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Effects of seed size and toucan regurgitation on the germination of the tropical tree Eugenia uniflora

Published online by Cambridge University Press:  09 December 2022

Landon R. Jones*
Affiliation:
Department of Wildlife, Fisheries and Aquaculture, Mississippi State University, Mississippi State, Mississippi 39762, USA
Chelsey A. Hunts
Affiliation:
Department of Biological Sciences, California State University, Long Beach, 1250 Bellflower Boulevard, Long Beach, California 90840, USA
Lacy A. Dolan
Affiliation:
Department of Wildlife, Fisheries and Aquaculture, Mississippi State University, Mississippi State, Mississippi 39762, USA
Natasha K. Murphy
Affiliation:
Department of Wildlife, Fisheries and Aquaculture, Mississippi State University, Mississippi State, Mississippi 39762, USA
Gabrielle N. Ripa
Affiliation:
Department of Wildlife, Fisheries and Aquaculture, Mississippi State University, Mississippi State, Mississippi 39762, USA
Emma A. Schultz
Affiliation:
Department of Wildlife, Fisheries and Aquaculture, Mississippi State University, Mississippi State, Mississippi 39762, USA
Varsha S. Shastry
Affiliation:
Department of Wildlife, Fisheries and Aquaculture, Mississippi State University, Mississippi State, Mississippi 39762, USA
Craig A. Sklarczyk
Affiliation:
Department of Wildlife, Fisheries and Aquaculture, Mississippi State University, Mississippi State, Mississippi 39762, USA
Bradly S. Thornton
Affiliation:
Department of Wildlife, Fisheries and Aquaculture, Mississippi State University, Mississippi State, Mississippi 39762, USA
Melanie R. Boudreau
Affiliation:
Department of Wildlife, Fisheries and Aquaculture, Mississippi State University, Mississippi State, Mississippi 39762, USA
*
Author for correspondence: Landon R. Jones, Email: landon.jones@msstate.edu

Abstract

Understanding the quality of seed dispersal effectiveness of frugivorous species can elucidate how endozoochory structures tropical forests. Large seeds, containing more resources for growth, and gut passage by frugivores, which remove seed pulp, both typically enhance the speed and probability of germination of tropical seeds. However, the interaction of seed size and gut passage has not been well studied. We assessed the role of two species of toucans (Ramphastos spp.) in seed germination of the tropical tree Eugenia uniflora, which produces seeds that vary considerably in size (3.7–14.3 mm), using 151 control and 137 regurgitated seeds in germination trials. We found that toucan regurgitation did not increase germination success, although 93.4% germinated compared to 76.8% of control seeds; however, larger seeds germinated more often at faster rates. Although only marginally significant, germination rates were 3.6× faster when seeds were both large and regurgitated by toucans, demonstrating that toucan regurgitation can disproportionally benefit larger E. uniflora seeds. As tropical forests are increasingly disturbed and fragmented by human activities, the ability of toucans to continue providing seed dispersal services to degraded habitats may be vital to the persistence of many tropical plants that contain larger seeds and depend on larger dispersers.

Type
Short Communication
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Amador, TS and Barbedo, CJ (2015) Germination inhibits the growth of new roots and seedlings in Eugenia uniflora and Eugenia brasiliensis. Journal of Seed Science 37, 241247.CrossRefGoogle Scholar
Andresen, E, Arroyo-Rodriguez, V and Ramos-Robles, M (2018) Primate seed dispersal: old and new challenges. International Journal of Primatology 39, 443465.CrossRefGoogle Scholar
Aslan, CE, Zavaleta, ES, Tershy, B and Croll, D (2013) Mutualism disruption threatens global plant biodiversity: a systematic review. PLoS ONE 8, e66993.CrossRefGoogle ScholarPubMed
Barnea, A, Yom-Tov, Y and Friedman, J (1991) Does ingestion by birds affect seed germination? Functional Ecology 5, 394402.CrossRefGoogle Scholar
Bazzaz, FA and Pickett, STA (1980) Physiological ecology of tropical succession: a comparative review. Annual Review of Ecology, Evolution, and Systematics 11, 287310.CrossRefGoogle Scholar
Bewleyl, JD (1997) Seed germination and dormancy. The Plant Cell 9, 10551056.CrossRefGoogle Scholar
Central American Commission on Environment and Development (1998) Central American Vegetation/Land Cover Classification and Conservation Status. Palisades, NY: NASA Socioeconomic Data and Applications Center (SEDAC).Google Scholar
Daws, MI, Crabtree, LM, Dalling, JW, Mullins, CE and Burslem, DFRP (2008) Germination responses to water potential in neotropical pioneers suggest large-seeded species take more risks. Annals of Botany 102, 945951.CrossRefGoogle ScholarPubMed
Daws, MI, Garwood, NC and Pritchard, HW (2005) Traits of recalcitrant seeds in a semi-deciduous tropical forest in Panamá: some ecological implications. Functional Ecology 19, 874885.CrossRefGoogle Scholar
Deb, P and Sundriyal, RC (2017) Effect of seed size on germination and seedling fitness in four tropical rainforest tree species. Indian Journal of Forestry 40, 313322.CrossRefGoogle Scholar
Fricke, EC, Bender, J, Rehm, EM and Rogers, HS (2019) Functional outcomes of mutualistic network interactions: a community-scale study of frugivore gut passage on germination. Journal of Ecology 107, 757767.CrossRefGoogle Scholar
Fukui, A (2003) Relationship between seed retention time in bird’s gut and fruit characteristics. Ornithological Science 2, 4148.CrossRefGoogle Scholar
Fuzessy, LF, Conelissen, TG, Janson, C and Silveira, FAO (2016) How do primates affect seed germination? A meta-analysis of gut passage effects on neotropical plants. Oikos 125, 10691080.CrossRefGoogle Scholar
Fuzessy, LF, Janson, C and Silviera, FAO (2018) Effects of seed size and frugivory degree on dispersal by Neotropical frugivores. Acta Oecologica 93, 4147.CrossRefGoogle Scholar
Galetti, M, Guevara, R, Côrtes, MC, Fadini, R, Von Matter, S, Leite, AB, Labecca, F, Ribeiro, T, Carvalho, CS, Collevatti, RG, Pires, MM, Guimarães, PR, Brancalion, PH, Ribeiro, MC and Jordano, P (2013) Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340, 10861090.CrossRefGoogle ScholarPubMed
Godínez-Alvarez, H, Ríos-Casanova, L and Peco, B (2020) Are large frugivorous birds better seed dispersers than medium- and small-sized ones? Effect of body mass on seed dispersal effectiveness. Ecology and Evolution 10, 61366143.CrossRefGoogle ScholarPubMed
Graham, CH (2001) Factors influencing movement patterns of keel-billed toucans in a fragmented tropical landscape in southern Mexico. Conservation Biology 15, 17891798.CrossRefGoogle Scholar
Holbrook, KM and Loiselle, BA (2007) Using toucan-generated dispersal models to estimate seed dispersal in Amazonian Ecuador. In Dennis, A, Schupp, E, Green, R and Westcott, D (eds), Seed Dispersal: Theory and Its Application in a Changing World. Wallingford, UK: CAB International Publishing, pp. 300321.Google Scholar
Holbrook, KM and Loiselle, BA (2009) Dispersal in a Neotropical tree, Virola flexuosa (Myristicaceae): does hunting of large vertebrates limit seed removal? Ecology 90, 14491455.Google Scholar
Howe, H (1981) Dispersal of a neotropical nutmeg (Virola sebifera) by Birds. The Auk 98, 8898.Google Scholar
Howe, HF (1993) Aspects of variation in a neotropical seed dispersal system. In Fleming, TH and Estrada, A (eds), Frugivory and Seed Dispersal: Ecological and Evolutionary Aspects. Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 149162.CrossRefGoogle Scholar
Howe, HF and Smallwood, J (1982) Ecology of seed dispersal. Annual Review of Ecology and Systematics 13, 201228.Google Scholar
Jones, LR (2017) Modeling the effects of animal movements and behavior on spatial patterns of seed dispersal in fragmented landscapes. PhD Thesis. University of Louisiana at Lafayette.Google Scholar
Levey, DJ (1987) Seed size and fruit-handling techniques of Avian Frugivores. The American Naturalist 129, 471485.Google Scholar
Levine, JM and Murrell, DJ (2003) The community-level consequences of seed dispersal patterns. Annual Review of Ecology, Evolution, and Systematics 34, 549574.Google Scholar
Loayza, AP and Rios, RS (2014) Seed-swallowing Toucans are less effective dispersers of Guettarda viburnoides (Rubiaceae) than Pulp-feeding Jays. Biotropica 46, 6977.CrossRefGoogle Scholar
McConkey, KR, Prasad, S, Corlett, RT, Campos-Arceiz, A, Brodie, JF, Rogers, H and Santamaria, L (2012) Seed dispersal in changing landscapes. Biological Conservation 146, 113.CrossRefGoogle Scholar
Moreira, JI, Riba-Hernández, P and Lobo, JA (2017) Toucans (Ramphastos ambiguus) facilitate resilience against seed dispersal limitation to a large-seeded tree (Virola surinamensis) in a human-modified landscape. Biotropica 49, 502510.CrossRefGoogle Scholar
Morton, J (1987) Fruits of Warm Climates. Miami, USA: Creative Resource Systems, Inc.Google Scholar
Murali, KS (1997) Patterns of seed size, germination and seed viability of tropical tree species in Southern India. Biotropica 29, 271279.CrossRefGoogle Scholar
Nakagawa, S and Cuthill, IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biological Reviews 82, 591605.CrossRefGoogle ScholarPubMed
Nathan, R and Muller-Landau, HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology & Evolution 15, 278285.CrossRefGoogle ScholarPubMed
Pavithra, S, Swamy, G, Suresh, GJ and Ruchita, T (2020) Study on viability of Surinam cherry (Eugenia uniflora L.) seeds on germination behaviour and Vigour of the seedling. Journal of Pharmacognosy and Phytochemistry 9, 18021804.Google Scholar
Pirola, K, Wagner, A Jr, Dotto, M, Cassol, DA, Possenti, JC and Citadin, I (2021) Dormancy in native fruit seeds of the Brazilian South Region. Colloquium Agrariae 17, 2132.CrossRefGoogle Scholar
R Core Team (2021) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Schupp, EW, Jordano, P and Gómez, JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188, 333353.CrossRefGoogle ScholarPubMed
Short, LL and Horne, JFM (2002) Toucans, Barbets, and Honeyguides. In Perrins, CM, Bock, WJ and Kikkawa, J (eds), Bird Families of the World Series. New York, USA: Oxford University Press, pp. 4455.Google Scholar
Smiderle, OJ, Souza, G and Souza, AA (2016) Morphological aspects of seeds, emergence and growth of seedlings of Surinam cherry trees sown at different depths. Journal of Plant Sciences 4, 119.Google Scholar
Snell, RS, Beckman, NG, Fricke, E, Loiselle, BA, Carvalho, CS, Jones, LR, Lichti, NI, Lustenhouwer, N, Schreiber, SJ, Strickland, C, Sullivan, LL, Cavazos, BR, Giladi, I, Hastings, A, Holbrook, K, Jongejans, E, Kogan, O, Montaño-Centellas, F, Rudolph, J, Rogers, HS, Zwolok, R, Schupp, E (2019) Consequences of intraspecific variation in seed dispersal for plant demography, communities, evolution and global change. AoB Plants 11, plz016.CrossRefGoogle ScholarPubMed
Stricker, KB and Stiling, P (2013) Seedlings of the introduced invasive shrub Eugenia uniflora (Myrtaceae) outperform those of its native and introduced non-invasive congeners in Florida. Biological Invasions 15, 19731987.CrossRefGoogle 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, Riera, N and Mas, RE (2001) Passage through bird guts causes interspecific differences in seed germination characteristics. Functional Ecology 15, 669675.CrossRefGoogle Scholar
Travaset, A, Robertson, AW and Rodriguez-Perez, J (2007) A review on the role of endozoochory in seed germination. In Dennis, AJ, Schupp, EW, Green, RJ and Westcott, DA (eds), Seed Dispersal: Theory and Its Application in a Changing World. Wallinford, UK: CAB International, pp. 78103.CrossRefGoogle Scholar
Travaset, A and Verdú, M (2009) A meta-analysis of the effect of gut treatment on seed germination. In Levey, DJ, Silva, WR and Galetti, M (eds), Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. New York, USA: CAB International, pp. 339349.Google Scholar
Vázquez-Yanez, C and Orozco-Segovia, A (1993) Patterns of seed longevity and germination in the tropical rainforest. Annual Review of Ecology and Systematics 24, 6987.CrossRefGoogle Scholar
Verdú, M and Traveset, A (2004) Bridging meta-analysis and the comparative method: a test of seed size effect on germination after frugivores’ gut passage. Oecologia 138, 414418.Google Scholar
Vespa, NI, Zurita, GA, Gatti, MG and Bellocq, MI (2018) Seed movement between the native forest and monoculture tree plantations in the southern Atlantic forest: a functional approach. Forest Ecology and Management 430, 126133.CrossRefGoogle Scholar
Vidal, MM, Pires, MM and Guimarães, PR (2013) Large vertebrates as the missing components of seed-dispersal networks. Biological Conservation 163, 4248.CrossRefGoogle Scholar
Young, JA and Evans, RA (1977) Squirreltail seed germination. Journal of Range Management 30, 3336.CrossRefGoogle Scholar