Overlooked Parrot Seed Dispersal in Australia and South America: Insights on the Evolution of Dispersal Syndromes and Seed Size in Araucaria Trees

Abstract

While Psittaciformes (parrots and allies) are well-recognized as highly-mobile seed predators, their role as seed dispersers has been overlooked until very recently. It remains to be determined whether this role is anecdotic or is a key mutualism for some plant species. We recently found that the large nut-like seeds of the two South American Araucaria tree species (Araucaria araucana in Andean forests and Araucaria angustifolia in Atlantic forests, weighing c. 3.5 and 7 g, respectively) are frequently dispersed, and to long distances, by parrots. Moreover, both observational and experimental work demonstrated that dispersed seeds can germinate faster after partial predation by parrots. Here, we hypothesized that a third, even larger-seeded (17.5 g) congeneric Australian species (A. bidwillii) is also dispersed by parrots. We surveyed 52 A. bidwillii and 42 A. cunninghamii (a sympatric species with small winged seeds, c. 0.2 g) during the seeding period. We found that sulfur-crested cockatoos (Cacatua galerita) consumed large amounts of seeds from all of the A. bidwillii trees surveyed. Cockatoos dispersed ca. 30% of the seeds they removed from the mother tree, carrying the seeds to distant perches for handling or dropped them while flying. Dispersal distances ranged between 10 and 153 m (mean = 61 m). Most seeds handled for consumption (93%) were fully eaten but others were dropped intact (3%) or only partially eaten (4%), and germination was confirmed for both intact and partially-eaten dispersed seeds. Moreover, seeds dropped by cockatoos facilitated secondary seed dispersal by conspecifics and another three bird species. We found no evidence of other primary dispersal species for A. bidwillii, while the small, winged seeds of Araucaria cunninghamii were only dispersed through barochory and anemochory. The seed weight of the three Araucaria species dispersed by zoochory is strongly related to the body mass of their main seed-disperser Tella et al. Parrot Seed Dispersal of Araucaria parrot species. These results support a role for parrots as key dispersers of the three large-seeded Araucaria species around the world, and suggest that large seeds may have evolved-at least partially-as an adaptation that allows trees to attract parrots, satiate them, and benefit from their long-distance seed dispersal services.

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

“…This supports the key role of parrots as efficient dispersal agents of many large-fruited plants (reviewed in Blanco et al, 2018). Owing to their general wasteful feeding behavior, parrots disperse seeds at distances ranging from below the fruiting palm where secondary dispersers act, to long distances (up to several kilometers) that are generally underestimated due to logistic challenges of measurement (Tella et al, 2016a(Tella et al, , 2019Baños-Villalba et al, 2017). Among secondary dispersers, rich assemblages of frugivorous and omnivorous vertebrates mostly disseminated seeds externally, although some also ingested and defecated or regurgitated the seeds of the smallest-fruited palm species.…”

“…Overall, external dispersal emerges as the major mechanism exploited by these large-fruited plants to disseminate their seeds at variable distances by an array of dispersers. Information on disperser assemblages of the study palms in other geographical areas (Zona and Henderson, 1989;Eiserhardt et al, 2011;Virapongse et al, 2017), as well as on other large-fruited plants (Jansen et al, 2012;Tella et al, 2015Tella et al, , 2019Blanco et al, 2016;Rebein et al, 2017) support these mixed redundant and complementary dispersal systems by ectozoochory. Indeed, studies revisiting and adopting the megafaunal seed dispersal hypothesis recognized guilds of external dispersers with a role in population dynamics of these plants, although overlooked their potential impacts as selective agents shaping large size and other fruit traits (Guimarães et al, 2008;McConkey et al, 2018).…”

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

“…We traveled through the foraging areas of the species and stopped when we found a group of foraging macaws. We then observed their foraging behavior with binoculars and telescopes from a distance to avoid disturbance (see [28,32,45] for the same methodology). We recorded how macaws handled fruits (consuming or not the seeds) and any event in which they dispersed fruits from the mother plant (primary dispersal) or seeds excreted by livestock (tertiary dispersal).…”

“…Similar to other parrot species, macaws often move within and among canopies, making it difficult to focus on individual birds. We, therefore, recorded the total number of fruits consumed on the mother palm and the total number of fruits dispersed to distant perches by any individual observed to calculate the flocks' dispersal rate (see [24,32,46] for the same methodology). On the other hand, the fruits of the two bush-layer palm species present in the Cerrado (Attalea barreirensis and Attalea eichleri) are almost at ground level, thus making direct observations of foraging macaws from a distance difficult.…”

“…Similarly, it is unknown whether this tertiary dispersal process, following secondary dispersal by livestock, translates into effective seed dispersal. We relied on direct observations of foraging and fruit-dispersing macaws, complemented with camera trapping, as the most recommendable approach when the visual tracking of seed-dispersing vectors is affordable [30,31] (see also [24,32] for the same approach). Following this methodology, we were able to study all the subsequent steps of the multistage dispersal process: 1) fruit handling, 2) dispersal rates, 3) dispersal distances, 4) survival, and 5) germination of dispersed seeds (i.e., realized dispersal).…”