Plant Ecol DOI 10.1007/s11258-017-0745-7 Species identity influences secondary removal of seeds of Neotropical pioneer tree species Selina A. Ruzi . Daniel P. Roche . Paul-Camilo Zalamea . Abigail C. Robison . James W. Dalling Received: 31 March 2017 / Accepted: 24 June 2017 Ó Springer Science+Business Media B.V. 2017 Abstract Primary dispersal agents move seeds from species identity, primary dispersal mode (animal or the maternal plant to the soil surface where they are wind), dormancy type, seed mass, and capacity to persist often moved again by secondary dispersal agents. in the seed bank were correlated with removal rate. We However, the extent to which different species in the also investigated whether season (dry or wet) influences same location experience secondary dispersal is often removal from the soil surface. In general, both super- unknown despite the importance of this mechanism for ficial and buried seeds were highly mobile. We found an determining recruitment opportunities and conse- effect of primary dispersal mode and dormancy type on quently community structure. Here we examine the removal rates both on (12 species) and beneath the soil secondary removal rates of 12 Neotropical pioneer surface (six species). However, this pattern was largely species placed either on or 2 cm below the soil surface at driven by species identity. Season had no influence on five locations in lowland tropical forest on Barro seed removal rates from the soil surface. The dispersal of Colorado Island, Panama. We investigated whether small-seeded pioneer species is highly species depen- dent, indicating that generalizations made using broader categories, such as primary dispersal mode or dormancy Communicated by Miguel Franco. type, do not accurately describe the observed patterns hindering our understanding of community assembly Electronic supplementary material The online version of within even a single functional group of plants. this article (doi:10.1007/s11258-017-0745-7) contains supple- mentary material, which is available to authorized users. S. A. Ruzi (&) A. C. Robison Program in Ecology, Evolution, and Conservation Department of Biology, Butler University, 4600 Sunset Biology, University of Illinois, Urbana-Champaign, 515 Avenue, Indianapolis, IN 46208, USA Morrill Hall, 505 South Goodwin Avenue, Urbana, IL 61801, USA J. W. Dalling Department of Plant Biology, University of Illinois, e-mail: [email protected] Urbana-Champaign, 265 Morrill Hall, 505 South D. P. Roche Goodwin Avenue, Urbana, IL 61801, USA Department of Biological Sciences, Purdue University, West Lafayette, 915 West State Street, West Lafayette, IN 47907, USA P.-C. Zalamea Á J. W. Dalling Smithsonian Tropical Research Institute, Apartado, 0843-03092, Balboa, Ancon, Republic of Panama 123 Plant Ecol Keywords Barro Colorado Island Á Seed dispersal Á additional movement events (see Vander Wall et al. Plant communities Á Soil seed bank Á Forest 2005) resulting in secondary dispersal or predation. regeneration The activity of these secondary removal agents ultimately influences how many seeds are available for germination and can be important at structuring plant communities (Chambers and MacMahon 1994). Introduction Potential benefits of secondary dispersal include protection from predation, reduction of competition Plants face a wide variety of obstacles to the recruit- with conspecifics, and movement to microsites bene- ment of new individuals into the population. Plants are ficial for germination (Vander Wall and Longland limited not only by the number of seeds that they can 2004). Overall, whether secondary dispersal activity is produce (‘source limitation’), but also whether those beneficial or not to seeds is context dependent and seeds escape pre-dispersal predation, survive disper- relies on many different factors (Chambers and sal, and reach a suitable microsite for germination, MacMahon 1994). For example, secondary dispersal while surviving to emergence and establishment often comes with a price: many secondary dispersers (Nathan and Muller-Landau 2000). In tropical forests, also consume some of the seeds they remove (Vander some pioneer tree species produce sufficient numbers Wall and Longland 2004). However, the benefits of small seeds to overcome source limitation (Dalling accrued by the seeds that survive may outweigh the et al. 2002), yet only a small fraction of those seeds loss of seeds due to predation (Chambers and reach microsites suitable for onward growth. This MacMahon 1994). indicates that they are either limited in their ability to Incorporation of seeds into the soil seed bank effectively disperse seeds (‘dispersal limitation’) or (defined as the viable seeds present both on the soil that constraints imposed by reducing source limitation surface and in the soil profile; Long et al. 2015)isa negatively affect the range of sites favorable for critical part of dispersal activities. The seed bank is seedling establishment (Dalling and Hubbell 2002). often referred to as a safe site for seeds; however, the Dispersal away from the parent plant or con- seed bank is dynamic with many factors including specifics is important for seedling recruitment in plant seed, species, and environmental characteristics influ- communities, both to increase the probability of encing whether seeds persist or exit the seed bank, encountering suitable microsites and to avoid preda- either through decay or germination (reviewed in tors and pathogens that act in a density-dependent Long et al. 2015). Seed characteristics, such as manner (Janzen 1970; Connell 1971; Comita and dormancy type, can influence when seeds are able to Hubbell 2009; Mangan et al. 2010; Bagchi et al. 2014). respond to the environmental cues they require for In most forests, treefall gaps provide the microsites germination, while seed size, seed coat, and the required for germination and establishment of pioneer presence of appendages or exudates can influence the trees (Swaine and Whitmore 1988; Hubbell et al. vulnerability of seeds to predators and pathogens 1999). However, treefall gaps are uncommon, they (Long et al. 2015). For example, some physically exist for short periods of time, and their spatial dormant seeds may avoid predation while in the seed location and time of formation are fairly unpre- bank because their impermeable seed coat reduces the dictable (Young and Hubbell 1991; Schnitzer et al. diffusion of olfactory cues used by rodents to detect 2000). As a consequence, pioneer tree species are them (Paulsen et al. 2013). Spatial and temporal under selection to disperse seeds widely, and/or for variation in environmental conditions associated with their seeds to persist for decades in the seed bank climate seasonality and microsite heterogeneity can (Dalling and Brown 2009). also influence whether a seed is likely to persist (Long Primary dispersal, the initial movement of seeds et al. 2015), and these conditions may be altered away from the parent tree (Nathan and Muller-Landau through additional dispersal events into new micro- 2000), can be accomplished through a variety of sites. While secondary dispersal of seeds into the soil means, including animal, wind, gravity, and ballistic profile is frequently reported, it is unknown whether dispersal (Seidler and Plotkin 2006). After primary seeds experience the same potential for further move- dispersal has occurred, seeds may experience ment both at the soil surface and in the topsoil. 123 Plant Ecol Table 1 Soil and flora characteristics of sampling areas (plots) within Barro Colorado Island Plot/location name Forest age (years) Soil type/soil form/parent material 25 Ha 80–120 Marron/brown fine loam/Andesite Armour 80–140 AVA/red light clay/Andesite Drayton 400? Fairchild/red light clay/Bohio Pearson 400? Standley/brown fine loam/Bohio Zetek 400? Marron/brown fine loam/Andesite Forest age is approximated from classifications mapped in Mascaro et al. (2011) that were generated based on land-use data obtained from Enders (1935). Information on soil type, soil form, and parent material is from Baillie et al. (2006) In this study, we examine whether secondary Panama. BCI supports seasonal semi-deciduous forest removal rates of seeds vary among pioneer species at an average elevation of 70 m above sea level with found in lowland forest of central Panama. For 12 tree an annual rainfall of 2600 mm (Windsor 1990). The species, we tested whether the individual species forest experiences a pronounced dry season starting identity, season, primary dispersal mode (animal or late December or early January and continuing until wind), and dormancy type (physical, physiological, or late April or early May (Windsor 1990). Seed removal quiescent) influenced the rate of seed removal from the experiments were located at five sites at least 350 m forest floor. We also examined if two seed traits, seed apart, and at least 20 m from conspecific trees, within mass and seed persistence in the soil seed bank either old-growth or secondary forest and representing (defined here as the proportion of viable seeds that a range of soil types (Zalamea et al. 2015; Table 1). survive 18 months of burial enclosed in mesh bags), We selected 12 pioneer species found on BCI that were correlated with removal rates. For six species, we vary in seed size, primary dispersal mode, dormancy further tested whether seed removal occurred once type, and seed persistence capacity for experiments seeds were incorporated into the top 2 cm of soil. We during the dry and wet seasons (Table 2). The wet tracked the fate of 3000 seeds to test the following season experiments also included artificial seeds alternative, but not mutually exclusive, hypotheses: (30.5 ± 0.038 mg, mean ± SE, mass silica beads). (1) primary dispersal mode would serve as a strong Ripe fruits were collected directly from the parent tree predictor of secondary dispersal rates, predicting that or from beneath the crown and then cleaned to remove animal-dispersed seeds would experience higher seeds from fruit pulp (animal-dispersed species except above-ground removal rates than wind-dispersed Zanthoxylum ekmanii (Urb.) Alain) or kapok-like seeds (Fornara and Dalling 2005a); (2) seeds with fibers (Cochlospermum vitifolium Willd.