Aim Patterns of high biodiversity among less mobile organisms throughout isolated locations suggest that passive dispersal importantly contributes to biodiversity. We examined the contribution of waterbirds to the dispersal of plant seeds and macroinvertebrates between aquatic wetlands. Birds are renowned vectors for seeds of terrestrial plants, but less is known about their role in more dispersal-dependent aquatic systems. We therefore performed a meta-analysis on bird-mediated endozoochorous dispersal of aquatic species.Location Our review included studies that collected data world-wide.Methods We analysed data from 81 peer-reviewed publications on endozoochorous dispersal of aquatic plant seeds and macroinvertebrates by waterbirds. ResultsIn total, 36% of 1581 waterbird droppings collected in the field contained one or more intact propagules, with macroinvertebrates found almost as frequently as plant seeds. Positive droppings contained on average 3.3 intact propagules, of which one-third were viable. In 728 trials from 17 published feeding experiments 24% of the ingested propagules were retrieved intact, with c. 6.5% both viable and intact. As many as 17 species of Anatidae and Rallidae were involved in the dispersal of at least 39 species of macroinvertebrates and seeds from 97 species of plants across a wide taxonomic range. Smaller propagules seemed less affected by digestion than larger ones. We provide a first quantitative model that can be used to estimate waterbird-mediated dispersal of propagules between wetlands. This model indicates that an average waterbird has the potential to disperse five viable propagules after flying more than 100 km, and one additional propagule after flying 300 km. Main conclusionsWe demonstrate that waterbirds have the potential to transport a wide variety of aquatic plants and animals over several hundreds of kilometres. High survival of propagules might be explained by propagule adaptations or by the digestive adaptations of birds, whereby energy absorption is thought to be maximized rather than assimilation efficiency. Our meta-analysis suggests that waterbirds might contribute significantly to wetland biodiversity around the world, despite several limitations to our current knowledge. We outline avenues for future research to address these knowledge gaps. KeywordsAnatidae, aquatic propagules, digestive physiology, long-distance dispersal, macroinvertebrates, plant seeds, Rallidae.2006). Species distributions often range across geographical barriers, such as deserts and oceans (Schabetsberger et al., 2009;Jocque et al., 2010), suggesting high species mobility in the landscape (Lester et al., 2007). However, for many species it is still unknown how, and how often, they disperse ª 2012 Blackwell Publishing Ltd

SUMMARY1. How species reach and persist in isolated habitats remains an open question in many cases, especially for rapidly spreading invasive species. This is particularly true for temporary freshwater ponds, which can be remote and may dry out annually, but may still harbour high biodiversity. Persistence in such habitats depends on recurrent colonisation or species survival capacity, and ponds therefore provide an ideal system to investigate dispersal and connectivity. 2. Here, we test the hypothesis that the wide distributions and invasive potential of aquatic snails is due to their ability to exploit several dispersal vectors in different landscapes. We explored the population structure of Physa acuta (recent synonyms: Haitia acuta, Physella acuta, Pulmonata: Gastropoda), an invasive aquatic snail originating from North America, but established in temporary ponds in Doñ ana National Park, southern Spain. In this area, snails face land barriers when attempting to colonise other suitable habitat. 3. Genetic analyses using six microsatellite loci from 271 snails in 21 sites indicated that (i) geographically and hydrologically isolated snail populations in the park were genetically similar to a large snail population in rice fields more than 15 km away; (ii) these isolated ponds showed an isolation-by-distance pattern. This pattern broke down, however, for those ponds visited frequently by large mammals such as cattle, deer and wild boar; (iii) snail populations were panmictic in flooded and hydrologically connected rice fields. 4. These results support the notion that aquatic snails disperse readily by direct water connections in the flooded rice fields, can be carried by waterbirds flying between the rice fields and the park and may disperse between ponds within the park by attaching to large mammals. 5. The potential for aquatic snails such as Physa acuta to exploit several dispersal vectors may contribute to their wide distribution on various continents and their success as invasive species. We suggest that the interaction between different dispersal vectors, their relation to specific habitats and consequences at different geographic scales should be considered both when attempting to control invasive freshwater species and when protecting endangered species.

Many plant seeds and invertebrates can survive passage through the digestive system of birds, which may lead to long distance dispersal (endozoochory) in case of prolonged retention by moving vectors. Endozoochorous dispersal by waterbirds has nowadays been documented for many aquatic plant seeds, algae and dormant life stages of aquatic invertebrates. Anecdotal information indicates that endozoochory is also possible for fully functional, active aquatic organisms, a phenomenon that we here address experimentally using aquatic snails. We fed four species of aquatic snails to mallards (Anas platyrhynchos), and monitored snail retrieval and survival over time. One of the snail species tested was found to survive passage through the digestive tract of mallards as fully functional adults. Hydrobia (Peringia) ulvae survived up to five hours in the digestive tract. This suggests a maximum potential transport distance of up to 300 km may be possible if these snails are taken by flying birds, although the actual dispersal distance greatly depends on additional factors such as the behavior of the vectors. We put forward that more organisms that acquired traits for survival in stochastic environments such as wetlands, but not specifically adapted for endozoochory, may be sufficiently equipped to successfully pass a bird's digestive system. This may be explained by a digestive trade-off in birds, which maximize their net energy intake rate rather than digestive efficiency, since higher efficiency comes with the cost of prolonged retention times and hence reduces food intake. The resulting lower digestive efficiency allows species like aquatic snails, and potentially other fully functional organisms without obvious dispersal adaptations, to be transported internally. Adopting this view, endozoochorous dispersal may be more common than up to now thought.