Frugivory and seed dispersal in a hyperdiverse plant clade and its role as a keystone resource for the Neotropical fauna

Abstract

Background and aims: Much of our understanding of the ecology and evolution of seed dispersal in the Neotropics is founded on studies involving the animal-dispersed, hyperdiverse plant clade Miconia (Melastomataceae). Nonetheless, no formal attempt has been made to establish its relevance as a model system or indeed provide evidence of the role of frugivores as Miconia seed dispersers.

Methods: We built three Miconia databases (fruit phenology/diaspore traits, fruit-frugivore interactions and effects on seed germination after gut passage) to determine how Miconia fruiting phenology and fruit traits for >350 species interact with and shape patterns of frugivore selection. In addition, we conducted a meta-analysis evaluating the effects of animal gut passage/seed handling on Miconia germination.

Key results: Miconia produce numerous small berries that enclose numerous tiny seeds within water- and sugar-rich pulps. In addition, coexisting species provide sequential, year long availability of fruits within communities, with many species producing fruits in periods of resource scarcity. From 2396 pairwise interactions, we identified 646 animal frugivore species in five classes, 22 orders and 60 families, including birds, mammals, reptiles, fish and ants that consume Miconia fruits. Endozoochory is the main dispersal mechanism, but gut passage effects on germination were specific to animal clades; birds, monkeys and ants reduced seed germination percentages, while opossums increased it.

Conclusions: The sequential fruiting phenologies and wide taxonomic and functional diversity of animal vectors associated with Miconia fruits underscore the likely keystone role that this plant clade plays in the Neotropics. By producing fruits morphologically and chemically accessible to a variety of animals, Miconia species ensure short- and long-distance seed dispersal and constitute reliable resources that sustain entire frugivore assemblages.

Keywords: Miconia; Fruiting phenology; Melastomataceae; germination; mutualism; seed ecology.

Fig. 1.

Diversity in shapes, sizes and colours of Miconia fruits. (A) M. capilliflora; (B) M. subciliata; (C) M. blepharodes; (D) M. macrosperma; (E) M. loligomorpha; (F) Miconia sp.; (G) M. calvescens; (H) M. albicans; (I) M. leacordifolia; (J) M. affinis; (K) M. gratissima; (L) M. dolichostachya; (M) M. sellowiana; (N) M. ampla; (O) Miconia sp.; (P) M. candelabriforme; (Q) M. heliotropoides; (R) M. impetiolaris; (S) M. rimalis; (T) M. minutiflora; (U) M. dasytricha; (V) M. oxymeris; (W) M. neourceolata; (X) Miconia sp. (All pictures were kindly provided by Renato Goldenberg.)

Fig. 2.

Percentage of Miconia species with corresponding ripe fruit colour (n = 185 species) (A) and partitioned consumption by different animal groups according to Miconia ripe fruit colours; animal icons corresponds to the animal clades Aves (n = 90 Miconia species), Mammalia (n = 34), Reptilia (n = 3) and Insecta (Formicidae; n = 17) (B).

Fig. 3.

Species rarefaction curves describing the number of animal species of different clades increasing in function of Miconia species with reports of fruit consumption. Lines represent means and shaded areas the 95 % confidence interval. Blue = Aves; green = Formicidae; pink = Actinopterygii; red = Mammalia; yellow = Reptilia.

Fig. 4.

Top 15 Miconia species consumed by Neotropical frugivores (A) and top 15 animal species consuming Miconia fruits (B).

Fig. 5.

Percentage of seed germination in Miconia species across different experimental treatments. Control I, seeds within fruits; control II, manually extracted seeds; Aves; Primates; Didelphimorphia; Rodentia; Formicidae. Dots are the independent germination percentage of each plant species reported in each study according to the experimental group. Dashed lines represent means, and whiskers the standard error. n is the number of observations for each experimental group.

Fig. 6.

Effect sizes of vertebrate gut passage and fruit handling by ants on germination performance. Overall effects are for germination percentage (circle) and mean germination time (square). Animal groups mediating germination are Formicidae, Rodentia, Didelphimorphia, Primates and Aves (from top to bottom). The cumulative effect size is reported with its 95 % confidence interval. Numbers in parentheses indicate the number of outcomes for each effect. Effects are significant if the confidence intervals do not overlap zero.