Skip to main content
Log in

A meta-analysis of the effects of frugivory (endozoochory) on seed germination: role of seed size and kind of dormancy

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Heretofore, no study has determined how germination of ingested seeds is affected by the kind (class) of dormancy nor by seed dormancy x seed size interaction. Thus, we aimed to determine the effects of seed size, kind of dormancy and their interaction on germination of defecated seeds using a meta-analysis. We collected data for 366 plant species in 97 plant families from 76 publications. In general, gut passage significantly increased germination percentage of defecated seeds by 5% compared with that of control seeds. Germination percentages of non-dormant, physiologically dormant, and morphologically/morphophysiologically dormant seeds (all water-permeable) significantly decreased after gut passage by 40, 18, and 14%, respectively, compared with control seeds (non-gut-passed). Changes in germination percentage of seeds with physical dormancy (water-impermeable) were positive, and gut passage increased germination by 69% compared with control seeds. Germination of small seeds decreased 8% after gut passage, whereas germination of both medium and large seeds increased by 18%. However, changes in germination percentage differed between categories of seed size in each class of dormancy. In physically dormant seeds, germination of all seed sizes improved after gut passage, and the magnitude of increase was higher for large than for medium and small seeds. Thus, gut passage increased germination of medium-size water-permeable seeds (physiologically dormant and morphologically/morphophysiologically dormant) more than it did for large and small seeds. However, gut-passage decreased or did not change the germination percentage of non-dormant seeds. Seed size and kind of dormancy should be included in studies on the effect of gut passage on germination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Barrett GJ (2003) Seed dormancy and germinability in the halophyte Halosarcia pergranulata subsp. pergranulata. Seed Sci Technol 31:289–299

    Article  Google Scholar 

  • Baskin JM, Baskin CC (2004) A classification system for seed dormancy. Seed Sci Res 14:1–16

    Google Scholar 

  • Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination –, 2nd edn. Elsevier/Academic Press, San Diego

    Google Scholar 

  • Benthien O, Bober J, Castens J, Stolter C (2016) Seed dispersal capacity of sheep and goats in a near-coastal dry grassland habitat. Basic Appl Ecol 17:508–515

    Article  Google Scholar 

  • Brochet A, Guillemain M, Gauthier-Clerc M, Fritz H, Green AJ (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. Aquat Bot 93:99–106

    Article  Google Scholar 

  • Cáceres NC, Monteiro-Filho ELA (2007) Germination in seed species ingested by opossums: implications for seed dispersal and forest conservation. Braz Arch Biol Technol 50:921–928

    Article  Google Scholar 

  • Calvino-Cancela M, Rubido-Bará M (2012) Effects of seed passage through slugs on germination. Plant Ecol 213:663–673

    Article  Google Scholar 

  • Camacho Morfin F (1990) Eliminacion de la dormicion de semillas de capulin Prunus serotina ssp. capuli (Cav.) mediante el remojo y secado. Rev Cienc For Mexico 67:63–73

    Google Scholar 

  • Chapman HM, Goldson SL, Beck J (2009) Post dispersal removal and germination of seed dispersed by Cercopithecus nictitans in a West African montane forest. Folia Primatol 81:41–50

    Article  Google Scholar 

  • Cirak C, Kevseroglu K, Sağlam B (2004) Physical and physiological dormancy in black henbane (Hyoscyamus niger L.) seeds. J Plant Biol 47:391–395

    Article  CAS  Google Scholar 

  • Cox JR, De Alba-Avila A, Rice RW, Cox JN (1993) Biological and physical factors influencing Acacia constricta and Prosopis velutina establishment in the Sonoran Desert. J Range Manag 46:43–48

    Article  Google Scholar 

  • de Azevedo CS, da Silva MC, Teixeira TP, Young RJ, Garcia QS, Rodrigues M (2013) Effect of passage through the gut of Greater Rheas on the germination of seeds of plants of cerrado and caatinga grasslands. Emu 113:177–182

    Article  Google Scholar 

  • Eriksson O (2016) Evolution of angiosperm seed disperser mutualisms: the timing of origins and their consequences for coevolutionary interactions between angiosperms and frugivores. Biol Rev 91:168–186

    Article  Google Scholar 

  • Eriksson O, Friis EM, Löfgren P (2000) Seed size, fruit size, and dispersal systems in angiosperms from the Early Cretaceous to the Late Tertiary. Am Nat 156:47–58

    Article  Google Scholar 

  • Figuerola J, Green AJ (2002) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshw Biol 47:483–494

    Article  Google Scholar 

  • Foley ME (2004) Leafy spurge (Euphorbia escula) seed dormancy. Weed Sci 52:74–77

    Article  CAS  Google Scholar 

  • Fukui AW (1995) The role of the brown-eared bulbul Hypsypetes amaurotis as a seed dispersal agent. Res Popul Ecol 37:211–218

    Article  Google Scholar 

  • Fuzessy LF, Cornelissen TG, Janson C, Silveira FAO (2016) How do primates affect seed germination? A meta-analysis of gut passage effects on neotropical plants. Oikos 125:1069–1080

    Article  Google Scholar 

  • Garcia QS, Sharif RR (1995) Germinacao e dormencia em aquenios de Acanthospermum hispidum, DC., uma especia invasora. Rev Brasil Bot 18:17–25

    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 

  • Gardener MR, Whalley RDB, Sindel BM (2003a) Ecology of Nassella neesiana, Chilean needle grass, in pastures on the Northern Tablelands of New South Wales. I. Seed production and dispersal. Aust J Agric Res 54:613–619

    Article  Google Scholar 

  • Gardener MR, Whalley RDB, Sindel BM (2003b) Ecology of Nassella neesiana, Chilean needle grass, in pastures on the Northern Tablelands of New South Wales. II. Seedbank dynamics, seed germination, and seedling recruitment. Aust J Agric Res 54:621–626

    Article  Google Scholar 

  • Gasque M, Garcia-Fayos P (2003) Seed dormancy and longevity in Stipa tenacissima L. (Poaceae). Plant Ecol 168:279–290

    Article  Google Scholar 

  • Graae BJ, Pagh S, Bruun HH (2004) An experimental evaluation of the afox (Alopex lagopus) as a seed disperser. Arct Antarct Alp Res 36:468–473

    Article  Google Scholar 

  • Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analysis. Ecology 80:1142–1149

    Article  Google Scholar 

  • Hedges LV, Gurevitch J, Curtis P (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156

    Article  Google Scholar 

  • Ishikawa H (2010) Effects of ingestion of seeds by sika deer (Cervus nippon) and dung presence on their germination in a herbaceous community. Ecol Res 25:591–598

    Article  Google Scholar 

  • Izhaki I, Korine C, Arad Z (1995) The effect of bat (Rousettus aegyptiacus) dispersal on seed germination in eastern Mediterranean habitats. Oecologia 101:335–342

    Article  CAS  Google Scholar 

  • Jaganathan GK, Wu GR, Han YY, Liu BL (2016) Role of lens in controlling physical dormancy break and germination of Delonix regia (Fabaceae: Caesalpinioideae). Plant Biol 19:53–60

    Article  Google Scholar 

  • Jurado E, Joel F (2005) Is seed dormancy under environmental control or bound to plant traits? J Veg Sci 16:559–564

    Article  Google Scholar 

  • Kuiters A, Huiskes H (2010) Potential of endozoochorous seed dispersal by sheep in calcareous grasslands: correlations with seed traits. Appl Veg Sci 13:163–172

    Article  Google Scholar 

  • Lautenschlager RA (1997) Effects of perturbations and stimulants on red raspberry (Rubus idaeus L.) seed germination. For Chron 73:453–457

    Article  Google Scholar 

  • Lehouck V, Spanhove T, Lens L (2011) Avian fruit ingestion differentially facilitates seed germination of four fleshy-fruited plant species of an Afrotropical forest. Plant Ecol Evol 144:96–100

    Article  Google Scholar 

  • Linnebjerg JF, Hansen DM, Olesen JM (2009) Gut passage effect of the introduced red-whiskered bulbul (Pycnonotus jocosus) on germination of invasive plant species in Mauritius. Aust Ecol 34:272–277

    Article  Google Scholar 

  • Linquist BA, Liu L, van Kessel C, van Groenigen KJ (2013) Enhanced efficiency of nitrogen fertilizers for rice systems: meta-analysis of yield and nitrogen uptake. Field Crops Res 154:246–254

    Article  Google Scholar 

  • Lopez JE, Vaugh C (2004) Observations on the role of frugivorous bats as seed dispersers in Costa Rican secondary humid forests. Acta Chiropt 6:111–119

    Article  Google Scholar 

  • Manzano P, Malo JE, Peco B (2005) Sheep gut passage and survival of Mediterranean shrub seeds. Seed Sci Res 15:21–28

    Article  Google Scholar 

  • Milotić T, Hoffmann M (2016) How does gut passage impact endozoochorous seed dispersal success? Evidence from a gut environment simulation experiment. Basic Appl Ecol 17:165–176

    Article  Google Scholar 

  • Morpeth DR, Hall AM (2000) Microbial enhancement of seed germination in Rosa corymbifera ‘laxa’. Seed Sci Res 10:489–494

    Article  Google Scholar 

  • Mouissie A, Van Der Veen CE, Veen GC, Van Diggelen R (2005) Ecological correlates of seed survival after ingestion by fallow deer. Funct Ecol 19:284–290

    Article  Google Scholar 

  • Pakeman R, Digneffe G, Small J (2002) Ecological correlates of endozoochory by herbivores. Funct Ecol 16:296–304

    Article  Google Scholar 

  • Pardón B, Nogales M, Traveset A, Vilá M, Martínez-Abraín A, Padilla DP, Marrero P (2011) Integration of invasive Opuntia spp. by native and alien seed dispersers in the Mediterranean area and the Canary Islands. Biol Invasions 13:831–844

    Article  Google Scholar 

  • Pollux BJA, Ouborg NJ, Van Groenendael JM, Klaassen M (2007) Consequences of intraspecific seed-size variation in Sparganium emersum for dispersal by fish. Funct Ecol 21:1084–1091

    Article  Google Scholar 

  • Robertson AW, Trass A, Ladley JJ, Kelly D (2006) Assessing the benefits of frugivory for seed germination: the importance of the deinhibition effect. Funct Ecol 20:58–66

    Article  Google Scholar 

  • Rosenberg MS, Garrett KA, Su Z, Bowden RL (2004) Meta-analysis in plant pathology: synthesizing research results. Phytopathology 94:1013–1017

    Article  CAS  Google Scholar 

  • Rosenthal R (1979) The “file drawer problem” and tolerance for null results. Psycol Bull 86:638–641

    Article  Google Scholar 

  • Russi L, Cocks P, Roberts E (1992) The fate of legume seeds eaten by sheep from a Mediterranean grassland. J Appl Ecol 29:772–778

    Article  Google Scholar 

  • Samuels IA, Levey DJ (2005) Effects of gut passage on seed germination: do experiments answer the questions they ask? Funct Ecol 19:365–368

    Article  Google Scholar 

  • Sato H (2009) Gut passage time and size of swallowed seeds in the common brown lemur and the mongoose lemur. Primatol Res 25:45–54

    Article  Google Scholar 

  • Sengupta A, Mcconkey KR, Radhakrishna S (2014) Seed dispersal by rhesus macaques Macaca mulatta in Northern India. Am J Primatol 76:1175–1184

    Article  Google Scholar 

  • Soltani E, Soltani A (2015) Meta-analysis of seed priming effects on seed germination, seedling emergence and crop yield: Iranian studies. Int J Plant Prod 9:413–432

    Google Scholar 

  • Stevenson PR, Castellanos MC, Pizarro JC, Garavito M (2002) Effects of seed dispersal by three ateline monkey species on seed germination at Tinigua National Park, Colombia. Int J Primatol 23:1187–1204

    Article  Google Scholar 

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

    Google Scholar 

  • Traveset A, Robertson AW, Rodríguez-Pérez J (2007) A review on the role of endozoochory in seed germination. In: Dennis AJ, Schupp EW, Green RJ, Westcott (eds) Seed dispersal: theory and its application in a changing world. CABI International, Wallingford, pp 78–103

    Chapter  Google Scholar 

  • Valenta K, Fedigan LM (2009) Effects of gut passage, feces, and seed handling on latency and rate of germination in seeds consumed by capuchins (Cebus capucinus). Am Phys Anthropol 138:486–492

    Article  Google Scholar 

  • Van Auken OW (2001) Germination requirements of seeds of Helianthus paradoxus (Asteraceae). Texas J Sci 53:157–170

    Google Scholar 

  • Verdu M, Travest A (2004) Bridging meta-analysis and the comparative method: a test of seed size effect on germination after frugivores’ gut passage. Oecologia 138:414–418

    Article  Google Scholar 

  • Wang S, Lu W, Waly N, Ma C (2017) Recovery and germination of seeds after passage through the gut of Kazakh sheep on the north slope of the Tianshan Mountains. Seed Sci Res 27:43–49

    Article  CAS  Google Scholar 

  • Willis C, Baskin CC, Baskin JM, Auld J, Venable D, Cavender-Bares J, Donohue K, de Casas R, The NESCent Germination Working Group (2014) The evolution of seed dormancy: environmental cues, evolutionary hubs, and diversification of the seed plants. New Phytol 203:300–309

    Article  Google Scholar 

  • Xing F, Guo J, Wang Y (2003) Seed germination characteristics and regeneration mechanism of Stellera chamaejasme population. Ying Sheng Xueb 14:1851–1854 (in Chinese with English abstract)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elias Soltani.

Additional information

Communicated by Elizabeth Pringle.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soltani, E., Baskin, C.C., Baskin, J.M. et al. A meta-analysis of the effects of frugivory (endozoochory) on seed germination: role of seed size and kind of dormancy. Plant Ecol 219, 1283–1294 (2018). https://doi.org/10.1007/s11258-018-0878-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-018-0878-3

Keywords

Navigation