Seed mass, hardness, and phylogeny explain the potential for endozoochory by granivorous waterbirds

Abstract

Field studies have shown that waterbirds, especially members of the Anatidae family, are major vectors of dispersal by endozoochory for a broad range of plants lacking a fleshy fruit, yet whose propagules can survive gut passage. Widely adopted dispersal syndromes ignore this dispersal mechanism, and we currently have little understanding of what traits determine the potential of angiosperms for endozoochory by waterbirds. Results from previous experimental studies have been inconsistent as to how seed traits affect seed survival and retention time in the gut and have failed to control for the influence of plant phylogeny. Using 13 angiosperm species from aquatic and terrestrial habitats representing nine families, we examined the effects of seed size, shape, and hardness on the proportion of seeds surviving gut passage through mallards (Anas platyrhynchos) and their retention time within the gut. We compiled a molecular phylogeny for these species and controlled for the nonindependence of taxa due to common descent in our analyses. Intact seeds from all 13 species were egested, but seed survival was strongly determined by phylogeny and by partial effects of seed mass and hardness (wet load): species with seeds harder than expected from their size, and smaller than expected from their loading, had greater survival. Once phylogeny was controlled for, a positive partial effect of seed roundness on seed survival was also revealed. Species with seeds harder than expected from their size had a longer mean retention time, a result retained after controlling for phylogeny. Our study is the first to demonstrate that seed shape and phylogeny are important predictors of seed survival in the avian gut. Our results demonstrate that the importance of controlling simultaneously for multiple traits and relating single traits (e.g., seed size) alone to seed survival or retention time is not a reliable way to detect important patterns, especially when phylogenetic effects are ignored.

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

“…We also found no influence of seed size on network structure. However, seed size is linked to the effectiveness of seed dispersal, since small and hard seeds survive gut passage in larger numbers (Lovas‐Kiss et al., 2020; Soons et al., 2008). Morphological dispersal syndromes also played no role in the assemblage structure, although this is not surprising since they ignore endozoochory of non‐fleshy fruited plants (i.e.…”

“…Diet was determined from the content of the digestive tract, and seeds were identified to the genus or species level in most cases. Presence of seeds in the upper digestive tract is a suitable proxy for seed dispersal, because experimental and field studies show that a proportion of ingested seeds (often exceeding 30%;) from all taxa survive digestion via rapid gut passage or regurgitation (Brochet, Guillemain, Gauthier‐Clerc, Fritz, & Green, 2010; Lovas‐Kiss et al., 2020; Soons et al., 2008). The probability of effective dispersal increases with the number of seeds in a bird's digestive tract, so that the number of seeds ingested provides a quantitative proxy for seed dispersal (Schupp, Jordano, & Gómez, 2010).…”

“…Experimental studies with dabbling ducks and shorebirds suggest that longer maximum retention times during gut passage of relatively small and hard seeds confer a higher seed survival and increase long‐distance dispersal (Green et al., 2016; Lovas‐Kiss et al., 2020; Soons, van der Vlugt, van Lith, Heil, & Klaassen, 2008). However, there is an absence of community‐level analyses of how animal and seed traits determine the structure of waterbird–plant assemblages, and of which traits drive dispersal interactions.…”

The decline and recovery of populations of Potamogeton coloratus in Hungary

“…The faecal samples were collected at 1, 2, 3, 4, 5, 6, 7, 21, 31 and 45 h after force-feeding. Each dropping was dried at room temperature and every intact seed was separated and counted under a binocular microscope (see detailed methodology in Lovas-Kiss et al 2020). We determined seeds to be intact if there were no visible fissure or any damage to their coat.…”

“…P. pusillus, P. pectinatus) is reported in faeces of wild mallards in Hungary (Lovas-Kiss et al 2018). The seed of P. coloratus is the smallest of the pondweeds, which is known to facilitate rapid, intact and viable passage through the digestive tract of aquatic birds and is thought to facilitate long-distance dispersal (Jakobsson & Eriksson 2000, Soons et al 2008, Lovas-Kiss et al 2020. Germination of the seed of some species of plants benefit from the passage through the digestive tract of water birds, which results in both mechanical and chemical scarification, as in P. pectinatus (Santamaría et al 2002), but we were not able to test this in our study on P. coloratus.…”