Seed dispersal by waterbirds: a mechanistic understanding by simulating avian digestion

Abstract

Waterbirds disperse plant species via ingestion and egestion of seeds (endozoochory). However, our understanding about the regulating effects of seed traits, underlying mechanisms and possible (co)evolutionary processes is limited by our traditional reliance on data from feeding experiments with living waterbirds. Here, we overcome these limitations by developing and applying a new bioassay that realistically simulates digestive processes for Anseriformes waterbirds. We test three hypotheses: 1) seed survival and germination are most affected by mechanical digestion in the waterbird gizzard; 2) seed size, hardness, imbibition and shape regulate seed survival; and 3) plants growing in aquatic habitats benefit most from endozoochory by waterbirds. Experiments with 28 200 seeds of 48 plant species demonstrated species‐specific seed survival that was entirely determined by digestion in the avian gizzard. Intestinal digestion did not affect seed survival but affected seed establishment (germinability and germination time) for 21% of the species. Large, hard seeds survived the simulations the best, in contrast to generally higher seed survival for smaller seeds during in vivo experiments. This mechanistically explains that small seeds escape digestive processes rather than being inherently more resistant (the ‘escape mechanism'), while large seeds are retained until fully digested or regurgitated (the ‘resistance and regurgitation mechanism'). Plants growing in wetter habitats had similar seed survival, but digestive processes stimulated their germinability and accelerated their germination more than for terrestrial plants. This indicates a relative advantage of endozoochory for plant species growing in wet habitats, possibly reflecting a co‐evolutionary response related to dormancy breaking by gut passage. Simulating seed gut passage using a bioassay allowed establishing mechanisms and identifying relevant seed traits involved in seed dispersal by waterbirds. This information enhances our understanding of how animal species shape plant species distributions, which is extremely relevant now that current anthropogenic pressures already severely impact plant dispersal capacities.

Dispersal of aquatic and terrestrial organisms by waterbirds: A review of current knowledge and future priorities

“…Furthermore, these syndromes fail dismally to predict dispersal events in the case of waterbirds and other non‐frugivorous vectors, whether by endozoochory or epizoochory (Green et al, 2022). This implies that research focus should shift from classical syndromes to other traits known to influence the rates of waterbird zoochory, such as seed size, shape, hardness or buoyancy (de Vlaming & Proctor, 1968; Green et al, 2016; Soons et al, 2016; van Leeuwen, Soons, et al, 2022). Plant life forms and habitat requirement (e.g., soil moisture, salinity tolerance) indicators also can partly explain the importance of waterbird vectors (Almeida et al, 2022; Hattermann et al, 2019; Soons et al, 2016).…”

“…In general, plants with seeds of a smaller size show higher survival during gut passage, and higher prevalence in field studies of endozoochory, although the latter may partly reflect the inverse relationship between propagule size and propagule abundance across species in nature (Green et al, 2022; Hattermann et al, 2019; van Leeuwen, van der Velde, van Groenendael, et al, 2012). Small seeds pass more quickly from the gizzard into the intestines, not only promoting survival, but also shortening retention time (Kleyheeg, Nolet, et al, 2018; van Leeuwen, Soons, et al, 2022). Hence, plant species with large, hard seeds can have higher seed survival and longer retention times than small, soft‐seeded species (García‐Álvarez et al, 2015).…”

“…No single seed trait is an adequate predictor of fate during gut passage, yet experimental studies to date have focused on only one or two traits, and have usually overlooked the important role of phylogeny (Lovas‐Kiss, Vincze, Löki, et al, 2020). In future experiments, larger numbers of plant species and more seed traits should be included, and this may be facilitated via laboratory simulations of gut passage, reducing the need for animal experimentation (Kleyheeg, Claessens, et al, 2018; van Leeuwen, Soons, et al, 2022). However, more work is needed to develop convincing simulations, and clarify how they compare with seed passage through real digestive systems and their microbiomes.…”

“…How seed traits interact with gut passage to influence germination patterns is complex, and general patterns remain unclear (Kleyheeg, Claessens, et al, 2018), especially since the results of comparisons with control seeds also are highly dependent on storage and germination conditions, and their own interactions with dormancy strategies of different plant species (see Interaction between zoochory and dormancy section below). However, simulated gut passage increases germinability and germination speed more in aquatic plants than in terrestrial ones (van Leeuwen, Soons, et al, 2022). Some of the seed traits described in this section also may be relevant for epizoochory, although data for waterbirds remain scarce (Coughlan et al, 2017; Green et al, 2016; Raulings et al, 2011; Reynolds & Cumming, 2016b), and should be expanded experimentally.…”

“…Waterfowl with a more powerful gizzard, and more grit used to crush food, destroy more propagules before they reach the intestines (Figuerola et al, 2002, 2005). Grit size also is important, since smaller propagules can fit into gaps and avoid being crushed between larger particles (van Leeuwen, Soons, et al, 2022).…”