Aims: Research into the dispersal of plants lacking a fleshy fruit by avian endozoochory remains limited, particularly regarding the different roles of specific vectors in the same habitat. Methods: We compared plants dispersed by endozoochory between two migratory waterbirds differing in body size: the lesser black-backed gull Larus fuscus, and the white stork Ciconia ciconia. We collected faeces and pellets from roosting flocks on dykes in rice fields in Doñana, SW Spain, and extracted intact seeds. Results: We recovered 424 intact seeds from excreta, representing 21 plant taxa, 11 of which germinated under laboratory conditions. Eight plant species are considered weeds, four of them as alien species, and only two have a fleshy fruit. Seed abundance and species richness per sample did not differ between storks and gulls. Toadrush (Juncus bufonius) was the dominant species, accounting for 49% of seeds recovered. PERMANOVA and mvabund analyses revealed no differences in the proportions of each plant species dispersed by the two vectors, and seasonal variation in abundance was absent. Overall, germinability was 19%, and declined with increasing delay between sample collection and processing. Transects along dykes identified 52 plant taxa, only 18 of which were recorded in excreta. Conclusions: Overlap in the communities of non-fleshy-fruited plants dispersed by two unrelated birds of different size suggests that waterbird plant dispersal networks are different from frugivore networks. Unlike for frugivores, decoupling between seed production and ingestion reduces seasonal variation in endozoochory rates. For Juncus bufonius and other plants, these avian vectors provide maximum dispersal distances several orders of magnitude greater than predicted from their dispersal syndromes. Endozoochory by migratory waterbirds has major implications for plant distributions in a rapidly changing world, and more research is required before we can predict which plants disperse regularly via this mechanism.
1. Non-frugivorous waterbirds disperse a wide variety of plants by endozoochory, providing longer-dispersal distances than other mechanisms. Many waterbirds visit both agricultural and natural landscapes during their daily movements, but potential bird-mediated dispersal of weed plants within and from agricultural landscapes to other habitats is commonly overlooked. Gulls (Laridae) are expanding in numbers and increasingly exploiting anthropogenic habitats worldwide, with possible growing implications for the spread of weeds. Yet, to date, there are no studies on the spatial distribution of weed dispersal by waterbirds. 2. We developed a plant dispersal model based on movements of 19 Larus fuscus using ricefields, via GPS telemetry. We combined daily movements with two curves estimating the retention times of plant seeds in their guts: (a) an experimental curve based on retention time in captivity for four weeds with dry fruits known to be dispersed by gulls: Juncus bufonius, Cyperus difformis, Polypogon monspeliensis and the alien Amaranthus retroflexus; (b) a theoretical curve based on the interspecific scaling relationship between body mass and mean retention time. 3. Median dispersal distances of weed plant seeds by gulls ranged between 690 and 940 m, but maximum distances exceeded 150 km. The theoretical retention time model showed higher median dispersal distances than the experimental retention time model. Spatial patterns of weed deposition were very similar between retention time methods, and most strongly depended on gull movements. Variation between individual gulls had little influence on seed shadows. About 92% of all seeds (>10,000 intact seeds per day) were dispersed within the ricefield area of 370 km 2. The remaining 8% of seeds were deposited beyond ricefields into other habitats, 42% of which reached moist environments (other irrigated agriculture, rivers and natural wetlands) presumably suitable for weed establishment.
Eutrophication of aquatic ecosystems is a global problem with major ecological and economic impacts. In many lakes and reservoirs, guanotrophication occurs when roosting waterbirds import nutrients (nitrogen and phosphorus) from surrounding terrestrial habitats. To date, nutrient loading by waterbirds has been estimated based on censuses in the absence of detailed information on their movements. We quantified nutrient importation by the lesser black‐backed gull (Larus fuscus) to Fuente de Piedra (1,350 ha) in Andalusia (south‐west Spain), where an average of 36,288 individuals are counted in January. During seven winters from 2010 to 2017, we used movement data from 20 individual gulls tagged with Global Positioning System trackers that foraged in four landfills. Together with monthly bird counts and measurements of total N and P content in faeces and pellet samples, movement data were used to quantify the total external loading effect for different winters. Movement data allowed us to quantify the proportion of time spent in the lake and the time spent at different foraging sites and enabled correction of censuses. According to tracking data, on average 69% of the birds had already left the lake to head for feeding sites when waterbird counts were carried out. Nutrient inputs to the lake depend partly on the proportion of the day that gulls spend there, which was higher in late winters and was reduced when lake depth went below or above 20–35 cm. An estimated average of 10.17 kg N ha−1 year−1 and 2.07 kg P ha−1 year−1 were imported to this closed‐basin lake by gulls each winter, with highest values recorded in winter 2016–2017. Gull guano is the most important winter source of nutrients to the lake. Regurgitated pellets have been ignored as a source of nutrients in other guanotrophy studies, but we found them to be a more important source of P than faeces. A movement ecology approach complements traditional censuses and facilitates the study of guanotrophication in multiple ways, including identification of sources of nutrients, correction of censuses, and measuring time spent at roost sites.
Waterbirds can transport aquatic invertebrates internally, contributing to metapopulation dynamics between aquatic habitats in a terrestrial matrix. However, research into this dispersal process to date has focused on individual field sites or laboratory studies. We investigated the invertebrates dispersed by endozoochory by the lesser black-backed gull Larus fuscus wintering in Andalusia, south-west Spain in 2016–2017, comparing seven sites interconnected by their movements, with different degrees of anthropogenization [three landfills, two saltpan complexes, a natural lake, and a large (370 km2) ricefield area]. In the ricefields, we also compared invertebrates dispersed by gulls with those dispersed by the larger white stork Ciconia ciconia. A total of 642 intact invertebrates and their propagules (mainly plumatellid bryozoans, cladocerans, and other branchiopods) were recorded in excreta (faeces and pellets) from gulls and storks. A greater diversity and abundance of invertebrates were recorded in ricefields, notably 43 individuals of the alien snail Physella acuta. One snail was still alive in a gull pellet 3 weeks after being stored in a fridge. This represents the first record of snail dispersal within waterbird pellets. Viability was also confirmed for the cladoceran Macrothrix rosea recorded in ricefields, and the alien brine shrimp Artemia franciscana recorded mainly in saltpans. In ricefields, gulls and pellets had significantly fewer propagules and fewer taxa per gram of excreta than storks and faeces, respectively. Through their high mobility, gulls and storks can disperse invertebrates between different natural and artificial habitats, and even to landfills. They can promote metapopulation dynamics for native bryozoans and branchiopods, but also the spread of invasive snails and brine shrimp.
AimHow plants can disperse in response to global change is a critical question, yet major knowledge gaps persist about long‐distance dispersal (LDD) mechanisms. We studied the potential a migratory waterfowl has for LDD of flowering plants via gut passage of seeds (endozoochory), comparing spring and autumn migration.LocationUnited Kingdom and Iceland.TaxonPink‐footed Goose (Anser brachyrhynchus, Baillon) and Angiosperma.MethodsWe studied endozoochory by Pink‐footed geese migrating within and between the UK and Iceland by faecal sampling and GPS tracking. We collected 614 faecal samples from 14 areas in the UK and one in Iceland. Using GPS tracks to and from these areas, we estimated how far seeds can be dispersed by Pink‐footed geese, and where to or from.ResultsWe recorded 5507 intact seeds of 35 species (27 terrestrial) from 15 plant families, with lower seed abundance per dropping when birds were migrating northwards in the UK during spring than upon their arrival in autumn. Species richness of plant seeds was highest in Iceland and in autumn. Only four plant species dispersed had an “endozoochory syndrome”. GPS movements showed that seeds retained in guts for up to 24 h can be readily dispersed in both directions between the UK and Iceland, with maximum distances exceeding 2000 km, as well as between UK localities separated by 100 s of km. Movements northwards of ≤400 km were even recorded in autumn. While at stopover sites, daily movements between roost and feeding sites often exceed 20 km.Main ConclusionsPink‐footed geese are LDD vectors for plants previously assumed to lack an LDD mechanism. Spring migration is not the only period when geese move plants to cooler latitudes. The pink‐footed goose can allow terrestrial and aquatic plants to cross the ocean and to keep pace with climate change.
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