Multiple External Seed Dispersers Challenge the Megafaunal Syndrome Anachronism and the Surrogate Ecological Function of Livestock

Abstract

The dispersal of many large-seeded plants is thought to have been handicapped by the extinction of megafauna in the late Pleistocene, and due to the ongoing defaunation of the largest of the extant dispersers. Oversized fruits defined as "megafaunal" provide variable amounts of flesh even though many of them cannot be ingested entirely, nor their seeds defecated, by any extant vertebrate. This apparent mismatch lead to the hypothesis of anachronisms involving extinct megafauna as dispersal-mediated selective agents on fruit traits shaped through endozoochory. It has been suggested that free-ranging livestock partially supply the dispersal functions previously provided by those globally or regionally extinct species. However, there is little knowledge on the role of livestock as a surrogate for megafauna dispersal agents relative to living wild dispersers. Here, we focus on seed dispersal of six palm species (Attalea eichleri, Attalea barreirensis, Attalea speciosa, Attalea princeps, Mauritia flexuosa, Acrocomia totai) with large fruits that conform to the so-called "megafaunal syndrome". Data on seed dispersal were obtained by observations and camera trapping in the Cerrado, Pantanal and Amazonia biomes in Bolivia and Brazil. Rich communities of wild seed dispersers differing among palm species and study areas were recorded, including rodents, monkeys, canids, and a wide variety of birds, especially parrots. Long-distance primary dispersal was mainly conducted by parrots, while multiple species acted as short-and medium-distance secondary dispersers. Among livestock, dispersal was limited to seeds of A. totai and A. princeps moved by several species through stomatochory and endozoochory (mainly regurgitation). These results show that the large seeds can be efficiently dispersed externally by a wide array of present-day vertebrates of variable size but much smaller than extinct megafauna and livestock. A knowledge gap of the natural history of these and other plants with oversized fruits assumed to be maladapted for contemporary dispersal may have been partially favored by neglecting some key disperser guilds (e.g., parrots) and dispersal mechanisms (e.g., ectozoochory). The evaluation of historic and ongoing defaunation of key external dispersers is advocated to understand the influence of actual (rather than putative) dispersers on contemporary frugivore-plant mutualistic interactions.

Conserving the Diversity of Ecological Interactions: The Role of Two Threatened Macaw Species as Legitimate Dispersers of “Megafaunal” Fruits

“…In these cases, we also considered minimum dispersal distances, as measured from the location of the first sighting to where the disperser perched for handling the fruit, where they released the fruit in flight, or where they were lost from sight in flight. In other instances, we found seeds under perches (trees, cliffs, and fence poles), where we observed macaws consuming them, and conservatively estimated the minimum dispersal distance as the distance to the closest fruiting female plant (see [17,32,46] for the same methodology).…”

“…Following this argument, the survival of megafauna-dependent plants since the Pleistocene could be explained by the action of less efficient secondary or sporadic primary dispersers, anthropogenic, and abiotic factors [15]. We did not aim to identify here the potential disperser coteries for several palm species [17], but rather we endeavored to test the hypothesis that two macaw species could serve as their legitimate, long-distance seed dispersers. This potential plant-animal mutualism has been so far highly unexpected since, contrary to other macaws that only consume the pulp and discard the seeds of palms [24], Anodorhynchus macaws are able to crack the woody coat to consume the seeds that dominate their diet.…”

“…This impact can be traced back to the possible human influence on the extinction of Pleistocene megafauna [11,14], i.e., mammals, such as giant sloths and gomphotheres, of seven genera with a body mass >1000 kg [15], which were thought to act in the past as dispersers of large fruits ("megafaunal fruits", usually >4 cm in diameter [15]) of many still extant plants. Although it has been argued that livestock partially filled the seed dispersal role of extinct megafauna [15][16][17], and of extant but largely decimated large mammals, such as tapirs [17,18], the presumably reduced dispersal of these large-fruited plants nowadays is widely recognized as a seed dispersal anachronism, the so-called megafaunal syndrome [15,16].…”

“…They have the strongest beaks among parrots, allowing them even to crack the nuts of large-sized palm fruits after defleshing them and discarding the mesocarp [25,27]. Therefore, these macaws might not be contributing to legitimate seed dispersal despite having been observed transporting fruits in flight using their beaks or feet [17,23].…”

“…This was prompted by recent findings showing that other parrot species, also considered pure seed predators, acted as seed dispersers within an antagonism-mutualism continuum [28]. As previously mentioned, Anodorhynchus macaws have been observed transporting fruits picked from the mother plants to distant perches for handling and consumption [17,23], but it is unknown whether all seeds are then predated, or a fraction of them survive predation and thus contributes to effective primary seed dispersal. On the other hand, these macaws have been reported actively searching for and predating on large palm seeds excreted by livestock, which has been interpreted as an evolutionary adaptation to exploit seeds excreted by extinct megafauna [27,29].…”