Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate

Abstract

Background: Some neotropical, fleshy-fruited plants have fruits structurally similar to paleotropical fruits dispersed by megafauna (mammals > 10(3) kg), yet these dispersers were extinct in South America 10-15 Kyr BP. Anachronic dispersal systems are best explained by interactions with extinct animals and show impaired dispersal resulting in altered seed dispersal dynamics.

Methodology/principal findings: We introduce an operational definition of megafaunal fruits and perform a comparative analysis of 103 Neotropical fruit species fitting this dispersal mode. We define two megafaunal fruit types based on previous analyses of elephant fruits: fruits 4-10 cm in diameter with up to five large seeds, and fruits > 10 cm diameter with numerous small seeds. Megafaunal fruits are well represented in unrelated families such as Sapotaceae, Fabaceae, Solanaceae, Apocynaceae, Malvaceae, Caryocaraceae, and Arecaceae and combine an overbuilt design (large fruit mass and size) with either a single or few (< 3 seeds) extremely large seeds or many small seeds (usually > 100 seeds). Within-family and within-genus contrasts between megafaunal and non-megafaunal groups of species indicate a marked difference in fruit diameter and fruit mass but less so for individual seed mass, with a significant trend for megafaunal fruits to have larger seeds and seediness.

Conclusions/significance: Megafaunal fruits allow plants to circumvent the trade-off between seed size and dispersal by relying on frugivores able to disperse enormous seed loads over long-distances. Present-day seed dispersal by scatter-hoarding rodents, introduced livestock, runoff, flooding, gravity, and human-mediated dispersal allowed survival of megafauna-dependent fruit species after extinction of the major seed dispersers. Megafauna extinction had several potential consequences, such as a scale shift reducing the seed dispersal distances, increasingly clumped spatial patterns, reduced geographic ranges and limited genetic variation and increased among-population structuring. These effects could be extended to other plant species dispersed by large vertebrates in present-day, defaunated communities.

Figure 1. Examples of megafauna fruits and seeds.

a, Lacunaria jemmani, Quiinaceae. b, Parinari montana, Chrysobalanaceae (seeds); c, Caryocar villosum, Caryocaraceae, fruit split open with two seeds; d, Theobroma grandiflora, Malvaceae; e, Attalea martiana, Arecaceae; f, Phytelephas macrocarpa, Arecaceae (seeds). Black line is 2 cm length. Photos from specimens at Herbarium João Murça Pires (MG) of the Museu Paraense Emílio Goeldi, Belém, Brazil; by PJ.

Figure 2. Fleshy fruited megafaunal-dependent species illustrating size, shape, and color variation.

a, Attalea speciosa, Arecaceae; b, Mouriri elliptica, Melastomataceae; c, Hymenaea stigonocarpa, Fabaceae; d, Genipa americana, Rubiaceae; e, Salacia elliptica, Celastraceae; f, Annona dioica, Annonaceae. Black reference line is 2 cm length. Photos from Fazenda Rio Negro, Pantanal, Brazil; by PJ, MG, and Camila I. Donatti.

Figure 3. Frequency of megafauna species with different fruit colors (blank bars) compared to the summed frequency in different communities (filled bars).

The available data for Manu (Peru), Monteverde (Costa Rica), Florida, Europe New Zealand , and Brazilian Myrtaceae have been pooled to characterize the color distribution pattern in extant communities.

Figure 4. Bivariate plots of fleshy fruit traits for megafauna and non-megafauna species.

Dots, megafauna-fruit species; +, non-megafauna fruited species. (A) dry mass of seeds per fruit and fruit mass. Intrafamilial comparisons are indicated by connecting lines between dots and +s; (B) individual seed mass and number of seeds per fruits.

Figure 5. Principal components analysis of ecological and life-history variables of megafauna fruit species.

Only genera (N = 11) with several species available for the analyses have been included. Cubes indicate the relative positions of individual species on the space defined by the three first principal components. Axes are labeled with short descriptions of the variables having larger loads (>0.40) on them.

Figure 6. Within-family contrasts for fruit traits of megafauna and non-megafauna plant species.

The pattern for fruit length was very similar to fruit diameter and has been omitted for clarity. Each line corresponds to the contrast (difference in mean trait value) between species of the same family with each syndrome.