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Internal dispersal of seeds by waterfowl: effect of seed size on gut passage time and germination patterns

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Abstract

Long distance dispersal may have important consequences for gene flow and community structure. The dispersal of many plants depends on transport by vertebrate seed dispersers. The shapes of seed shadows produced by vertebrates depend both on movement patterns of the dispersers and on the dynamics and effects of passage through the disperser’s gut (i.e. the retention time, survival and germination of ingested seeds). A combination of experiments with captive waterbirds and aquatic plant seeds was used to analyse the following: (a) the effects of inter- and intra-specific variation in seed size and duck species on seed retention time in the gut and (b) the relationship between retention time and the percent germination and germination rates of seeds. Among the three Scirpus species used, those with smaller seeds showed higher survival after ingestion by birds and longer retention times inside their guts than those with larger seeds. For Potamogeton pectinatus, only seeds from the smaller size class (<8 mg) survived ingestion. Retention time affected the percent germination and germination rate of Scirpus seeds but in a manner that varied for the different plant and bird species studied. We recorded both linear and non-linear effects of retention time on percent germination. In addition, germination rate was positively correlated with retention time in Scirpus litoralis but negatively correlated in Scirpus lacustris. Small seed size can favour dispersal over larger distances. However, the effects of retention time on percent germination can modify the seed shadows produced by birds due to higher percent germination of seeds retained for short or intermediate periods. The changes in dispersal quality associated with dispersal distance (which is expected to be positively related to retention time) will affect the probability of seedling establishment over longer distances and, thus, the spatial characteristics of the effective seed shadow.

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References

  • Allison PD (1995) Survival analysis using the SAS System. A practical guide. SAS Institute, Cary

    Google Scholar 

  • Barnea A, Yom-Tov Y, Friedman J (1991) Does ingestion by birds affect seed germination? Funct Ecol 5:394–402

    Article  Google Scholar 

  • Barnes GG, Thomas VG (1987) Digestive organ morphology, diet, and guild structure of North American Anatidae. Can J Zool 65:1812–1817

    Article  Google Scholar 

  • Brochet AL, Guillemain M, Fritz H, Gauthier-Clerc M, Green AJ (2009) The role of migratory ducks in the long-distance dispersal of native plants and the spread of exotic plants in Europe. Ecography 32:919–928

    Google Scholar 

  • Brochet AL, Guillemain M, Fritz H, Gauthier-Clerc M, Green AJ (2010) Plant dispersal by teal (Anas crecca) in the Camargue: duck guts are more important than their feet. Freshw Biol. doi:10.1111/j.1365-2427.2009.02350.x

    Google Scholar 

  • Campredon S, Campredon P, Pirot JY, Tamisier A (1982) Manuel d’analyse des contenus stomacaux de Canards et de Foulques. Centre d’Ecologie de Camargue, CNRS, Arles, France

    Google Scholar 

  • Charalambidou I, Santamaría L, Langevoord O (2003) Effect of ingestion by five avian dispersers on the retention time, retrieval and germination of Ruppia maritima seeds. Funct Ecol 17:747–753

    Article  Google Scholar 

  • Charalambidou I, Santamaría L, Jansen C, Nolet BA (2005) Digestive plasticity in Mallard ducks modulates dispersal probabilities of aquatic plants and crustaceans. Funct Ecol 19:513–519

    Article  Google Scholar 

  • Clausen P, Nolet BA, Fox AD, Klaasen M (2002) Long-distance endozoochorous dispersal of submerged macrophyte seeds by migratory waterbirds in Northern Europe—a sceptical review of possibilities. Acta Oecol 23:191–203

    Article  Google Scholar 

  • Clevering OA (1995) Germination and seedling emergence of Scirpus lacustris L. and Scirpus maritimus L. with special reference to the restoration of wetlands. Aquat Bot 50:63–78

    Article  Google Scholar 

  • De Vlaming V, Proctor VW (1968) Dispersal of aquatic organisms: viability of seeds recovered from the droppings of captive Killdeer and Mallard ducks. Am J Bot 55:20–26

    Article  Google Scholar 

  • Fenner M (1985) Seed ecology. Chapman & Hall, London

    Google Scholar 

  • Figuerola J, Green AJ, Santamaría L (2002) Comparative dispersal effectiveness of wigeongrass seeds by waterfowl wintering in south-west Spain: quantitative and qualitative aspects. J Ecol 90:989–1001

    Article  Google Scholar 

  • Gardener CJ, McIvor JG, Janzen A (1993) Passage of legume and grass seeds through the digestive tract of cattle and their survival in faeces. J Appl Ecol 30:63–74

    Article  Google Scholar 

  • Garland T, Adolph SC (1994) Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool 67:797–828

    Google Scholar 

  • Geritz SAH (1995) Evolutionary stable seed polymorphism and small-scale spatial variation in seedling density. Am Nat 146:685–707

    Article  Google Scholar 

  • Green AJ, Figuerola J, Sánchez M (2002) Implications of waterbird ecology for the dispersal of aquatic organisms. Acta Oecol 23:177–189

    Article  Google Scholar 

  • Guillemain M, Fritz H, Duncan P (2002) The importance of protected areas as nocturnal feeding grounds for dabbling ducks wintering in western France. Biol Conserv 103:183–198

    Article  Google Scholar 

  • Higgins SI, Nathan R, Cain ML (2003) Are long-distance dispersal events in plants usually caused by nonstandard means of dispersal? Ecology 84:1945–1956

    Article  Google Scholar 

  • Holbrook KM, Smith TB (2000) Seed dispersal and movement patterns in two species of Ceratogymna hornbills in a West African tropical lowland forest. Oecologia 125:249–257

    Article  Google Scholar 

  • Holt ML, van der Valk AG (2002) The potential role of ducks in wetland seed dispersal. Wetlands 22:170–178

    Article  Google Scholar 

  • Jakobsson A, Eriksson O (2000) A comparative study of seed number, seed size, seedling size and recruitment in grassland plants. Oikos 88:494–502

    Article  Google Scholar 

  • Jansen PA, Bartholomeus M, Bongers F, Elzinga JA, den Ouden J, van Wieren SE (2002) The role of seed size in dispersal by a scatter-hoarding rodent. In: Levey DJ, Silva WR, Galotti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford, pp 209–225

    Google Scholar 

  • Jordano P (2000) Fruits and frugivory. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CABI Publishing, New York, pp 125–166

    Chapter  Google Scholar 

  • Karasov WH (1990) Digestion in birds: chemical and physiological determinants and ecological implications. Stud Avian Biol 13:391–415

    Google Scholar 

  • Kehoe FP, Ankney CD (1985) Variation in digestive organ size among five species of diving ducks (Aythya spp.). Can J Zool 63:2339–2342

    Article  Google Scholar 

  • Liukkonen-Anttila T, Saartoala R, Hissa R (2000) Impact of hand-rearing on morphology and physiology of the capercaillie (Tetrao urogallus). Comp Biochem Physiol A 125:211–221

    CAS  Google Scholar 

  • Mathsoft (1999) S-Plus 2000 Guide to statistics, vol 2. Data Analysis Products Division Mathsoft, Seattle, WA

    Google Scholar 

  • Murphy SR, Reid N, Yan ZG, Venables WN (1993) Differential passage time of mistletoe fruits through the gut of honeyeaters and flowerpeckers. Effect on seedling establishment. Oecologia 93:171–176

    Article  Google Scholar 

  • Murray KG, Russell S, Picone CM, Winnett-Murray K, Sherwood W, Kuhlmann ML (1994) Fruit laxatives and seed passage rates in frugivores: consequences for plant reproductive success. Ecology 75:989–994

    Article  Google Scholar 

  • Nathan R, Schurr FM, Spiegel O, Steinitz O, Trakhtenbrot A, Tsoar A (2008) Mechanisms of long-distance seed dispersal. TREE 23:638–647

    PubMed  Google Scholar 

  • Piersma T, Koolhaas A, Dekinga A (1993) Interactions between stomach structure and diet choice in shorebirds. Auk 110:552–564

    Google Scholar 

  • Pollux BJA, Santamaria L, Ouborg NJ (2005) Differences in endozoochorous dispersal between aquatic plant species, with reference to plant population persistence in rivers. Freshw Biol 50:232–242

    Article  Google Scholar 

  • Pollux BJA, Verbruggen E, Van Groenendael JM, Ouborg NJ (2009) Intraspecific variation of seed floating ability in Sparganium emersum suggests a bimodal dispersal strategy. Aquat Bot 90:199–203

    Article  Google Scholar 

  • Santamaría L, Charalambidou I, Figuerola J, Green AJ (2002) Effect of passage through duck gut on germination of fennel pondweed seeds. Arch Hydrobiol 156:11–22

    Article  Google Scholar 

  • SAS Institute (2000) SAS/SAT ® software: user’s guide. SAS Institute, Cary, NC

    Google Scholar 

  • Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107(108):15–29

    Google Scholar 

  • Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506

    Article  Google Scholar 

  • Soons MB, van der Vlugt C, van Lith B, Heil GW, Klaassen M (2008) Small seed size increases the potential for dispersal of wetlands plants by ducks. J Ecol 96:619–627

    Article  Google Scholar 

  • Therneau TM, Grambsch PM (2000) Modeling survival data: extending the Cox model. Springer, New York

    Google Scholar 

  • Traveset A (1998) Effects of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect Plant Ecol 1/2B:151–190

    Article  Google Scholar 

  • Traveset A, Riera N, Mas RE (2001) Passage through bird guts causes interspecific differences in seed germination characteristics. Funct Ecol 15:669–675

    Article  Google Scholar 

  • Traveset A, Verdú M (2002) A meta-analysis of the effect of gut treatment on seed germination. In: Levey DJ, Silva WR, Galotti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford, pp 339–350

    Google Scholar 

  • Turnbull LA, Rees M, Crawley MJ (1999) Seed mass and the competition/colonization trade-off: a sowing experiment. J Ecol 87:899–912

    Article  Google Scholar 

  • Westcott DA, Graham DL (2000) Patterns of movement and seed dispersal of a tropical frugivore. Oecologia 122:249–257

    Article  Google Scholar 

  • Westoby M, Jurado E, Leishman M (1992) Comparative evolutionary ecology of seed size. Trends Ecol Evol 7:368–372

    Article  Google Scholar 

  • Westoby M, Leishman M, Lord J (1996) Comparative ecology of seed size and dispersal. Philos Trans R Soc Lond B 351:1309–1318

    Article  Google Scholar 

  • Winn AA (1985) Effects of seed size and germination site on seedling emergence of Prunella vulgaris in four habitats. J Ecol 73:831–840

    Article  Google Scholar 

  • Wongsriphuek C, Dugger BD, Bartuszevige AM (2008) Dispersal of wetland plant seeds by mallards: influence of gut passage on recovery, retention, and germination. Wetlands 28:290–299

    Article  Google Scholar 

  • Wulff RD (1986) Seed size variation in Desmodium paniculatum. II. Effects on seedling growth and physiological performance. J Ecol 74:99–114

    Article  Google Scholar 

Download references

Acknowledgments

Doñana National Park allowed us to use their installations. We are grateful to Pablo Pereira, Begoña Gutíerrez, Cristina Belén Sánchez and Celia Sánchez for their help during the setup of the experiments. Pedro Jordano and two anonymous referees provided valuable comments on an earlier version of the manuscript. Our research was supported by the European Union project “LAKES—Long distance dispersal of Aquatic Key Species” (ENV4-CT97-0585), by the Spanish Ministry of Science and Technology (project BOS2000-1368), and ESF project BIOPOOL (project CGL2006-27125-E/BOS from the Spanish Ministry of Education and Science).

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Author notes

  1. Iris Charalambidou

    Present address: Unit of Environmental Studies, CCEIA, University of Nicosia (Intercollege), 46 Makedonitissas Avenue, Nicosia, 1700, Cyprus

  2. Luis Santamaria

    Present address: IMEDEA, CSIC-UIB, c/Miquel Marquès 21, E-07190, Esporles, Mallorca, Spain

Authors and Affiliations

  1. Department of Wetland Ecology, Estación Biológica de Doñana, CSIC, Apartado de Correos 1056, E-41080, Sevilla, Spain

    Jordi Figuerola & Andy J. Green

  2. Netherlands Institute of Ecology-KNAW, P.O. Box 1299, 3600 BG, Maarssen, The Netherlands

    Iris Charalambidou & Luis Santamaria

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  1. Jordi Figuerola
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  2. Iris Charalambidou
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Correspondence to Jordi Figuerola.

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Figuerola, J., Charalambidou, I., Santamaria, L. et al. Internal dispersal of seeds by waterfowl: effect of seed size on gut passage time and germination patterns. Naturwissenschaften 97, 555–565 (2010). https://doi.org/10.1007/s00114-010-0671-1

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