An avian seed dispersal paradox: New Zealand's extinct megafaunal birds did not disperse large seeds

Abstract

Often the mutualistic roles of extinct species are inferred based on plausible assumptions, but sometimes palaeoecological evidence can overturn such inferences. We present an example from New Zealand, where it has been widely assumed that some of the largest-seeded plants were dispersed by the giant extinct herbivorous moa (Dinornithiformes). The presence of large seeds in preserved moa gizzard contents supported this hypothesis, and five slow-germinating plant species () with thick seedcoats prompted speculation about whether these plants were adapted for moa dispersal. However, we demonstrate that all these assumptions are incorrect. While large seeds were present in 48% of moa gizzards analysed, analysis of 152 moa coprolites (subfossil faeces) revealed a very fine-grained consistency unparalleled in extant herbivores, with no intact seeds larger than 3.3 mm diameter. Secondly, prolonged experimental mechanical scarification of and seeds did not reduce time to germination, providing no experimental support for the hypothesis that present-day slow germination results from the loss of scarification in moa guts. Paradoxically, although moa were New Zealand's largest native herbivores, the only seeds to survive moa gut passage intact were those of small-seeded herbs and shrubs.

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

“…Therefore, the results of this study suggest that fruits of these palms cannot be further supported as anachronistic. These findings add to growing evidence indicating that assumptions related to extinct megafauna because of their large size are not necessary to understand all past and current mutualistic frugivore-large fruit interactions (Howe, 1985;Jansen et al, 2012;Baños-Villalba et al, 2017;Rebein et al, 2017;Carpenter et al, 2018).…”

“…A comparative study of Neotropical large-fruited plants revisited and refined the megafaunal seed dispersal hypothesis, introducing an operational definition and classification of megafaunal fruits, like oversized fruits with fleshy pulp packaging extremely large individual seeds or large numbers of moderatelysized seeds (Guimarães et al, 2008). In using these criteria, subsequent studies have adopted the conjecture that extinct megafauna acted as legitimate past dispersers of many oversized fruits (Onstein et al, 2018;van Zonneveld et al, 2018), while others critically tested its assumptions given knowledge on the effectiveness of smaller contemporary dispersal agents using variable dispersal mechanisms (Jansen et al, 2012;Boone et al, 2015;Baños-Villalba et al, 2017;Rebein et al, 2017;Carpenter et al, 2018;McConkey et al, 2018). Multiple variably-sized extant dispersers and abiotic factors have been recognized in present-day dispersal interactions with "megafaunal plants, " while assuming the existence of body-size trade-offs constraining dispersal ability via fruit ingestion and seed defecation (Donatti et al, 2007;Guimarães et al, 2008;Pires et al, 2018).…”

“…Multiple variably-sized extant dispersers and abiotic factors have been recognized in present-day dispersal interactions with "megafaunal plants, " while assuming the existence of body-size trade-offs constraining dispersal ability via fruit ingestion and seed defecation (Donatti et al, 2007;Guimarães et al, 2008;Pires et al, 2018). Thus, the main challenge facing the megafaunal hypothesis remains the establishment of the disperser size that represents a functionally pervasive trait for each plant species (Howe, 1985(Howe, , 2016Jansen et al, 2012;Carpenter et al, 2018;McConkey et al, 2018), without succumbing to the circular rationale that assumes that large-sized vertebrates are major seed dispersers of large-fruited plants (Burns, 2013;Chen and Moles, 2015;Sebastián-González, 2017). Therefore, since Howe's (1985) critical review, the testing of the megafaunal seed dispersal hypothesis continues to be challenged by a general lack of knowledge on dispersers and dispersal strategies of many large-fruited plants (Fleming and Kress, 2013;Jordano, 2014).…”

Introduction of mammalian seed predators and the loss of an endemic flightless bird impair seed dispersal of the New Zealand tree Elaeocarpus dentatus

“…A New Zealand study on two other large-fruited native trees (Corynocarpus laevigatus and Beilschmiedia tarairi) found better recruitment to the 2-year-old seedling stage away from parents of both species, suggesting that frugivore declines would reduce regeneration (Wotton & Kelly, 2011). Carpenter, Wood, Wilmshurst, and Kelly (2018) demonstrated that simulated avian gut passage may increase the germinability of hinau compared to whole fruits, so the results we have shown could have flow-on effects to recruitment, but further research is needed to examine hinau's susceptibility to Janzen-Connell effects.…”

“…While weka provided good dispersal quantity for hinau, further research is required to assess the quality of dispersal they provide. Mechanical scarification of the seed coat has been shown to increase the germinability of hinau seeds (Carpenter et al., ), and it is possible that the grit within weka gizzards (Carroll, ) may abrade hinau seeds during gut passage in a similarly beneficial way. Germination trials using weka‐passed seeds from a wide range of plant species would be useful.…”