Fungal infestation boosts fruit aroma and fruit removal by mammals and birds

Abstract

For four decades, an influential hypothesis has posited that competition for food resources between microbes and vertebrates selects for microbes to alter these resources in ways that make them unpalatable to vertebrates. We chose an understudied cross kingdom interaction to experimentally evaluate the effect of fruit infection by fungi on both vertebrate (mammals and birds) fruit preferences and on ecologically relevant fruit traits (volatile compounds, toughness, etc). Our well-replicated field experiments revealed that, in contrast to previous studies, frugivorous mammals and birds consistently preferred infested over intact fruits. This was concordant with the higher level of attractive volatiles (esters, ethanol) in infested fruits. This investigation suggests that vertebrate frugivores, fleshy-fruited plants, and microbes form a tripartite interaction in which each part could interact positively with the other two (e.g. both orange seeds and fungal spores are likely dispersed by mammals). Such a mutualistic view of these complex interactions is opposed to the generalized idea of competition between frugivorous vertebrates and microorganisms. Thus, this research provides a new perspective on the widely accepted plant evolutionary dilemma to make fruits attractive to mutualistic frugivores while unattractive to presumed antagonistic microbes that constrain seed dispersal.

Strong among population variation in frugivory strength by functional diverse frugivores: a ‘reciprocal translocation’ experiment

“…Other possibility to be considered in future studies is variation among focal P. bourgaeana populations being based on fruit traits other than size or reward (e.g. volatile compounds, chemical defenses; Lomáscolo et al 2010, Schaefer and Ruxton 2011, Whitehead et al 2016, Peris et al 2017.…”

“…For instance, seed dispersers (foxes and badgers) were most active in Reserva (Fig. 3b), which may be responsible of the observed tree colonization of vacant habitats in this area (Fedriani et al 2017; Authors unpublished data). Such population expansion is taking place even though seed predators (red and fallow deer) are also abundant in Reserva, where every season they depredate large fractions of P.…”

“…To facilitate the precise identification of frugivore visitors based on their footprints in the local sandy substrate, we cleaned carefully the offering point at the start of the experiment and then after each observation (e.g. Mendoza and Dirzo 2007, Peris et al 2017. All offering points were checked early in the morning during five consecutive days and removed fruits were not replaced.…”

“…Functionally diverse vertebrate frugivores often vary among populations in density and activity (e.g. Brodie et al 2009, Peris et al 2017. Furthermore, different frugivore guilds are likely to exert different effects (e.g.…”

Reunion overseas: introduced wild boars and cultivated orange trees interact in the Brazilian Atlantic Forest

“…eat, but do not disperse, seeds of certain Citrus species. In our study, we also very frequently recorded several bird species underneath orange trees; however, they were always picking pulp remains from fruits previously processed by boars or from fungusinfected fruits (which soften the fruit peel allowing birds to access the pulp; Peris, Rodríguez, Peña, & Fedriani, 2017) and no evidence of seed ingestion (and thus potential dispersal) was found during this study. Thus, the potential role of other mammals on citrus seed dispersal deserves further research.…”