Gut travellers: internal dispersal of aquatic organisms by waterfowl
Casper H.A. van Leeuwen, Gerard van der Velde, Jan M. van Groenendael and Marcel Klaassen
Journal of Biogeography
Appendix S2 Explanation of the calculations for the quantitative dispersal model.
The collected data allowed us to calculate a first quantitative estimate of the average number of propagules dispersed by waterbirds over distance. We combined the average number of propagules per dropping, their viability, bird dropping rates, the flight speed of waterfowl, and retention times of ingested propagules. Thirty-eight per cent of the droppings were found positive, with an average of 3.32 propagules per positive dropping. Dropping rates ranged between 6.5 and 9.7 droppings per hour for herbivorous vector species . For carnivores this is generally lower, i.e. 2.4 to 3.1 droppings per hour . We modelled dropping rates from the full range of 2.4 to 9.7 droppings per hour, considering it to vary between these values due to differences between species, bird feeding guild, and factors like the diet of an individual bird at a certain moment. Propagule release decreased exponentially over time based on the six feeding experiment studies that reported detailed propagule release over time intervals of 4 hours up to now . We fitted an exponentially declining function to the data retrieved from these six publications (for equation see Fig. 3). This exponential decline (68% after 4h, 85% after 8h, and 92% after 12h) was further supported by an experiment monitoring nightingales (Luscinia megarhynchos) flying in a wind tunnel, of which dropping rates were measured continuously and decreased exponentially to 25% of its initial rate after 8 hours (M. Klaassen, A. Kvist, Å. Lindström, unpublished data).
Viability of aquatic propagules has also been shown to decrease exponentially with increasing retention time , with an average regression coefficient of 0.0688 + 0.0243 (limited to n=4, but consistent over studies). Viability of propagules collected in the field was on average 33.6%. Since 92% of the propagules would have been excreted in the first 12 hours according to feeding experiments, we fitted an exponential declining function with a regression coefficient of 0.0688 and an average of 33.6% over the first 12 hours as the declining viability curve (for equation see Fig. 3). We deliberately did not include possible positive effects of gut passage, such as enhanced germination , because this is a variable phenomenon with both intra- and interspecific differences still hardly understood .
The average flight speed of waterfowl is ~75 km h-1, but is known to vary with flight conditions and species from as low as 42 km h-1 up to 116 km h-1 . Using this flight speed data and our model depicted in figure 3, we can now calculate quantitative dispersal for any hypothetical bird. For example, an average bird flying at 75 km h-1 will produce 6.1 droppings per hour, and would thus excrete 3 viable propagules during the first hour of flying (visualized in Fig. 3). These will be excreted between the point of ingestion and the location of the birds’ destination, at a maximum possible distance of 75 km from the origin. Assuming the bird continues its flight without foraging or resting, dropping rate and propagule viability will continue to decrease exponentially over time, but the bird will still release cumulatively 4.1 propagules over the next 3 hours (i.e. 2.0 + 1.2 + 0.9 = 4.1 propagules). After 4 hours (if spent in flight at a maximum of 4*75km = 300 kilometre from the propagules’ origin), it will continue to release propagules at the hourly rates indicated in Fig. 3. Each bird departing after a foraging baud and flying at average speed should thus transport at least one propagule over the first 300 kilometres. Similarly, we can estimate propagule transport over distance for any bird species, if we know its behaviour over time including flight speed and direction.
Brochet, A.-L., Guillemain, M., Gauthier-Clerc, M., Fritz, H. & Green, A.J. (2010) Endozoochory of Mediterranean aquatic plant seeds by teal after a period of desiccation: determinants of seed survival and influence of retention time on germinability and viability. Aquatic Botany, 93, 99-106.
Bruderer, B. & Boldt, A. (2001) Flight characteristics of birds: I. radar measurements of speeds. Ibis, 143, 178-204.
Bruinzeel, L.W., Van Eerden, M.R., Drent, R.H. & Vulink, T. (1997) Scaling metabolisable energy intake and daily energy expenditure in relation to the size of herbivorous waterfowl: limits set by available foraging time and digestive performance. Patchwork. Patch use, habitat exploitation and carrying capacity for waterbirds in Dutch freshwater wetlands (ed. M.R. Van Eerden), pp. 111-132. Van Zee tot Land, Vol. 63. Ministerie van Verkeer en Waterstaat Directoraat-Generaal Rijkswaterstaat Directie IJsselmeergebied, Lelystad
Charalambidou, I., Ketelaars, H.A.M. & Santamaría, L. (2003a) Endozoochory by ducks: influence of developmental stage of Bythotrephes diapause eggs on dispersal probability. Diversity and Distributions, 9, 367-374.
Charalambidou, I., Santamaría, L. & Figuerola, J. (2003b) How far can the freshwater bryozoan Cristatella mucedo disperse in duck guts? Archiv für Hydrobiologie, 157, 547-554.
Charalambidou, I., Santamaría, L. & Langevoord, O. (2003c) Effect of ingestion by five avian dispersers on the retention time, retrieval and germination of Ruppia maritima seeds. Functional Ecology, 17, 747-753.
Charalambidou, I., Santamaría, L., Jansen, C. & Nolet, B.A. (2005) Digestive plasticity in mallard ducks modulates dispersal probabilities of aquatic plants and crustaceans. Functional Ecology, 19, 513-519.
Clausen, P., Nolet, B.A., Fox, A.D. & Klaassen, M. (2002) Long-distance endozoochorous dispersal of submerged macrophyte seeds by migratory waterbirds in northern Europe - a critical review of possibilities and limitations. Acta Oecologica – International Journal of Ecology, 23, 191-203.
Espinar, J.L., Garcia, L.V., Figuerola, J., Green, A.J. & Clemente, L. (2004) Helophyte germination in a Mediterranean salt marsh: gut-passage by ducks changes seed response to salinity. Journal of Vegetation Science, 15, 315-322.
Figuerola, J., Charalambidou, I., Santamaría, L. & Green, A.J. (2010) Internal dispersal of seeds by waterfowl: effect of seed size on gut passage time and germination patterns. Naturwissenschaften, 97, 555-565.
Hahn, S., Bauer, S. & Klaassen, M. (2007) Estimating the contribution of carnivorous waterbirds to nutrient loading in freshwater habitats. Freshwater Biology, 52, 2421-2433.
Hahn, S., Bauer, S. & Klaassen, M. (2008) Quantification of allochthonous nutrient input into freshwater bodies by herbivorous waterbirds. Freshwater Biology, 53, 181-193.
Miller, M.R., Takekawa, J.Y., Fleskes, J.R., Orthmeyer, D.L., Casazza, M.L., Haukos, D.A. & Perry, W.M. (2005) Flight speeds of Northern Pintails during migration determined using satellite telemetry. Wilson Bulletin, 117, 364-374.
Pollux, B.J.A., Santamaría, L. & Ouborg, N.J. (2005) Differences in endozoochorous dispersal between aquatic plant species, with reference to plant population persistence in rivers. Freshwater Biology, 50, 232-242.
Santamaría, L., Charalambidou, I., Figuerola, J. & Green, A.J. (2002) Effect of passage through duck gut on germination of fennel pondweed seeds. Archiv für Hydrobiologie, 156, 11-22.
Traveset, A. (1998) Effect of seed passage through vertebrate frugivores' guts on germination: a review. Perspectives in Plant Ecology Evolution and Systematics, 1, 151-190.
Traveset, A., Rodriguez-Perez, J. & Pias, B. (2008) Seed trait changes in dispersers' guts and consequences for germination and seedling growth. Ecology, 89, 95-106.
Welham, C.V.J. (1994) Flight speeds of migrating birds – a test of maximum range speed predictions from 3 aerodynamic equations. Behavioral Ecology, 5, 1-8.
Wongsriphuek, C., Dugger, B.D. & Bartuszevige, A.M. (2008) Dispersal of wetland plant seeds by mallards: influence of gut passage on recovery, retention, and germination. Wetlands, 28, 290-299.