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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 (Elaeocarpus dentatus, E. hookerianus, Prumnopitys ferruginea, P. taxifolia, Vitex lucens) 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 E. dentatus and P. ferruginea 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.

SUBMITTER: Carpenter JK

PROVIDER: S-EPMC5936733 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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

Carpenter Joanna K JK Wood Jamie R JR Wilmshurst Janet M JM Kelly Dave D

Proceedings. Biological sciences 20180401 1877

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 (<i>Elaeocarpus dentatus, ...[more]

PMID: 29669903

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Project description:BackgroundSome 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 findingsWe 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/significanceMegafaunal 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.

Project description:The widespread loss of native species and the introduction of non-native species has important consequences for island ecosystems. Non-native species may or may not functionally replace the role of native species in ecological processes such as seed dispersal. Although the majority of Hawaii's native plants require bird-mediated seed dispersal, only one native frugivore, Omao (Myadestes obscurus), persists in sufficient numbers to fill this functional role. Omao are restricted to less than half their original range, but two introduced frugivores are abundant throughout Hawaii. Given large-scale extinctions on islands, it is important to understand whether introduced birds serve as functional replacements or whether the absence of native frugivores alters plant communities. To assess seed dispersal by native and introduced birds, seed rain, vegetation characteristics, bird diet, density and habitat use were measured at three sites with Omao and three sites without Omao on Hawaii Island. The diet of native and introduced birds overlapped substantially, but Omao dispersed a variety of native species (n = 6) relatively evenly. In contrast, introduced birds dispersed an invasive species and fewer native species (n = 4), and >90 % of seeds dispersed by introduced birds were from two ubiquitous small-seeded species. Seed rain was significantly greater and more species rich at sites with Omao. These findings suggest that patterns of seed dispersal are altered following the local extinction of a native island frugivore. To more directly evaluate the relative roles of native and introduced frugivores in ecological processes, future studies could include reintroducing Omao to a suitable habitat within its historic range, or novel introductions to nearby islands where closely related species are now extinct. In an era of widespread extinction and invasion of island ecosystems, understanding the consequences of novel animal assemblages for processes like seed dispersal will be critical for maintaining diverse and self-regenerating plant communities.

Project description:Accurate tracking of seed dispersal is critical for understanding gene flow and seed bank dynamics, and for predicting population distributions and spread. Available seed-tracking techniques are limited due to environmental and safety issues or requirements for expensive and specialized equipment. Furthermore, few techniques can be applied to studies of water-dispersed seeds. Here we introduce a new seed-tracking method using safranine to stain seeds/fruits by immersing in (ex situ) or spraying with (in situ) staining solution. The hue difference value between pre- and post-stained seeds/fruits was compared using the HSV color model to assess the effect of staining. A total of 181 kinds of seeds/fruits out of 233 tested species of farmland weeds, invasive alien herbaceous plants and trees could be effectively stained magenta to red in hue (320-360°) from generally yellowish appearance (30-70°), in which the other 39 ineffectively-stained species were distinguishable by the naked eye from pre-stained seeds. The most effectively stained seeds/fruits were those with fluffy pericarps, episperm, or appendages. Safranine staining was not found to affect seed weight or germination ability regardless of whether seeds were stained ex situ or in situ. For 44 of 48 buried species, the magenta color of stained seeds clearly remained recognizable for more than 5 months after seeds were buried in soil. Tracking experiments using four species (Beckmannia syzigachne, Oryza sativa f. spontanea, Solidago Canadensis, and Acer buergerianum), representing two noxious agricultural weeds, an alien invasive plant, and a tree, respectively, showed that the safranine staining technique can be widely applied for studying plant seed dispersal. Identifying and counting the stained seeds/fruits can be executed by specially complied Python-based program, based on OpenCV library for image processing and Numpy for data handling. From the above results, we conclude that staining with safranine is a cheap, reliable, easily recognized, automatically counted, persistent, environmentally safe, and user-friendly tracking-seed method. This technique may be widely applied to staining most of the seed plant species and the study of seed dispersal in arable land and in disturbed and natural terrestrial or hydrophytic ecological systems.

Dataset Information

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

Publications

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

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