Megafrugivores as fading shadows of the past: extant frugivores and the abiotic environment as the most important determinants of the distribution of palms in Madagascar

Abstract

The extinction of all Madagascar's megafrugivores ca 1000 years ago, may have left its signature on the current distribution of vertebrate-dispersed plants across the island, due to the loss of effective seed dispersal. In this study, we dissect the roles of extinct and extant frugivore distributions, abiotic variables, human impact and spatial predictors on the compositional turnover, or beta-diversity, of palm (Arecaceae) species and their dispersal-related traits across 40 assemblages in Madagascar. Variation partitioning showed that palm beta-diversity is mostly shaped by the distribution of extant frugivores (eight lemur, three bird, two rodent and one bat species) and the abiotic environment (e.g. forest cover, slope and temperature), and to a lesser extent by the distribution of extinct megafrugivores (several giant lemur and elephant bird species). However, the contribution of these variables differed between dry western assemblages and wet eastern assemblages, with a more prominent role, albeit still small, of extinct megafrugivores in the west. These results suggest that palm distributions in the dry west of Madagascar, where megafrugivores were probably most abundant in the past, still show signatures of past interactions. With a fourth-corner analysis we observed that the distribution of palm species with relatively large fruits and seeds was negatively associated with frugivore richness of both past and present communities and home range sizes of extant mammalian frugivores. This suggests that palm species with relatively large fruits tend to occur in places with fewer, small-ranged mammalian frugivores, which may indicate dysfunctional seed dispersal. Nevertheless, our results also indicate that several wide-ranging bird species with high dispersal ability (large hand-wing index) that also occasionally feed on fruits may compensate for this potential dispersal loss. Our study sheds new light on dispersal anachronisms in Madagascar, and how defaunation and past species interactions may underlie current plant distributions.

Genomic signatures of past megafrugivore-mediated dispersal in Malagasy palms

“…Climatic variables were retrieved from https://www.worldclim.org/ (1 km resolution), rivers from http://landscapeportal.org/, percentage of forest cover for 2010 from https://madaclim.cirad.fr/ and human-related variables (e.g., road density and human population density from 2010) from Venter et al (2016) (1 km resolution). To assess co-occurrence between palm populations and frugivores, we focused on the 93 Malagasy frugivore species identified in Méndez et al (2022), and used the current polygon ranges from the International Union for Conservation of Nature, ver. 2020-2 (IUCN 2020).…”

“…2020-2 (IUCN 2020). Similarly, for the extinct megafrugivores, we used the reconstructed historical distribution maps from Méndez et al (2022), including 14 species of megafrugivores, which were modelled using co-occurrence of extant and extinct taxa across fossil sites. For extinct giant tortoises, we used the historical ranges in Pedrono et al (2013).…”

“…Fossil pollen suggests that the extinction of endemic megafauna coincided with a gradual decline in abundance of trees relying on megafrugivores for seed dispersal (Domic et al, 2021). Moreover, Malagasy palm distributions still retain signals of past dispersal by extinct megafrugivore animals, mostly in the western part of the island (Méndez et al, 2022). However, the extent to which dispersal services provided by Madagascar's past megafrugivores can still be detected in the genomes of extant plant populations remains unclear.…”

The megaherbivore gap after the non-avian dinosaur extinctions modified trait evolution and diversification of tropical palms

“…This resulted in 90 observations for which we assembled the taxonomy of the fossil and its nearest living relatives (tribe, genus and species), fossil site location, fossil age, and length and/or width of the fossil fruit or seed. Although seed size differs from fruit size, they are strongly correlated in palms [ 33 ] as most fruits bear a single or a few seeds. Seed size thus provides a minimum size estimate of fruit size for a particular taxon and time period.…”

“…Palms comprise approximately 2500 extant species and show a spectacular diversity of fruit sizes (from 0.3 to 45 cm in length, most of them dispersed by animals including megafauna) and armature (e.g. spiny leaves and/or stems) [30][31][32][33]. Furthermore, palms co-occurred with dinosaurs in the Cretaceous and may have been important dinosaur food [34], and there are instances of seed-like structures of palms in dinosaurian coprolites from the Cretaceous Lameta Formation in India [15,16].…”