Abstract
Simulation of seed passage through a bird’s gut is an important tool for comparing the effect of bird digestion and thus the potential for plant dispersal by endozoochory. However, sufficient methodology is missing. Thus, we subjected seeds of 20 plant species to seven different simulations of gut passage and to the real passage through a pigeon’s gut to determine which simulation type best reflects the effects of real bird digestion. We also measured various seed traits to identify the traits responsible for differences between species. Results show that four out of seven simulations were significant predictors of seed survival after gut passage. The fit between direct digestion by the pigeon and the different simulation treatments was, however, species-specific and depends not only on the commonly tested traits such as seed mass and water permeability, but also on other unmeasured traits. Seed mass was the best predictor of differences between real digestion and simulation. Selecting one type of simulation to be a good predictor of seed survival after gut passage is difficult. The strongest simulation (24-h scarification and 240-min acid immersion) is the best predictor and may be used to compare the ability of seeds to be dispersed by bird endozoochory. Such knowledge can be included in databases of species traits, as is currently done for many other species traits.
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References
Arechavaleta M, Rodríguez S, Zurita N, García A (Coord.) 2010 Lista de especies silvestres de Canarias. Hongos, plantas y animales terrestres 2009. Gobierno de Canarias. Available at: http://www.gobiernodecanarias.org/cmayot/medioambiente/medionatural/biodiversidad/especies/bancodatos/Lista_Especies_Silvestres.pdf
Barnea A, Yom-Tov Y, Friedman J (1990) Differential germination of two closely related species of Solanum in response to bird ingestion. Oikos 57:222–228
Barnea A, Yom-tov Y, Friedman J (1991) Does ingestion by birds affect seed germination? Funct Ecol 5:394–402
Baumel JJ (1993) Handbook of avian anatomy: Nomina Anatomica Avium. Ed. 2. Nuttall Ornithological Club, Cambridge, MA
Bonn S (2004) Assessment of endozoochorous dispersal potential of plant species by ruminants – approaches to simulate digestion. In Bonn S Dispersal of plants in the Central European landscape – dispersal processes and assessment of dispersal potential exemplified for endozoochory. PhD thesis, University of Regensburg, Regensburg, pp 41–75
Bramwell D (1985) Contribucion a la biogeografia de las Islas Canarias. Bot Macaronés 14:3–34
Brochet AL et al. (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 Bot 93:99–106
Bucher EH, Bocco PJ (2009) Reassessing the importance of granivorous pigeons as massive, long distance seed dispersers. Ecology 90:2321–2327
Carlquist S (1974) Island biology. Columbia University Press, New York and London
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
Clench MH, Mathias JR (1992) Intestinal transit: How can it be delayed long enough for birds to act as long-distance dispersal agents? The Auk 109:933–936
Clench MH, Mathias JR (1995) The avian caecum: a review. Wilson Bull 107:93–121
Clergeau P (1992) The effect of birds on seed germination of fleshy-fruited plants in temperate farmland. Acta Oecol 13:679–686
Clout MN, Tilley JAV (1992) Germination of miro (Prumnopitys ferruginea) seeds after consumption by New Zealand pigeons (Hemiphaga novaeseelandiae). New Zealand J Bot 30:25–28
Cottrell HJ (1947) Tetrazolium salt as a seed germination indicator. Nature 159:748
Crawley MJ (2002) Statistical computing: an introduction to data analysis using S-plus. Wiley & Sons, Chichester
De Vlaming V, Proctor VW (1968) Dispersal of aquatic organisms: viability of seeds recovered from the droppings of captive killdeer and mallard ducks. Amer J Bot 55:20–26
Evenari M (1949) Germination inhibitors. Bot Rev (Lancaster) 15:153–194
Ferianc O et al. (1982) Príručka holubiara (The handbook of pigeon breeders). Príroda, Bratislava (in Slovak)
Figuerola J, Green AJ (2002) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshwater Biol 47:483–494
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
Glyphis JP, Milton SJ, Siegfried WR (1981) Dispersal of Acacia cyclops by birds. Oecologia 48:138–141
Götzenberger L (2005) Seed weight & seed shape. In Knevel IC, Bekker RM, Kunzmann D, Stadler M, Thompson K (eds) The LEDA traitbase collecting and measuring standards of life history traits of the Northwest European flora. Scholma Druk B.V., Bedum, pp 101–104
Hughes L, Dunlop M, French K, Leishman MR, Rice B, Rodgerson L, Westoby M (1994) Predicting dispersal spectra: a minimal set of hypotheses based on plant attributes. J Ecol 82:933–950
Izhaki I, Safriel UN (1990) The effect of some Mediterranean scrubland frugivores upon germination pattern. J Ecol 78:56–65
Janzen DH (1983) Dispersal of seeds by vertebrate guts. In Futuyma DJ, Slatkin M (eds) Coevolution. Sinauer Associates, Sunderland, MA, pp 232–262
Kleyer M, Broker RM, Knevel IC, Bakker JP, Thompson K, Sonnenschein M, Poschlod P, van Groenendael JM, Klimeš L, Klimešová J, Klotz S, Rusch GM, Hermy M, Adriaens D, Boedeltje G, Bossuyt B, Dannemann A, Endels P, Götzenberger L, Hodgson JG, Jackel A-K, Kühn I, Kunzmann D, Ozinga WA, Römermann C, Stadler M, Schlegelmilch J, Steendam HJ, Tackenberg O, Wilmann B, Cornelissen JHC, Eriksson O, Garnier E, Peco B (2008) The LEDA Traitbase: A database of life-history traits of the Northwest European flora. J Ecol 96:1266–1274
Knevel IC, Bekker RM, Kunzmann D, Stadler M, Thompson K (2005) The LEDA traitbase collecting and measuring standards of life history traits of the Northwest European flora. Scholma Druk B.V., Bedum. Available at: http://www.leda-traitbase.org
Krefting LW, Roe EI (1949) The role of some birds and mammals in seed germination. Ecol Monogr 19:270–286
Lakon G (1949) The topographical tetrazolium method for determining the germination capacity of seeds. Pl Physiol 24:389–394
Levey DJ, Grajal A (1991) Evolutionary implications of fruit-processing limitations in Cedar Waxwings. Amer Naturalist 138:171–189
Lieberman M, Lieberman D (1986) An experimental study of seed ingestion and germination in a plant-animal assemblage in Ghana. J Tropic Ecol 2:113–126
MathSoft, Inc. (2000) S-Plus 2000, Professional edition for windows, release 2. Mathsoft, Inc., Massachusetts
McDiarmid RW, Ricklefs RE, Foster MS (1977) Dispersal of Stemmadenia donnell-smithii (Apocynaceae) by birds. Biotropica 9:9–25
Meyer GA, Witmer MC (1997) Influence of seed processing by frugivorous birds on germination success of three North American shrubs. Amer Midl Naturalist 140:129–139
Midya S, Brahmachary RL (1991) The effect of birds upon germination of banyan (Ficus bengalensis) seeds. J Tropical Ecol 7:537–538
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
Murray KG, Winnett-Murray K, Cromie EA, Minor M, Meyers E (1993) The influence of seed packaging and fruit color on feeding preferences of American Robins. Vegetatio 107/108:217–226
Murray KG, Russell S, Picone ChM, 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
Nogales M, Medina FM, Quilis V, González-Rodríguez M (2001) Ecological and biogeographical implications of Yellow-Legged Gulls (Larus cachinnans Pallas) as seed dispersers of Rubia fruticosa Ait. (Rubiaceae) in the Canary Islands. J Biogeogr 28:1137–1145
Ocumpaugh WR, Swakon DHD (1993) Simulating grass seed passage through the digestive system of cattle: A laboratory technique. Crop Sci 33:1084–1090
Paulsen TR, Högstedt GH (2002) Passage through bird guts increase germination and seedling growth in Sorbus aucuparia. Funct Ecol 16:608–616
Ridley HN (1930) The dispersal of seeds throughout the world. Reeve, Ashford, Kent
Rodríguez-Pérez J, Riera N, Traveset A (2005) Effect of seed passage through birds and lizards on emergence rate of mediterranean species: differences between natural and controlled conditions. Funct Ecol 19:699–706
Römermann C, Tackenberg O, Poschlod P (2005) Internal animal dispersal (endozoochory). In Knevel IC, Bekker RM, Kunzmann D , Stadler M, Thompson K (eds) The LEDA traitbase collecting and measuring standards of life history traits of the Northwest European flora. Scholma Druk B.V., Bedum. Available at: http://www.leda-traitbase.org
Sánchez MI, Green AJ, Castellanos EM (2006) Internal transport of seeds by migratory waders in the Odiel marshes, south-west Spain: consequences for long-distance dispersal. J Avian Biol 37:201–206
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
Simao Neto M, Jones RM (1987) Recovery of pasture seed ingested by ruminants. 2. Digestion of seed in sacco and in vitro. Austral J Exp Agric 27:247–251
Soons MB, van der Vlugt C, van Lith B, Heil GW, Klaassen M (2008) Small seed size increases the potential for dispersal of wetland plants by ducks. J Ecol 96:619–627
Spence DHN, Milburn TR, Ndawula-Senyimby M, Roberts E (1971) Fruit biology and germination of two tropical Potamogeton species. New Phytol 70:197–212
Teltscherová L, Hejný S (1973) The germination of some Potamogeton species from South-Bohemian fishponds. Folia Geobot & Phytotax 8:231–239
Traveset A (1998) Effect of seed passage through vertebrates on germination: a review. Perspect Pl Ecol Evol Syst 1:151–190
Traveset A, Riera N, Mas RE (2001) Passage through bird guts causes interspecific differences in seed germination characteristics. Funct Ecol 15:669–675
Traveset A, Rodríguez-Pérez J, Pías B (2008) Seed trait changes in dispersers’ guts and consequences for germination and seedling growth. Ecology 89:95–106
Wahaj SA, Levey DJ, Sanders AK, Cipollini ML (1998) Control of gut retention time by secondary metabolites in ripe Solanum fruits. Ecology 79:2309–2319
Wilkinson DM (1997) Plant colonization: are wind dispersed seeds really dispersed by birds at larger spatial and temporal scales? J Biogeogr 24:61–65
Willson MF (1983) Plant reproductive ecology. John Willey & Sons, New York
Wongsriphuek Ch, 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
Yagihashi T, Hayashida M, Miyamoto T (1998) Effects of bird ingestion on seed germination of Sorbus commixta. Oecologia 114:209–212
Acknowledgements
We thank Dr. D. Bramwell, the director of the Botanical Garden “Jardín Canario Viera y Clavijo” and Dr. J. Caujapé Castells, the Head of Molecular Biodiversity Labs and DNA Bank for enabling collection of seeds in the botanical garden. We also thank other people from these institutes, namely R. Jaén Molina and M. Soto Medina for all the kind help. Many thanks belong also to the staff of the Institute of Botany in Průhonice for helping with all the experiments. This project was supported by GAČR P505/10/0593, GAUK 48807, Mobility Fund of the Charles University in Prague and partly by MSMT and RVO 67985939. All the experiments comply with the current laws of the Czech Republic.
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Vazačová, K., Münzbergová, Z. Simulation of Seed Digestion by Birds: How Does It Reflect the Real Passage Through a Pigeon’s Gut?. Folia Geobot 48, 257–269 (2013). https://doi.org/10.1007/s12224-012-9146-9
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DOI: https://doi.org/10.1007/s12224-012-9146-9