The turnover of plant–frugivore interactions along plant range expansion: consequences for natural colonization processes

Abstract

Plant–animal mutualisms such as seed dispersal are key interactions for sustaining plant range shifts. It remains elusive whether the organization of interactions with seed dispersers is reconfigured along the expansion landscape template and, if so, whether its effects accelerate or slow colonization. Here we analyse plant–frugivore interactions in a scenario of rapid population expansion of a Mediterranean juniper. We combined network analyses with field surveys, sampling interactions between individual plants and frugivores by DNA-barcoding and phototrapping over two seasons. We assess the role of intrinsic and extrinsic intraspecific variability in shaping interactions and we estimate the individual plant contributions to the seed rain. The whole interaction network was highly structured, with a distinct set of modules including individual plants and frugivore species arranged concordantly along the expansion gradient. The modular configuration was partially shaped by individual neighbourhood context (density and fecundity) and phenotypic traits (cone size). Interaction reconfiguration resulted in a higher and more uneven propagule contribution, with most effective dispersers having a prominent role at the colonization front stand, where a distinct subset of early arriving plants dominated the seed rain. Our study offers new insights into the key role of mutualistic interactions in colonization scenarios by promoting fast plant expansion processes.

Downscaling mutualistic networks from species to individuals reveals consistent interaction niches and roles within plant populations

“…Differential contribution by frugivores to plant consumption was widespread in all populations, supporting previous studies and providing more evidence on how just a few species, even within diversified assemblages, perform most of the mutualistic interactions (Fig. S5, Rother et al 2016, Guerra et al 2017, Isla et al 2023, Rehling et al 2023, Thiel et al 2023). These interaction patterns will result in asymmetric dependencies between plant individuals and frugivore species, where the main frugivore species show low specificity for specific plants, while most plant individuals rely just on the main frugivore’s service (Quintero et al 2023).…”

“…This pattern reinforces previous findings in food webs, which revealed the presence of a core group of species fulfilling similar ecological roles, alongside peripheral species exhibiting idiosyncratic profiles (Mora et al 2018). It is likely that within frugivory networks these key individuals present unique phenotypic traits, such as abundant fruit crops or advantageous locations that make them reliable to many frugivores (Snell et al 2019, Isla et al 2023).…”

“…It was Darwin’s idea that individual variation acts as the necessary raw material for natural selection (Bolnick et al 2011). Intraspecific trait variability, neighborhood attributes and spatio-temporal context drive animal preferences for certain plant individuals, which will govern the establishment of interactions between plant individuals and their mutualistic partner species (Sallabanks 1993, Snell et al 2019, Isla et al 2023). These differences among plant individuals in interactions will be ultimately translated into outcome variations, acting as raw material for coevolution (Thompson 1999).…”

“…Several studies have used node-level metrics to characterize individuals ’positioning in the network, informing us about their role and significance in their population (e.g. Gómez & Perfectti 2012, Rodríguez-Rodríguez et al 2017, Crestani et al 2019, Vissoto et al 2022, Isla et al 2023, Arroyo-Correa et al 2023, Guerra et al 2017). However, most of these studies have used a single or several metrics separately to understand the interaction profile of individuals and for single populations.…”

Lasting effects of avian‐frugivore interactions on seed dispersal and seedling establishment

“…For example, most of the (few) seeds arriving at open areas are brought by a single bird species, Turdus merula . Hence, this disperser must play an important role in colonising new spaces, and its eventual local disappearance could have important consequences on P. lentiscus' colonisation ability and plant community structuring (Campo‐Celada et al., 2022; González‐Varo et al., 2017; Isla et al., 2023). The overall spatial clumping of the seed rain was concordant with many previous studies (e.g.…”