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

Abstract

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”.

Waterbird seed‐dispersal networks are similarly nested but less modular than those of frugivorous birds, and not driven by functional traits

“…Data for (d) and (e) were from the LEDA traitbase (Kleyer et al., 2008), data for (g) and (h) from the Baseflor database (Julve, 1998). Dispersal syndromes are not reliable indicators of dispersal mechanisms since they only assign endozoochory for fleshy‐fruited plants (Costea et al., 2019). However, since they assign the plant species studied to water, wind and other vectors, birds feeding in different ways may be expected to ingest seeds from different syndromes.…”

“…Most angiosperms have dry indehiscent fruits or small seeds released from dehiscent fruits (Julve, 1998). Many plant taxa are dispersed by vertebrate vectors such as ungulates or waterbirds, in which plants obtain benefits from seeds that survive gut passage and are effectively dispersed, and animals obtain food from foliage and from the fraction of seeds digested during gut passage (Albert et al., 2015; Costea et al., 2019). Migratory waterbirds are particularly important for long‐distance dispersal, and hence for maintaining ecosystem biodiversity and functioning, genetic flow or mixing between plant populations (Kleyheeg, Treep, de Jager, Nolet, & Soons, 2017).…”

Cuscuta seeds: Diversity and evolution, value for systematics/identification and exploration of allometric relationships

“…Seeds were dehydrated through an ethanol series (50%, 70%, 85%, 95%, and 100%; each step 1h) and then dried with a Tousimis Autosamdri-931 critical point dryer. Using SEM has been proven to be a valid approach to study not only the external morphology of seeds, but also the seed coat anatomy in Cuscuta [13,14]. For anatomy, 5-10 seeds were sectioned longitudinally by hand with a razor blade along the hilum area.…”

“…In Cuscuta, the inner (or single palisade when only one palisade layer is present outside hilum area) is strongly lignified and it represents the ultimate mechanical defense of the seeds. Bird endozoochory experiments reported that gut passage partially or entirely stripped the outer palisade layer, while the inner or single palisade layer was little affected [13,14]. If the function of the inner palisade layer (or single one in Monogynella) is to safeguard the impermeability of the seed coat, ensure physical dormancy and provide an ultimate line of mechanical defense, the role of the external palisade layer is not clear.…”

“…The seeds of Cuscuta lack apparent morphological adaptations for a particular dispersal syndrome and have been considered "simple" or "unspecialized" [e.g., [10][11][12]. However, dodder seeds have been recently reported to be long-distance dispersed via bird endozoochory [13,14] or water in the species with indehiscent fruits [15].…”