The effect of gut passage by waterbirds on the seed coat and pericarp of diaspores lacking "external flesh": Evidence for widespread adaptation to endozoochory in angiosperms

The widely accepted "endozoochory syndrome" is assigned to angiosperm diaspores with a fleshy, attractive tissue and implies the existence of adaptations for protection against digestion during gut passage. This syndrome has led diaspore fleshiness to be emphasized as the exclusive indicat...

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Published in:	PloS one Vol. 14; no. 12; p. e0226551
Main Authors:	Costea, Mihai, El Miari, Hiba, Laczkó, Levente, Fekete, Réka, Molnár, Attila V, Lovas-Kiss, Ádám, Green, Andy J
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 19-12-2019 Public Library of Science (PLoS)
Subjects:	Adaptation Adaptation, Physiological Adaptations Angiosperms Animals Aquatic birds Biogeography Biology and Life Sciences Biomechanical Phenomena Birds Birds - physiology Cuticle Diaspore Digestion Digestive system Digestive tract Dispersal Dispersion Dormancy Ecology Frugivory Fruit Gastrointestinal tract Germinability Germination Granivory Gymnosperms Intestines - physiology Laurier, Wilfrid (1841-1919) Magnoliopsida - growth & development Magnoliopsida - physiology Morphology Pericarp Physiology Plant sciences Questions Seed coats Seed Dispersal Seeds Specialization Survival Waterfowl Hungary Waterloo Ontario Canada Canada
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Summary:	The widely accepted "endozoochory syndrome" is assigned to angiosperm diaspores with a fleshy, attractive tissue and implies the existence of adaptations for protection against digestion during gut passage. This syndrome has led diaspore fleshiness to be emphasized as the exclusive indicator of endozoochory in much of the ecology and biogeography research. Crucially, however, endozoochory in nature is not limited to frugivory, and diaspores without "external flesh" are commonly dispersed, often over long distances, via birds and mammals by granivory. A key question is: are such diaspores somehow less prepared from an architectural point of view to survive gut passage than fleshy diaspores? To answer this question, we selected 11 European angiosperm taxa that fall outside the classical endozoochory syndrome yet are known to be dispersed via endozoochory. We studied their seed coat/pericarp morphology and anatomy both before and after gut passage through granivorous waterfowl, and determined their seed survival and germinability. We found no fundamental differences in the mechanical architecture of the seed coat and pericarp between these plants dispersed by granivory and others dispersed by frugivory. Neither diaspore traits per se, nor dormancy type, were strong predictors of diaspore survival or degree of damage during gut passage through granivores, or of the influence of gut passage on germinability. Among our 11 taxa, survival of gut passage is enabled by the thick cuticle of the exotesta or epicarp; one or several lignified cell layers; and diverse combinations of other architectural elements. These protection structures are ubiquitous in angiosperms, and likely to have evolved in gymnosperms. Hence, many angiosperm diaspores, dry or fleshy, may be pre-adapted to endozoochory, but with differing degrees of specialization and adaptation to dispersal mechanisms such as frugivory and granivory. Our findings underline the broad ecological importance of "non-classical endozoochory" of diaspores that lack "external flesh".
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: The authors have declared that no competing interests exist.
ISSN:	1932-6203 1932-6203
DOI:	10.1371/journal.pone.0226551