Early genetic consequences of defaunation in a large-seeded vertebrate-dispersed palm (Syagrus romanzoffiana)

Abstract

Plant populations are seriously threatened by anthropogenic habitat disturbance. In particular, defaunation may disrupt plant-disperser mutualisms, thus reducing levels of seed-mediated gene flow and genetic variation in animal-dispersed plants. This may ultimately limit their adaptive potential and ability to cope with environmental change. Tropical forest remnants are typically deprived of medium to large vertebrates upon which many large-seeded plants rely for accomplishing effective seed dispersal. Our main goal was to examine the potential early genetic consequences of the loss of large vertebrates for large-seeded vertebrate-dispersed plants. We compared the genetic variation in early-stage individuals of the large-seeded palm Syagrus romanzoffiana between continuous protected forest and nearby partially defaunated fragments in the Atlantic Forest of South America. Using nine microsatellites, we found lower allelic richness and stronger fine-scale spatial genetic structure in the disturbed area. In addition, the percentage of dispersed recruits around conspecific adults was lower, although not significantly, in the disturbed area (median values: 0.0 vs 14.4%). On the other hand, no evidence of increased inbreeding or reduced pollen-mediated gene flow (selfing rate and diversity of pollen donors) was found in the disturbed area. Our findings are strongly suggestive of some early genetic consequences resulting from the limitation in contemporary gene flow via seeds, but not pollen, in defaunated areas. Plant-disperser mutualisms involving medium-large frugivores, which are seriously threatened in tropical systems, should therefore be protected to warrant the maintenance of seed-mediated gene flow and genetic diversity in large-seeded plants.

Seed dispersal effectiveness by a large‐bodied invasive species in defaunated landscapes

“…Considering that the mean isolation of Atlantic forest remnants is 1,441 m (Ribeiro et al., ), the estimated dispersal distances found here suggest that wild pigs may be able to promote seed dispersal among isolated forest fragments. Long‐distance seed dispersal has consequences at landscape and regional scales, since it mediates gene flow among forests remnants (Giombini et al., ), favors the colonization of unoccupied habitats such as restoration sites or abandoned agricultural areas (Fragoso et al., ), reinforces the persistence of species in fragmented landscapes (McConkey & O'Farrill, ) and is especially important in assisting the range shift of plant species distribution following climate change (Mokany, Prasad, & Westcott, ). Although similar on this regard to lowland tapirs, one key difference among wild pigs and this native large‐bodied ungulate concerns their trophic position.…”

“…Abbreviations: NS, no significant statistical differences among treatments; NT, Not tested, given lack of germination on control seeds. *p = .029; **p < .001. since it mediates gene flow among forests remnants (Giombini et al, 2017), favors the colonization of unoccupied habitats such as restoration sites or abandoned agricultural areas , reinforces the persistence of species in fragmented landscapes (McConkey & O'Farrill, 2016) and is especially important in assisting the range shift of plant species distribution following climate change (Mokany, Prasad, & Westcott, 2014). Although similar on this regard to lowland tapirs, one key difference among wild pigs and this native large-bodied ungulate concerns their trophic position.…”

“…The loss of such seed dispersers can ultimately affect important ecosystem services, such as vegetation regeneration (Levi & Peres, ) and carbon sequestration (Bello et al., ; Peres, Emilio, Schietti, Desmoulière, & Levi, ), even before frugivore populations go extinct (McConkey & O'Farrill, ). Moreover, dispersal limitation hinders seed‐mediated gene flow (Giombini, Bravo, Sica, & Tosto, ), affecting the evolutionary dynamics of the dispersed plants (Galetti et al., ).…”

Persisting in defaunated landscapes: Reduced plant population connectivity after seed dispersal collapse

“…Defaunation‐mediated downsizing of frugivorous vertebrates may trigger cascading effects with a myriad of consequences for demography (Cordeiro & Howe, ; Pérez‐Méndez et al., ; Traveset & Riera, ; Traveset et al., ) and genetics of plant populations (Calviño‐Cancela et al., ; Giombini et al, ; Pacheco & Simonetti, ; Pérez‐Méndez et al., ; Voigt et al., ). Here, we demonstrate that when seed dispersal interactions are disrupted (La Gomera) or functionally impaired (Tenerife), the genetic consequences may spread well beyond the local population scale.…”

“…Recent studies have documented the fast-paced action of these changes and their consequences, ultimately leading to significant alterations of population-scale genetic diversity (i.e. the distribution of genetic variation within plant populations; Carvalho, Galetti, Colevatti, & Jordano, 2016;Giombini, Bravo, Sica, & Tosto, 2017;Pacheco & Simonetti, 2000;Pérez-Méndez, Jordano, García, & Valido, 2016). Yet, the consequences at larger, regional scales (i.e.…”