Life on a leaf: The development of spatial structure in epiphyll communities

Biotic interactions play an important role in maintaining biodiversity (Bascompte & Jordano, 2007; Muscarella et al., 2018), and neighbour are among the main forces shaping plant communities (Gavini 2019; Grant 2014). These one of spatial patterns, analysing such patterns can be a powerful approach to deduce processes determining community structure (Alados 2017; Dale, 1999). Such (e.g. dispersal, biotic interactions) as well they create traits, configurations) both contribute aspects ecology (Rees 2001). Theoretical models distributions ecological range from strongly deterministic niche-based purely stochastic neutral theories (Alonso 2006; Hubbell, Stochastic tend lead random various non-random patterns. thus provide signature underlying processes. In most ecosystems, niche shape biological Schei 2012; Siepielski 2010; Stokes Archer, Weiher 2011), but relative importance will vary between ecosystems successional stages. It has been suggested that chance propagule arrival) dominant young communities, while become more during late stages succession (Måren 2018). As result, pattern (i.e. position different species each other) early stage should older Tropical rainforest have highest world-wide (Condit 2002). Traditionally, research addressing tropical forest focused on trees, highlighting their mostly aggregated at level 2000; Felix 2015; McFadden 2019). An (here: individuals focal or closely related grow closer together than expected by chance) indicate positive individuals, limited dispersal hidden environmental heterogeneity, also change with time. Some studies show woody (neutral) segregated along (Fibich 2016; Velázquez Thereby, negative interactions, competition, which increase succession. One less conspicuous elements forests is miniature inhabiting leaves vascular plants, epiphylls. Epiphyll consist algae, fungi, bacteria, lichens liverworts growing surface leaves. Despite small size, epiphylls functions forests, where nitrogen fixation (Zhou 2009), protect host herbivores (Coley 1993) serve habitat for, for example, protozoa (Barthlott 2000) bioindicators (Lücking, 1997). The form interesting model study changes (Gilbert 1997) 1993; Conran Rogers, 1983), because short life span, huge replication clear demarcation on. organisms complex relatively fast, even within 1 year 1997; Lücking, Marino Salazar Allen, 1992), contrast may take several decades (Wright 2003). epiphyll succession, primary assemblages recognized (Conran 1983; 1995; Sierra driving compositional unknown. Epiphyllous sometimes overgrow (never other way around, Coley 1993), whether this constitutes interaction uncertain, it does not appear replacement (Mežaka Instead, reproductive traits seem order appearance (Sierra However, although some basic information development exists, potential within-leaf understand remains unexplored. stress-gradient hypothesis (Bertness Callaway, 1994) postulates predominant exposed harsher conditions, typical under mild conditions. This corroborated wide (Casalini Bisigato, 2018; Kjær facilitation probably mechanism poikilohydric whose water status follows moisture conditions; Barkman, 1958; Green Lange, Rydin, Rydin Barber, 2001), has, our knowledge, evaluated communities. According hypothesis, drier environments, gaps, larger role, neighbours (in particular liverworts) help maintain longer. contrast, dark forest, interior competition resources, light, dominate. differences would result only compositions 1997, 1999), We consider drought stress factor defining gradient, type could indeed aggregation. Spatial aggregation occur functional groups. A detailed analysis associations all groups allow testing thereby increasing understanding what shapes leaf. present study, we characterized four (algae, 12 months how through time, forest-gap closed-forest sites. tested following hypotheses: (1) Young structure, shaped (propagule arrival, colonization); (2) With leaf ageing, epiphylls, groups, increasingly leading (indicating segregation interactions); (3) accordance (facilitation), common lighter conditions gaps dry season, (competition) understorey sites wet season. By these hypotheses, aim elucidate tree shrub leaves, add unique example conducted lowland Barro Colorado Island (BCI) Panama (Appendix S1). Monthly rainfall averages 41 mm season (mid-December April) 257 (May December). Temperature little throughout year, average daytime temperature 32℃ night-time 23℃ (Paton, Inside recorded daily means 25–26℃ mean minima 22–23℃ maxima 27–33℃, depending site studied tree-sapling two microsite types: (representing light environment) closed (a darker wetter environment), six per type. On average, air gap became warmer day, though measurements showed high variability pairs no opposite pattern. Dry maximum temperatures were generally higher (by ~1 2℃) minimum humidity values consistently lower ~1% 25%) those types At S2), randomly selected five healthy hosts height 1.2 m one, three host, amounting 30 represented 18 S2). very tree- shrub-species diversity composition varied sites, was possible select enough replications. variety likely contributed variation results, so large sample size needed detect general considered independent sample, containing its community. mapped locations macroscopically visible differentiating groups—algae, liverworts. differ evolutionary histories, mechanisms, history morphologies, effects microenvironment due growth forms, water-holding capacities production allelopathic compounds). maps based digital photographs (an shown Appendix S3) taken Canon EOS Rebel T1i camera survey times (t = 0, 6, 9 months) December 2016 until 2017. All similar angle distance kept flat possible. Each patch manually digitized using Arcmap 10.5 (Esri, USA, Redlands). determined centroid define points used further analysis. expressed point density group number cm2 (60 leaf). To changed time relationship according microsite, applied GLMMs binomial lme4 R package (Bates 2015). statistical performed R, Version 3.5.1 (R Core Team, included (N 12) factor. fitted group. significance variable Anova function car (Fox Weisberg, 2011). distribution (SPP) (Wiegand Moloney, 2014) spatstat (Baddeley analysed scale, 10 Assuming represents homogeneous environment, Ripley's K-function (K-function). estimates certain radius acceptance interval (envelope) around (grey area Figure 1) encompasses indicating significantly calculated envelopes Monte Carlo simulations, 99 simulations 513 steps (Abellanas Pérez-Moreno, Baddeley 2015) data (empirical K-functions) against Loosmore Ford (2006) goodness-of-fit test (LF.gof function) ecespa (De la Cruz, 2008). empirical cumulative located point, corrected edge standardized compare areas (we so-called isotropic correction, suitable irregular Apart assuming complete randomness (CSR), null implies independence (one influence leaf) marked SPP aggregated, segregated. If (random), (clustered), if fewer expected, (overdispersed, 1; divided into parts, addressing: unmarked attributes except position); dynamics group, labelled time; For part 1, simple K-functions, parts 2 3, cross-type K-functions first aimed describe ageing differs (aggregated, segregated) ways: (does any K-function?), 0.5 cm 1.5 cm. pair frequencies differed microsites, Pearson's Chi-squared tests (Agresti, second observe dynamic are, (Figure 2). Here interpretation observing time: indicates static (low dynamics, stay same location), stronger locations. intervals 0 t 6; 6 9; leaf, many sufficient analysed. frequency low (aggregated patterns), medium pattern) (more tests. test, together. third analysis, this, infer microsites. method within-group SPPs over did Within found, found patterns—aggregated, associations. Although appeared significant, algae lichens. positions quite dynamic, especially fungi. Our results increased fungi (Appendices S4 S5). liverworts, densities There significant graphs suggest liverwort distances 3) when considering across radii S6). similar, here only. microsites S7), therefore combined 3). lichens, decreased expense surveys 6), stayed same, tended S8, lack thereof, indicated covered exceptional S8B), having (except lichens), about 50–50 (with tending randomness; S8A). S10; 4). Leaves low, middle (Pearson's χ2 13.57, p < 0.05) groups: Like S8), combined. between-group 5). association S9; 5), percentage showing last Other percentages S9). composed observed few shift development, remained Even dramatically evidence changing highly Finally, do support hypothesis. partly consistent hypotheses display lichen towards arrival colonization determine patches, seen seedlings (Bengtsson 1994; Chesson Warner, 1981; Sale, 1977). abundance dominance (Hubbell, 2001; Zobel, later vegetation grassland (Felinks Wiegand, 2008) reasons difference lie specificities fast reproduction adaptation short-term substrate, short-distance spores vegetative propagules) habits radial thalli), space pre-emption competitive replacement, Indeed previous accumulation turnover took place Still, seemed unimportant, current dynamic. frequently, speak pre-emption. original given up, directional growth. Fungi dynamics: nearly explained turning start symbiosis (Sanders 2002), easily move hyphae, centroids. fungal germinate clumps, autotropism common, germ tubes away (Carlile initial locations—though extent While throughout, great majority either facilitation, clustered (epiphyll propagules land individually clusters 2002)), (Lücking Bernecker-Lücking, shared preferences (Gjerde 2014; Svenning, meaning sensitivity, restricting them moister surface, position, features veins) epiphylls—this latter supported however, algae. age, establishment local rather long-distance arrivals. Reproductive structures develop find biodiversity, appears degree scale dependent (Götzenberger Matthews Whittaker, Munoz Huneman, 2016). smaller scales, heterogeneity decline, contribution events terms composition, increases. get neutrally structured environments (Chase, Shi include surfaces. factors (Benot 2013). small-scale (described only) 2019), stochasticity events. strong structuring community, weak indications like develop. interpreted (D'Amen brought differing preferences. oldest newly developed disappearance free-living whenever formed new symbioses 2008; pers. obs.). Also, thalli known encircle destroy phycobiont Segregation least just pattern, repulsion ability without necessarily causing experiencing damage layering. Negative epiphytes Europe attributed mechanical destruction, suffocation, chemical action (Barkman, 1958). grasslands bryophyte (Löbel 2006) overgrowing directions terrestrial (During van Tooren, 1990). another temperate concluded bryophytes hardly occurred 2009). true rainforest. made caution, compared emerge space, increases (Crowley 2005). Most still had free expansion times, frequently patches touching other, particularly surveys. limitation centroids) contact zones explicitly. cover whole reality aggregation, centroids segregation. observed. Further explore polygons 2006). classical 1994). explanation gradients drought, shade) cause gradients, always (Maestre Qi reason ‘stress’ often poorly defined. gradient usually contain stress. Experimental plants shows typically habitats wind), noticeable (López 2013; reduced neighbours. understoreys, shade major factor, reducing survival (Körner, 2003), unlikely promote clustering interactions. Another absence response high-stress tolerance, making stressful soil crusts (Bowker 2010). summary, becoming frequent Associations additionally segregated, spatially random—with Segregated (aggregated) driven (segregated patterns) facilitative patterns). better processes, recommend individual temporal taxonomic resolution experimental studies. providing insights presents basis balance financially European Union Framework Programme Research Innovation Horizon 2020, Marie Skłodowska-Curie Global Fellowship project Nr. 708585-EPIDYN. authors grateful Joe Wright discussions references, Milton Solano helping ArcMap. They thankful Roni Saenz, Freddy Nay, Lilisbeth Rodriguez, Yessenia Guadalupe, Marjorie Vargas Alina Ortega field assistance José Gudiño laboratory. fieldwork done framework Smithsonian Institute specific permits necessary. declare conflict interest. A.M. M.Y.B. conceived research; collected N.S.A.; G.M.-L.; led writing manuscript critically revised agree publication. Data available Dryad Digital Repository https://doi.org/10.5061/dryad.0cfxpnw3v 2021). Please note: publisher responsible content functionality supporting supplied authors. Any queries (other missing content) directed corresponding author article.