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Effects of great bustard (Otis tarda) gut passage on black nightshade (Solanumnigrum) seed germination

Published online by Cambridge University Press:  22 May 2014

C. Bravo*
Affiliation:
Department of Evolutionary Ecology, Museo Nacional de Ciencias Naturales-CSIC, C/José Gutiérrez Abascal, 2. 28006Madrid, Spain
S. Velilla
Affiliation:
Department of Ecology, Universidad Autónoma de Madrid, C/Darwin, Ciudad Universitaria Cantoblanco, 28049Madrid, Spain
L.M. Bautista
Affiliation:
Department of Evolutionary Ecology, Museo Nacional de Ciencias Naturales-CSIC, C/José Gutiérrez Abascal, 2. 28006Madrid, Spain
B. Peco
Affiliation:
Department of Ecology, Universidad Autónoma de Madrid, C/Darwin, Ciudad Universitaria Cantoblanco, 28049Madrid, Spain
*
*Correspondence E-mail: [email protected]

Abstract

Birds are important seed dispersers for fleshy fruits through their transportation of ingested seeds. The seeds of many species germinate faster and in greater proportions after passing through a digestive tract, although the effects of this passage vary amongst bird and plant species. Many factors determine the germination success of ingested seeds, such as seed scarification during the digestion process, the fertilizing effect of droppings and the removal of pulp surrounding the seeds. In central Spain, the great bustard (Otis tarda) may act as a disperser of European black nightshade (Solanum nigrum). We analysed the germination success of ingested and non-ingested S. nigrum seeds. The fertilizing effect of bustard droppings and the disinhibition effect of the removal of Solanum pulp on final germination percentage, germination speed and viability were also assessed. Although ingested seeds germinated faster than non-ingested seeds, the former showed a lower germination percentage than the latter: 80–87% versus 99%. Droppings and fruit pulp showed no effect on germination enhancement, except in one aspect: the germination speed of non-ingested seeds decreased when they were sprayed with a fruit extract. We confirm that seeds ingested by great bustards had lower germination success than non-ingested seeds. Although seed ingestion by great bustards reduced seedling emergence, the number of emerged seedlings was still quite large. Thus, great bustards may play a role as a S. nigrum seed dispersal vector.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2014 

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References

AEMET (2014) Agencia Estatal de Meteorología. Available at http://www.aemet.es/es/serviciosclimaticos/datosclimatologicos/ (accessed June 2013).Google Scholar
Afik, D. and Karasov, W.H. (1995) The trade-offs between digestion rate and efficiency in warblers and their ecological implications. Ecology 76, 22472257.Google Scholar
Alonso, J.C., Magaña, M., Alonso, J.A., Palacín, C., Martín, C.A. and Martín, B. (2009) The most extreme sexual size dimorphism among birds: allometry, selection, and early juvenile development in the great bustard (Otis tarda). The Auk 126, 657665.Google Scholar
Bailey, T.A., Mensah-Brown, E.P., Samour, J.H., Naldo, J., Lawrence, P. and Garner, A. (1997) Comparative morphology of the alimentary tract and its glandular derivatives of captive bustards. Journal of Anatomy 191, 387398.Google Scholar
Barnea, A., Yomtov, Y. and Friedman, J. (1990) Differential germination of two closely related species of Solanum in response to bird ingestion. Oikos 57, 222228.Google Scholar
Barnea, A., Yomtov, Y. and Friedman, J. (1991) Does ingestion by birds affect seed-germination? Functional Ecology 5, 394402.Google Scholar
Baskin, C.C. and Baskin, J.M. (2001) Seeds. San Diego, USA, Academic Press.Google Scholar
Bautista, L.M., Silván, G., Cáceres, S., Martínez-Fernández, L., Bravo, C., Illera, J.C., Alonso, J.C. and Blanco, G. (2013) Faecal sexual steroids in sex typing and endocrine status of great bustards. European Journal of Wildlife Research 59, 815822.Google Scholar
Benvenuti, S. (2007) Weed seed movement and dispersal strategies in the agricultural environment. Weed Biology and Management 7, 141157.Google Scholar
Bravo, C., Ponce, C., Palacín, C. and Carlos Alonso, J. (2012) Diet of young Great Bustards Otis tarda in Spain: sexual and seasonal differences. Bird Study 59, 243251.Google Scholar
Carmona, C.P., Azcárate, F.M. and Peco, B. (2013) Does cattle dung cause differences between grazing increaser and decreaser germination response? Acta Oecologica-International Journal of Ecology 47, 17.Google Scholar
Chang, E.R., Zozaya, E.L., Kuijper, D.P.J. and Bakker, J.P. (2005) Seed dispersal by small herbivores and tidal water: are they important filters in the assembly of salt-marsh communities? Functional Ecology 19, 665673.CrossRefGoogle Scholar
Charalambidou, I., Santamaria, L. and Langevoord, O. (2003) Effect of ingestion by five avian dispersers on the retention time, retrieval and germination of Ruppia maritima seeds. Functional Ecology 17, 747753.Google Scholar
Cipollini, M.L. and Levey, D.J. (1997) Secondary metabolites of fleshy vertebrate-dispersed fruits: Adaptive hypotheses and implications for seed dispersal. American Naturalist 150, 346372.Google Scholar
Clergeau, P. (1992) The effect of birds on seed-germination of fleshy-fruited plants in temperate farmland. Acta Oecologica-International Journal of Ecology 13, 679686.Google Scholar
DeGolier, T.F., Mahoney, S.A. and Duke, G.E. (1999) Relationships of avian cecal lengths to food habits, taxonomic position, and intestinal lengths. Condor 101, 622634.Google Scholar
Delibes, M., Corbacho, C., Calvo, G. and Fedriani, J.M. (2012) Agriculture as matchmaker of an unexpected mutualism: Great bustard disperses and enhances emergence of domestic olive seeds. Basic and Applied Ecology 13, 125131.Google Scholar
Dinerstein, E. and Wemmer, C.M. (1988) Fruits rhinoceros eat – dispersal of Trewia nudiflora (Euphorbiaceae) in lowland Nepal. Ecology 69, 17681774.Google Scholar
Estrada, A. and Fleming, T.H. (1986) Frugivores and seed dispersal. Dordrecht, Dr W. Junk Publishers.Google Scholar
Figuerola, J., Charalambidou, I., Santamaria, L. and Green, A.J. (2010) Internal dispersal of seeds by waterfowl: effect of seed size on gut passage time and germination patterns. Naturwissenschaften 97, 555565.CrossRefGoogle ScholarPubMed
Herrera, C.M. (2002) Seed dispersal by vertebrates. pp. 185208 in Herrera, C.M.; Pellmyr, O. (Eds) Plant–animal interactions: An evolutionary approach. New York, Blackwell.Google Scholar
Hoekstra, N.J., Bosker, T. and Lantinga, E.A. (2002) Effects of cattle dung from farms with different feeding strategies on germination and initial root growth of cress (Lepidium sativum L.). Agriculture Ecosystems & Environment 93, 189196.Google Scholar
Howe, H.F. and Smallwood, J. (1982) Ecology of seed dispersal. Annual Review of Ecology and Systematics 13, 201228.Google Scholar
Jackson, S. (1992) Do seabird gut sizes and mean retention times reflect adaptation to diet and foraging method? Physiological Zoology 65, 674697.Google Scholar
Jordano, P. and Schupp, E.W. (2000) Seed disperser effectiveness: The quantity component and patterns of seed rain for Prunus mahaleb . Ecological Monographs 70, 591615.Google Scholar
Karasov, W.H. (1990) Digestion in birds: chemical and physiological determinants and ecological implications. pp. 391415 in Morrison, M.L.; Ralpa, C.J.; Verner, J.; Jehl, J.J.R. (Eds) Avian foraging theory, methodology and applications: Studies in avian biology. San Diego, California, USA, Cooper Ornithological Society Publishing.Google Scholar
Lane, S.J., Alonso, J.C., Alonso, J.A. and Naveso, M.A. (1999) Seasonal changes in diet and diet selection of great bustards (Otis tarda) in north-west Spain. Journal of Zoology 247, 201214.Google Scholar
Lucio, A.J. (1985) Datos sobre la alimentación de la avutarda (Otis tarda L. 1758) en la Cuenca del Duero. Alytes 3, 6986.Google Scholar
Luna, B. and Moreno, J.M. (2009) Light and nitrate effects on seed germination of Mediterranean plant species of several functional groups. Plant Ecology 203, 123135.Google Scholar
Mas, R.E. and Traveset, A. (1999) Efectes de la ingestió per ocells sobre la germinació i la dispersió de dues espècies próximes de Solanum . Bolletí de la Societat d'Història Natural de les Balears 42, 6977.Google Scholar
Mayer, A.M. and Poljakoff-Mayber, A. (1989) The germination of seeds. New York, Pergamon Press.Google Scholar
Meyer, G.A. and Witmer, M.C. (1998) Influence of seed processing by frugivorous birds on germination success of three North American shrubs. American Midland Naturalist 140, 129139.Google Scholar
Minderman, J., Reid, J.M., Hughes, M., Denny, M.J.H., Hogg, S., Evans, P.G.H. and Whittingham, M.J. (2010) Novel environment exploration and home range size in starlings Sturnus vulgaris . Behavioral Ecology 21, 13211329.Google Scholar
Palacín, C., Alonso, J.C., Alonso, J.A., Martín, C.A., Magaña, M. and Martín, B. (2009) Differential migration by sex in the Great Bustard: Possible consequences of an extreme sexual size dimorphism. Ethology 115, 617626.Google Scholar
Rey, P.J. and Alcántara, J.M. (2014) Effects of habitat alteration on the effectiveness of plant-avian seed dispersal mutualisms: consequences for plant regeneration. Perspectives in Plant Ecology Evolution and Systematics 16, 2131.Google Scholar
Robertson, A.W., Trass, A., Ladley, J.J. and Kelly, D. (2006) Assessing the benefits of frugivory for seed germination: the importance of the disinhibition effect. Functional Ecology 20, 5866.Google Scholar
Rodríguez-Pérez, J., Riera, N. and Traveset, A. (2005) Effect of seed passage through birds and lizards on emergence rate of Mediterranean species: differences between natural and controlled conditions. Functional Ecology 19, 699706.Google Scholar
Samuels, I.A. and Levey, D.J. (2005) Effects of gut passage on seed germination: do experiments answer the questions they ask? Functional Ecology 19, 365368.Google Scholar
Schupp, E.W. (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Advances in Vegetation Science 15, 1529.CrossRefGoogle Scholar
Schupp, E.W., Jordano, P. and Maria Gomez, J. (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188, 333353.Google Scholar
Spiegel, O. and Nathan, R. (2007) Incorporating dispersal distance into the disperser effectiveness framework: frugivorous birds provide complementary dispersal to plants in a patchy environment. Ecology Letters 10, 718728.Google Scholar
Taab, A. and Andersson, L. (2009) Seed dormancy dynamics and germination characteristics of Solanum nigrum . Weed Research 49, 490498.Google Scholar
Tobler, M. and Smith, H.G. (2004) Specific floater home ranges and prospective behaviour in the European starling, Sturnus vulgaris . Naturwissenschaften 91, 8589.Google Scholar
Torres, M. and Frutos, G. (1989) Analysis of germination curves of aged fennel seeds by mathematical models. Environmental and Experimental Botany 29, 409415.Google Scholar
Torres, M. and Frutos, G. (1990) Logistic function-analysis of germination behavior of aged fennel seeds. Environmental and Experimental Botany 30, 383390.Google Scholar
Traveset, A. (1998) Effect of seed passage through vertebrate frugivores' guts on germination: a review. Perspectives in Plant Ecology Evolution and Systematics 1, 151190.CrossRefGoogle Scholar
Traveset, A. and Verdú, M. (2002) A meta-analysis of the effect of gut treatment on seed germination in Levey, D.J.; Silva, W.R.; Galetti, M. (Eds) Seed dispersal and frugivory: ecology, evolution and conservation. New York, CAB International.Google Scholar
Traveset, A., Riera, N. and Mas, R.E. (2001) Passage through bird guts causes interspecific differences in seed germination characteristics. Functional Ecology 15, 669675.Google Scholar
Traveset, A., Robertson, A.W. and Rodríguez-Pérez, J. (2007) A review on the role of endozoochory in seed germination. pp. 78103 in Dennis, A.J.; Schupp, E.W.; Green, R.J.; Westcott, D.A. (Eds) Seed dispersal: theory and its application in a changing world. Wallingford, UK, CAB International.Google Scholar
Willson, M.F. and Traveset, A. (2000) The ecology of seed dispersal. pp. 85110 in Fenner, M. (Ed.) Seeds: the ecology of regeneration in plant communities. New York, CAB International.Google Scholar
Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A. and Smith, G.M. (2009) Mixed effects models and extensions in ecology with R. New York, Springer.CrossRefGoogle Scholar
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