Interspecific competition for frugivores: population-level seed dispersal in contrasting fruiting communities

Indirect interactions among plant species mediated by frugivorous animals can be central to population and community dynamics, since the successful seed dispersal of species may depend on facilitative or competitive interactions with heterospecific plants. Yet, empirical evidence on these interactions is very scarce and mostly available at small spatial scales, within populations. Because lipid-rich fruits are known to be preferred by migratory birds, here we test our prediction of competitive inferiority of a carbohydrate-rich fruited species (the hawthorn Crataegus monogyna) compared to lipid-rich co-fruiting species in a Mediterranean region where the bulk of seed dispersal relies on migratory birds. We assessed avian seed dispersal in both relative (fruit removal rate) and absolute terms (seed dispersal magnitude) in seven hawthorn populations distributed across an altitudinal gradient encompassing three contrasting fruiting contexts: hawthorn is scarce in the lowlands, common in the midlands, and the dominant fruit species in the highlands. We found evidence of seed dispersal reduction due to interspecific competition in the lowland populations, where lipid-rich fruits dominate. Besides, DNA barcoding analysis of bird-dispersed seeds revealed that only a small subset of the local frugivore assemblages consumed hawthorn fruits in the lowland communities. Instead, the consumers of hawthorn fruits resembled the local frugivore assemblages where hawthorn fruits were more dominant and frugivore choices more limited. Our study suggests mechanisms by which the rarity or dominance of plant species might be jointly influenced by environmental constraints (here, precipitation along the altitudinal gradient) and frugivore-mediated indirect interactions among plants hindering or facilitating seed dispersal.Logistical support was provided by the Molecular Ecology Laboratory, Estación Biológica de Doñana (LEM-EBD-CSIC), a facility certified to ISO9001:2015 and ISO14001:2015 quality and environmental management protocols. JPGV and this study were funded by a Severo Ochoa Award for Centres of Excellence in R + D + I (SEV-2012-0262). While writing this paper, JPGV and BR were funded by the ‘Rei Jaume I’ awarded to Prof. Anna Traveset (Institut Mediterrani d’Estudis Avançats, CSIC- UIB). JPGV was also funded by an Individual Fellowship from the Marie Sklodowska-Curie Actions (H2020-MSCA- IF-2014-656572: MobileLinks). We also acknowledge the Spanish ‘Juan de la Cierva Incorporación’ and ‘Ramón y Cajal’ Programmes that currently fund the research activity of BR (IJCI-2017-33475) and JPGV (RYC-2017-22095), respectively