How intraspecific variation in seed‐dispersing animals matters for plants

Seed dispersal by animals is a complex phenomenon, characterized by multiple mechanisms and variable outcomes. Most researchers approach this complexity by analysing context‐dependency in seed dispersal and investigating extrinsic factors that might influence interactions between plants and seed dispersers. Intrinsic traits of seed dispersers provide an alternative way of making sense of the enormous variation in seed fates. I review causes of intraspecific variability in frugivorous and granivorous animals, discuss their effects on seed dispersal, and outline likely consequences for plant populations and communities. Sources of individual variation in seed‐dispersing animals include sexual dimorphism, changes associated with growth and ageing, individual specialization, and animal personalities. Sexual dimorphism of seed‐dispersing animals influences seed fate through diverse mechanisms that range from effects caused by sex‐specific differences in body size, to influences of male versus female cognitive functions. These differences affect the type of seed treatment (e.g. dispersal versus predation), the number of dispersed seeds, distance of seed dispersal, and likelihood that seeds are left in favourable sites for seeds or seedlings. The best‐documented consequences of individual differences associated with growth and ageing involve quantity of dispersed seeds and the quality of seed treatment in the mouth and gut. Individual specialization on different resources affects the number of dispersed plant species, and therefore the connectivity and architecture of seed‐dispersal networks. Animal personalities might play an important role in shaping interactions between plants and dispersers of their seeds, yet their potential in this regard remains overlooked. In general, intraspecific variation in seed‐dispersing animals often influences plants through effects of these individual differences on the movement ecology of the dispersers. Two conditions are necessary for individual variation to exert a strong influence on seed dispersal. First, the individual differences in traits should translate into differences in crucial characteristics of seed dispersal. Second, individual variation is more likely to be important when the proportions of particular types of individuals fluctuate strongly in a population or vary across space; when proportions are static, it is less likely that intraspecific differences will be responsible for changes in the dynamics and outcomes of plant–animal interactions. In conclusion, focusing on variation among foraging animals rather than on species averages might bring new, mechanistic insights to the phenomenon of seed dispersal. While this shift in perspective is unlikely to replace the traditional approach (based on the assumption that all important variation occurs among species), it provides a complementary alternative to decipher the enormous variation observed in animal‐mediated seed dispersal.     

Restoration of Species Richness in Abandoned Mediterranean Grasslands: Seeds in Cattle Dung

Abstract Endozoochory has proven to be a highly effective mechanism in the dispersal of viable seeds in Mediterranean grasslands. We studied the effect of cattle dung application on species richness, particularly on the reintroduction of species lost after abandonment. Sown and control plots were monitored for 3 years after dung sowing. We found a significant increase in small‐scale richness, which may be attributed to the treatment, with the inclusion of species detected in the dung and in the grazed pasture. The differences in richness and floristic composition diminished over time. This experiment proves the potential utility of this treatment for the restoration of species richness in abandoned pastures, although supplementary steps are necessary, including further sowing and/or shrub cutting in subsequent years.     

Opposing forces of seed dispersal and seed predation by mammals for an invasive cactus in central Kenya

The invasive erect prickly pear cactus (Opuntia stricta) has reduced rangeland quality and altered plant communities throughout much of the globe. In central Kenya's Laikipia County, olive baboons (Papio anubis) frequently consume O. stricta fruits and subsequently disperse the seeds via defecation. Animal‐mediated seed dispersal can increase germination and subsequent survival of plants. However, consumption of seeds (seed predation) by rodents may offset the potential benefits of seed dispersal for cactus establishment by reducing the number of viable seeds. We investigated foraging preferences of a common and widely distributed small mammal—the fringe‐tailed gerbil (Gerbilliscus robustus), between O. stricta seeds deposited in baboon faeces versus control O. stricta seeds. In addition to providing evidence of seed predation on O. stricta by G. robustus, our data show that seed removal was higher (shorter time to use) for seeds within faeces than for control seeds. G. robustus clearly prefers seeds within faeces compared to control seeds. These results suggest that high abundances of rodents may limit successful establishment of O. stricta seeds, possibly disrupting seed dispersal via endozoochory by baboons.     

A non‐destructive sampling protocol for field studies of seed dispersal by fishes

This paper presents a standardized protocol for the non‐lethal capture of fishes, sampling of stomach contents and quantification of seed dispersal efficiency by frugivorous fishes. Neotropical pacu Piaractus mesopotamicus individuals were collected with fruit‐baited hooks. The diets of 110 fish were sampled using a lavage method, which retrieved >90% of stomach contents of both juveniles and adults and allowed individuals to recover within 5 min of treatment. The proportional volume of six food categories was similar for stomachs and whole digestive tracts retrieved by dissection. Fruit pulp was proportionally lower in the stomach. The abundance and species richness of intact seeds increased with fish size independent of whether only stomachs or whole digestive tracts were analysed. The analysis of stomach contents accounted for 62·5% of the total species richness of seeds dispersed by P. mesopotamicus and 96% of common seeds (seed species retrieved from more than one fish). Germination trials revealed that seed viability was similar for seeds collected from the stomach via lavage and seeds that passed through the entire digestive tract. Therefore, stomach contents provide an unbiased representation of the dietary patterns and seed dispersal of frugivorous fishes.     

Potential for passive internal dispersal: eggs of an aquatic leaf beetle survive passage through the digestive system of mallards

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Crayfish invasion facilitates dispersal of plants and invertebrates by gulls

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The potential for dispersal of microalgal resting cysts by migratory birds

Most microalgal species are geographically widespread, but little is known about how they are dispersed. One potential mechanism for long‐distance dispersal is through birds, which may transport cells internally (endozoochory) and deposit them during, or in‐between, their migratory stopovers. We hypothesize that dinoflagellates, in particular resting stages, can tolerate bird digestion; that bird temperature, acidity, and retention time negatively affect dinoflagellate viability; and that recovered cysts can germinate after passage through the birds’ gut, contributing to species‐specific dispersal of the dinoflagellates across scales. Tolerance of two dinoflagellate species (Peridiniopsis borgei, a warm‐water species and Apocalathium malmogiense, a cold‐water species) to Mallard gut passage was investigated using in vitro experiments simulating the gizzard and caeca conditions. The effect of in vitro digestion and retention time on cell integrity, cell viability, and germination capacity of the dinoflagellate species was examined targeting both their vegetative and resting stages. Resting stages (cysts) of both species were able to survive simulated bird gut passage, even if their survival rate and germination were negatively affected by exposure to acidic condition and bird internal temperature. Cysts of A. malmogiense were more sensitive than P. borgei to treatments and to the presence of digestive enzymes. Vegetative cells did not survive conditions of bird internal temperature and formed pellicle cysts when exposed to gizzard‐like acid conditions. We show that dinoflagellate resting cysts serve as dispersal propagules through migratory birds. Assuming a retention time of viable cysts of 2–12 h to duck stomach conditions, cysts could be dispersed 150–800 km and beyond.     

Seed dispersal by neotropical waterfowl depends on bird species and seasonality

1. Waterbird‐mediated endozoochory is an essential mechanism for the dispersal of sessile organisms in freshwater ecosystems. However, in the neotropics there are no previous studies of how different waterbird species vary in the dispersal functions they perform, and how seasonality influences endozoochory. In this study, we identified plant diaspores dispersed in faeces of five South American waterfowl (Brazilian teal Amazonetta brasiliensis, yellow‐billed teal Anas flavirostris, ringed teal Callonetta leucophrys, coscoroba swan Coscoroba coscoroba, and white‐faced whistling‐duck Dendrocygna viduata).
2. We collected 165 faecal samples from five wetlands in southern Brazil surrounded by pasture and rice fields, then separated and measured intact seeds and other diaspores. Using generalised linear models, we tested how diaspore abundance and taxonomic richness differed among bird species and between cold (April–September) and warm (October–March) periods. We also analysed bird‐specific and seasonal variations in diaspore composition through principal coordinates analysis and permutational multivariate analysis of variance. We used indicator species analysis to determine which diaspore species discriminated between bird species and seasons. Finally, we measured diaspore length in order to analyse differences among waterfowl species in the size of diaspores dispersed.
3. We found 2,066 intact diaspores from 40 different plant taxa, including seeds of 37 angiosperms and diaspores of Lycophyta (Isoetes cf. maxima), Pteridophyta (Azolla filiculoides), and Charophyceae. There was at least one diaspore in 65% of all faecal samples. Diaspores of native amphibious and emergent plants were dominant. We found 1,835 diaspores (from 33 taxa) in the cold period but only 231 (23 taxa) in the warm period. Seeds of the grass Zizaniopsis bonariensis and of the sedge Rynchospora sp. were the most abundant taxa. A strong interaction between bird species and season was the most important predictor of variation in both taxonomic richness and abundance of diaspores. The taxonomic composition of diaspores differed among waterfowl species and season. Indicator species analysis identified 12 plant taxa associated with particular bird species and seasons. Coscoroba swan, the largest bodied species in our study dispersed a higher proportion (8.2%) of large (length >2 mm) seeds.
4. Despite considerable overlap, there are important differences in the plants dispersed by each species, and the smallest (ringed teal) and largest (coscoroba swan) birds are particularly different. All five waterfowl species are distributed over wide areas of South America and here we demonstrated that they are likely to be important plant vectors connecting wetland species at different geographical scales. Many of these plants have previously been assumed to lack mechanisms for long‐distance dispersal.