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Species identity influences secondary removal of seeds of Neotropical pioneer tree species

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Abstract

Primary dispersal agents move seeds from the maternal plant to the soil surface where they are often moved again by secondary dispersal agents. However, the extent to which different species in the same location experience secondary dispersal is often unknown despite the importance of this mechanism for determining recruitment opportunities and consequently community structure. Here we examine the secondary removal rates of 12 Neotropical pioneer species placed either on or 2 cm below the soil surface at five locations in lowland tropical forest on Barro Colorado Island, Panama. We investigated whether species identity, primary dispersal mode (animal or wind), dormancy type, seed mass, and capacity to persist in the seed bank were correlated with removal rate. We also investigated whether season (dry or wet) influences removal from the soil surface. In general, both superficial and buried seeds were highly mobile. We found an effect of primary dispersal mode and dormancy type on removal rates both on (12 species) and beneath the soil surface (six species). However, this pattern was largely driven by species identity. Season had no influence on seed removal rates from the soil surface. The dispersal of small-seeded pioneer species is highly species dependent, indicating that generalizations made using broader categories, such as primary dispersal mode or dormancy type, do not accurately describe the observed patterns hindering our understanding of community assembly within even a single functional group of plants.

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References

  • Andreson E, Levey DJ (2004) Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 139:45–54. doi:10.1007/s00442-003-1480-4

    Article  Google Scholar 

  • Bagchi R, Gallery RE, Gripenberg S, Gurr SJ, Narayan L, Addis CE, Freckleton RP, Lewis OT (2014) Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506:85–88. doi:10.1038/nature12911

    Article  CAS  PubMed  Google Scholar 

  • Baillie I, Elsenbeer H, Barthold F, Grimm R, Stallard R (2006) A semi-detailed soil survey of Barro Colorado Island. Panama: Smithsonian Tropical Research Institute. http://biogeodb.stri.si.edu/bioinformatics/bci_soil_map/documentation/BCI_soil_report_complete.pdf. Accessed 6 June 2017

  • Barbosa AM, Brown JA, Jimenez-Valverde A, Real R (2016) modEvA: Model evaluation and analysis. R package version 1.3.2. http://CRAN.R-project.org/package=modEvA

  • Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055. doi:10.2307/1940179

    Article  Google Scholar 

  • Chambers JC, MacMahon JA (1994) A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annu Rev of Ecol Syst 25:263–292. doi:10.1146/annurev.es.25.110194.001403

    Article  Google Scholar 

  • Comita LS, Hubbell SP (2009) Local neighborhood and species’ shade tolerance influence survival in a diverse seeding bank. Ecology 90:328–334. doi:10.1890/08-0451.1

    Article  PubMed  Google Scholar 

  • Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: den Boer PJ, Gradwell GR (eds) Dynamics of Populations. Centre for Agricultural Publishing and Documentation, Wageningen, pp 298–312

    Google Scholar 

  • Dalling JW, Hubbell SP (2002) Seed size, growth rate and gap microsite conditions as determinants of recruitment success for pioneer species. J Ecol 90:557–568. doi:10.1046/j.1365-2745.2002.00695.x

    Article  Google Scholar 

  • Dalling JW, Brown TA (2009) Long-term persistence of pioneer seeds in tropical rain forest soil seed banks. Am Nat 173:531–535. doi:10.1086/597221

    Article  PubMed  Google Scholar 

  • Dalling JW, Swaine MD, Garwood NC (1997) Soil seed bank community dynamics in seasonally moist lowland tropical forest, Panama. J Trop Ecol 13:659–680. doi:10.1017/S0266467400010853

    Article  Google Scholar 

  • Dalling JW, Muller-Landau HC, Wright SJ, Hubbell SP (2002) Role of dispersal in the recruitment limitation of Neotropical pioneer species. J Ecol 90:714–727. doi:10.1046/j.1365-2745.2002.00706.x

    Article  Google Scholar 

  • Enders RK (1935) Mammalian life histories from Barro Colorado Island, Panama. Bull Museum Comp Zool 78:385–502

    Google Scholar 

  • Estrada A, Coates-Estrada R (1991) Howler monkeys (Alouatta palliata), dung beetles (Scarabaeidae) and seed dispersal: ecological interactions in the tropical rain forest of Los Tuxtlas, Mexico. J Trop Ecol 7:459–474. doi:10.1017/S026646740000585X

    Article  Google Scholar 

  • Fornara DA, Dalling JW (2005a) Post-dispersal removal of seeds of pioneer species from five Panamanian forests. J Trop Ecol 21:79–84. doi:10.1017/S026646740400197X

    Article  Google Scholar 

  • Fornara DA, Dalling JW (2005b) Seed bank dynamics in five Panamanian forests. J Trop Ecol 21:223–226. doi:10.1017/S0266467404002184

    Article  Google Scholar 

  • Franz NM, Wcislo WT (2003) Foraging behavior in two species of Ectatomma (Formicidae: Ponerinae): individual learning of orientation and timing. J Insect Behav 16:381–410

    Article  Google Scholar 

  • Garb J, Kotler BP, Brown JS (2000) Foraging and community consequences of seed size for coexisting Negev Desert granivores. Oikos 88:291–300

    Article  Google Scholar 

  • Garcia-Orth X, Martinez-Ramos M (2008) Seed dynamics of early and late successional tree species in tropical abandoned pasture: seed burial as a way of evading predation. Restor Ecol 16:435–443. doi:10.1111/j.1526-100X.2007.00320.x

    Article  Google Scholar 

  • Gripenberg S, Rota J, Kim J, Wright SJ, Garwood NC, Fricke EC, Zalamea P-C, Salminen J-P (2017) Seed polyphenols in a diverse tropical plant community. J Ecol. doi:10.1111/1365-2745.12814

  • Holt RD, Kotler BP (1987) Short-term apparent competition. Am Nat 130:412–430

    Article  Google Scholar 

  • Horvitz CC, Schemske DW (1986) Seed dispersal of a Neotropical myrmecochore: variation in removal rates and dispersal distance. Biotropica 18:319–323

    Article  Google Scholar 

  • Hubbell SP, Foster FB, O’Brien ST, Harms KE, Condit R, Wechsler B, Wright SJ, Loo de Lao S (1999) Light-gap disturbances, recruitment limitation, and tree diversity in a Neotropical forest. Science 283:554–557. doi:10.1126/science.283.5401.554

    Article  CAS  PubMed  Google Scholar 

  • Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528. doi:10.1086/282687

    Article  Google Scholar 

  • Janzen DH (1975) Intra- and interhabitat variations in Guazuma ulmifolia (Sterculiaceae) seed predation by Amblycerus cistelinus (Bruchidae) in Costa Rica. Ecology 56:1009–1013. doi:10.2307/1936314

    Article  Google Scholar 

  • Kaspari M, Weiser MD (2000) Ant activity along moisture gradients in a Neotropical forest. Biotropica 32:703–711

    Article  Google Scholar 

  • Leal IR, Oliveira PS (2000) Foraging ecology of attine ants in a Neotropical savanna: seasonal use of fungal substrate in the cerrado vegetation of Brazil. Insectes Soc 47:376–382. doi:10.1007/PL00001734

    Article  Google Scholar 

  • Long RL, Gorecki MJ, Renton M, Scott JK, Colville L, Goggin DE, Commander LE, Westcott DA, Cherry H, Finch-Savage WE (2015) The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biol Rev 90:31–59. doi:10.1111/brv.12095

    Article  PubMed  Google Scholar 

  • Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755. doi:10.1038/nature09273

    Article  CAS  PubMed  Google Scholar 

  • Marshall DL, Beattie AJ, Bollenbacher WE (1979) Evidence for diglycerides as attractants in an ant-seed interaction. J Chem Ecol 5:335–344

    Article  CAS  Google Scholar 

  • Mascaro J, Asner GP, Muller-Landau HC, van Breugel M, Hall J, Dahlin K (2011) Controls over aboveground forest carbon density on Barro Colorado Island, Panama. Biogeosciences 8:1615–1629. doi:10.5194/bg-8-1615-2011

    Article  Google Scholar 

  • Milton K, Windsor DM, Morrison DW, Estribi MA (1982) Fruiting phenologies of two Neotropical Ficus species. Ecology 63:752–762. doi:10.2307/1936796

    Article  Google Scholar 

  • Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285. doi:10.1016/S0169-5347(00)01874-7

    Article  CAS  PubMed  Google Scholar 

  • Paulsen TR, Colville L, Kranner I, Daws MI, Högstedt G, Vandvik V, Thompson K (2013) Physical dormancy in seeds: a game of hide and seek? New Phytol 198:496–503. doi:10.1111/nph.12191

    Article  CAS  PubMed  Google Scholar 

  • Phillips O (1990) Ficus insipida (Moraceae): ethnobotany and ecology of an Amazonian anthelmintic. Econ Bot 44:534–536

    Google Scholar 

  • Pinheiro J, Bates D, Sarkar D, Eispack, Heisterkamp S, Van Willigen B, R Core Team (2015) nlme: Linear and nonlinear mixed effects models. R package version 3.1-127. http://CRAN.R-project.org/package=nlme

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Sautu A, Baskin JM, Baskin CC, Deago J, Condit R (2007) Classification and ecological relationships of seed dormancy in a seasonal moist tropical forest, Panama, Central America. Seed Sci Res 17:127–140. doi:10.1017/S0960258507708127

    Article  Google Scholar 

  • Schnitzer SA, Dalling JW, Carson WP (2000) The impact of lianas on tree regeneration in tropical forest canopy gaps: evidence for an alternative pathway of gap-phase regeneration. Ecology 88:655–666. doi:10.1046/j.1365-2745.2000.00489.x

    Article  Google Scholar 

  • Scotti-Sintagne C, Dick CW, Caron H, Vendramin GG, Troispoux V, Sire P, Casalis M, Bounomici A, Valencia R, Lemes MR, Gribel R, Scotti I (2013) Amazon diversification and cross-Andean dispersal of the widespread Neotropical tree species Jacaranda copaia (Bignoniaceae). J Biogeogr 40:707–719. doi:10.1111/j.1365-2699.2012.02797.x

    Article  Google Scholar 

  • Seidler TG, Plotkin JB (2006) Seed dispersal and spatial pattern in tropical trees. PLoS Biol 4:e344. doi:10.1371/journal.pbio.0040344

    Article  PubMed  PubMed Central  Google Scholar 

  • Swaine MD, Whitmore TC (1988) On the definition of ecological species groups in tropical rain forests. Vegetatio 75:81–86

    Article  Google Scholar 

  • Tiansawat P, Davis AS, Berhow MA, Zalamea P-C, Dalling JW (2014) Investment in seed physical defense is associated with species’ light requirement for regeneration and seed persistence: evidence from Macaranga species in Borneo. PLoS ONE 9:e99691. doi:10.1371/journal.pone.0099691

    Article  PubMed  PubMed Central  Google Scholar 

  • Vander Wall SB, Longland WS (2004) Diplochory: are two seed dispersers better than one? Trends Ecol Evol 19:155–161. doi:10.1016/j.tree.2003.12.004

    Article  PubMed  Google Scholar 

  • Vander Wall SB, Kuhn KM, Beck MJ (2005) Seed removal, seed predation, and secondary dispersal. Ecology 86:801–806. doi:10.1890/04-0847

    Article  Google Scholar 

  • Vazquez-Yanes C, Perez-Garcia B (1976) Notas sobre la morfologia y la anatomia de la testa de las semillas de Ochroma lagopus Sw. Turrialba 26:310–311

    Google Scholar 

  • Veech JA (2000) Predator-mediated interactions among the seeds of desert plants. Oecologia 124:402–407

    Article  CAS  PubMed  Google Scholar 

  • Wilkie KT, Mertl AL, Traniello JFA (2007) Biodiversity below ground: probing the subterranean ant fauna of Amazonia. Naturwissenschaften 94:725–731. doi:10.1007/s00114-007-0250-2

    Article  Google Scholar 

  • Windsor DM (1990) Climate and moisture variability in a tropical forest: long-term records from Barro Colorado Island, Panama. Smithson Contrib Earth Sci 29:1–145

    Article  Google Scholar 

  • Young TP, Hubbell SP (1991) Crown asymmetry, treefalls, and repeat disturbance of broad-leaved forest gaps. Ecology 72:1464–1471. doi:10.2307/1941119

    Article  Google Scholar 

  • Zalamea P-C, Munoz F, Stevenson PR, Paine CET, Sarmiento C, Sabatier D, Heuret P (2011) Continental-scale patterns of Cecropia reproductive phenology: evidence from herbarium specimens. Proc R Soc B 278:2437–2445. doi:10.1098/rspb.2010.2259

    Article  PubMed  PubMed Central  Google Scholar 

  • Zalamea P-C, Heuret P, Sarmiento C, Rodríquez M, Berthouly A, Guitet S, Nicolini E, Delnatte C, Barthélémy D, Stevenson PR (2012) The genus Cecropia: a biological clock to estimate the age of recently disturbed areas in the Neotropics. PLoS ONE 7:e42643. doi:10.1371/journal.pone.0042643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zalamea P-C, Sarmiento C, Arnold AE, Davis AS, Dalling JW (2015) Do soil microbes and abrasion by soil particles influence persistence and loss of physical dormancy in seeds of tropical pioneers? Front Plant Sci 5:799. doi:10.3389/fpls.2014.00799

    Article  PubMed  PubMed Central  Google Scholar 

  • Zimmerman JK, Wright JS, Calderón O, Pagan MA, Paton S (2007) Flowering and fruiting phenologies of seasonal and aseasonal Neotropical forests: the role of annual changes in irradiance. J Trop Ecol 23:231–251. doi:10.1017/S0266467406003890

    Article  Google Scholar 

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Acknowledgements

We thank the Smithsonian Tropical Research Institute (STRI) for providing facilities, logistical support, and permission to conduct the project. We thank the University of Illinois Integrative Graduate Education and Research Traineeship-Vertically Integrated Training with Genomics training fellowship from the National Science Foundation (NSF) Department of Graduate Education Grant-1069157, NSF Department of Environmental Biology Grant-1120205 to JWD, and the Smithsonian Tropical Research Institute-Butler University internship program for funding. We also thank two anonymous reviewers for their comments.

Funding

This study was funded by University of Illinois Integrative Graduate Education and Research Traineeship-Vertically Integrated Training with Genomics training fellowship from the National Science Foundation (NSF) Department of Graduate Education Grant-1069157, NSF Department of Environmental Biology Grant-1120205 to JWD, and the Smithsonian Tropical Research Institute-Butler University internship program.

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Correspondence to Selina A. Ruzi.

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Communicated by Miguel Franco.

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Ruzi, S.A., Roche, D.P., Zalamea, PC. et al. Species identity influences secondary removal of seeds of Neotropical pioneer tree species. Plant Ecol 218, 983–995 (2017). https://doi.org/10.1007/s11258-017-0745-7

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