Functional Extinction of Birds Drives Rapid Evolutionary Changes in Seed Size

Abstract

Local extinctions have cascading effects on ecosystem functions, yet little is known about the potential for the rapid evolutionary change of species in human-modified scenarios. We show that the functional extinction of large-gape seed dispersers in the Brazilian Atlantic forest is associated with the consistent reduction of the seed size of a keystone palm species. Among 22 palm populations, areas deprived of large avian frugivores for several decades present smaller seeds than nondefaunated forests, with negative consequences for palm regeneration. Coalescence and phenotypic selection models indicate that seed size reduction most likely occurred within the past 100 years, associated with human-driven fragmentation. The fast-paced defaunation of large vertebrates is most likely causing unprecedented changes in the evolutionary trajectories and community composition of tropical forests.

Phenotypic plasticity and local adaptation favor range expansion of a Neotropical palm

“…Fernandez; Wendt et al., 2011), but molecular analysis with isoenzymes did not find relevant differentiation (Martins et al., 2007), and E. espiritosantensis is no longer considered a valid species. Populations with smaller seeds are found in defaunated forests, as a consequence of a rapid evolutionary change driven by the ecological extinction of large‐gaped birds (Carvalho, Ribeiro, Cortes, Galetti, & Collevatti, 2015; Galetti et al., 2013). Molecular analyses have corroborated the explanations of population divergences according to the site of origin (Gaiotto, Grattapaglia, & Vencovsky, 2003) and to forest fragmentation levels (Carvalho et al., 2015), but neither the investigation of adaptive molecular divergence with SNPs, nor reciprocal transplant experiments, had been performed for E. edulis so far.…”

Seed size-number trade-off in Euterpe edulis in plant communities of the Atlantic Forest

“…The investigation of seed size-number trade-off in populations of the endangered palm Euterpe edulis is worth considering because the variations of its seed size may affect its potential to adapt to defaunation and to persist in native ecosystems under climate change scenarios projected for the Atlantic Forest (Lopes, 2013;Galetti et al, 2013).Therefore, we sought to investigate seed size-number trade-off in Euterpe edulis populations growing in different plant communities of the Brazilian Atlantic Forest.…”

“…For instance, Galetti et al (2013) showed that the functional extinction of large-bodied frugivorous birds in the Atlantic Forest resulted in the reduction of seed size, due to the selection being mediated by smallgaped birds, of the Euterpe edulis palm in defaunated remnants. Additionally, seed size can influence the vulnerability of recalcitrant-seeded species to climate change, because smaller seeds may be more exposed to desiccation during the abnormal drought periods recently observed in tropical and temperate forests (Galetti et al, 2013;Joët et al, 2013). Thus, the ability of plant species to regulate seed size in different plant communities and under divergent environmental conditions may determine their capacity to overcome new ecological filters imposed by human-mediated disturbances and, consequently, to persist in native ecosystems.…”

Reproductive phenology, seed removal and early regeneration in relation to distance from parental plants of a native palm in small Atlantic forest fragments

“…Plants with large seeds (>15 mm) are more susceptible to the loss of dispersers because their regeneration is strongly seed-limited (Moles & Reproductive phenology, seed removal and early regeneration in relation to distance from parental plants of a native palm in small Atlantic forest fragments Westoby 2002) and these plants rely heavily on large-bodied animals as seed dispersers (Silva & Tabarelli 2000;Wright & Duber 2001;Cordeiro & Howe 2003;Galetti et al 2006;2013;Terborgh et al 2008). For instance, defaunation of large-gaped frugivorous birds has been pointed out as the main source of rapid evolutionary change in seed size of the palm Euterpe edulis in remnants of the Brazilian Atlantic forest (Galetti et al 2013). Therefore, large-seeded plants should be more susceptible to reductions in seed dispersal in fragmented and defaunated sites than small-seeded plants.…”