproductive benefits obtained in a legitimate pollination interaction (Bronstein, 2001). Although this kind of interaction sounds eccentric, nursery pollination had been described in several families of angiosperms, with classic examples like fig trees-fig wasps and yuccas-yucca moths (Dufaÿ and Anstett, 2003). In these systems, there must exist a subtle balance between the benefits (pollination) and costs (seed predation) to achieve a positive net outcome to the plant. Indeed, the balance may shift from positive to negative, and therefore from mutualism to antagonism, depending on the mechanisms evolved by the hosts to avoid over-exploitation and on the ecological context where the interaction takes place (Leung and Poulin, 2008).

One mechanism controlling over-exploitation by the plant consists of random abortion of fruits, or selective abortion of fruits containing eggs or larvae of the pollinating-seed predator. This feature has been argued, by mathematical modeling approaches, as an evolutionary strategy of interspecific population regulation (Holland and DeAngelis, 2001, Holland and DeAngelis, 2006, Westerbergh and Westerbergh, 2001). With respect to the ecological context, apart from regulation of population densities due to environmental fluctuations, a central topic is related to the presence of third partners. One central consideration is whether the seed predator is also the unique pollinator or not (hereafter, obligate and facultative nursery pollination systems, respectively). In facultative systems, the occurrence of co-pollinators can shift the sign of this interaction, because they contribute to seed production without the cost of seed predation (Thompson and Pellmyr, 1992). The nursery pollination system may be also affected by the existence of predators, pathogens and parasitoids that may regulate the population size of the pollinating-seed predator, avoiding excess seed loss and system instability. Several field studies suggest this kind of regulatory process in nursery pollination systems (Force and Thompson, 1984, Elzinga et al., 2003, Crabb and Pellmyr, 2006, Nunes et al., 2018), but it has not been tested by population dynamic models.

Complex biological systems such as the nursery pollination are paradigmatic frameworks because different actors can play a vital role in the equilibrium of the ecological system, and the importance of an apparently secondary species can be addressed using population dynamic modeling (Neuhauser and Fargione, 2004, Holland et al., 2002). In this study, we use a generalized version of the model of García-Algarra et al. (2014), which can describe multiple ecological interactions within the same equations. This approach has the advantage of treating species interactions based on fundamental ecological laws (Turchin, 2003) and independently of the model, i.e. without having to consider them as different phenomena, which is a conceptual burden. Such a generalization may allow researchers a better representation of ecological systems by including most observed interactions, weighting their importance where necessary and avoiding frameworks of specific systems and ad hoc modeling.

We hypothesize that, when the population density of two species can alternate the net effect of their interaction between mutualism and parasitism, the presence of a third species can regulate their population dynamics and stabilize the interaction towards mutualism. To test this prediction, we applied a generalized model of ecological relations to the system made up of Caryophyllaceous plants, the nursery pollinator Hadena moths and their parasitoid wasps. We expect that a subtle regulation of the moths population by its parasitoids may stabilize the dynamics of the system, allowing the high metabolic costs of other regulatory processes, like fruit abortion, to control over-exploitation.