Opposing Effects of Floral Visitors and Soil Conditions on the Determinants

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Opposing Effects of Floral Visitors and Soil Conditions on the Determinants Postprint of: Ecology Letters 21(6): 865-874 (2018) 1 Opposing effects of floral visitors and soil conditions on 2 the determinants of competitive outcomes maintain 3 species diversity in heterogeneous landscapes 4 5 Jose B. Lanuza, 1 Ignasi Bartomeus, 2 Oscar Godoy 3* 6 1School of Environmental and Rural Science, University of New England, Armidale, 2350, NSW 7 Australia 8 2 Estacion Biologica de Doñana (EBD-CSIC), C/Americo Vespucio 26, E-41092 Sevilla, Spain. 9 3Instituto de Recursos Naturales y de Agrobiología de Sevilla (IRNAS-CSIC), Avda. Reina 10 Mercedes 10, E -41012 Sevilla, Spain. 11 * corresponding author: [email protected] +34 954 624 711 12 13 Statement of authorship : I.B. and O.G. designed the study. J.B.L and O.G. conducted 14 fieldwork. All authors analysed the results, and J.B.L and O.G. wrote the manuscript 15 with substantial contributions from I.B. 16 Data accesibility statement : Raw data will be uploaded in Dryad upon acceptance. 17 Abbreviated form of title : Species coexistence and multitrophic interactions . 18 Keywords : demography, coexistence, community assembly, fitness, multitrophic 19 interactions, mutualism, niche, pollinators, salinity, spatial structure. 20 Type of article : Letters. 21 Number of words : abstract (150); main text considering equations (4985). 22 Nuber of references : 50. 23 Number of figures, tables and text boxes : figures (4); tables (1); no text boxes. 1 24 25 Abstract 26 Theory argues that both soil conditions and aboveground trophic interactions have 27 equivalent potential to limit or promote plant diversity. However, it remains 28 unexplored how they jointly modify the niche differences stabilising species 29 coexistence and the average fitness differences driving competitive dominance. We 30 conducted a field study in Mediterranean annual grasslands to parameterise 31 population models of six competing plant species. Spatially explicit floral visitor 32 assemblages and soil salinity variation were characterized for each species. Both 33 floral visitors and soil salinity modified species population dynamics via direct 34 changes in seed production and indirect changes in competitive responses. Although 35 the magnitude and sign of these changes were species-specific, floral visitors 36 promoted coexistence at neighbourhood scales while soil salinity did so over larger 37 scales by changing the superior competito rs’identity.Ourresultsshowhowbelow 38 and aboveground interactions maintain diversity in heterogeneous landscapes 39 through their opposing effects on the determinants of competitive outcomes. 40 41 Introduction 42 One central aim in ecology is understanding how plant species diversity is 43 maintained. Extensive empirical work has documented that variation in soil 44 conditions and multitrophic interactions modulate key processes of plant 45 population dynamics. For instance, plant offspring and the strength of competition 46 depend on the combined species' ability to deplete shared limiting soil resources 47 (Tilman 1982) and to cope with stressful soil conditions such as the amount of salt 48 (Bertness & Shumway 1993; Crain et al. 2004). Likewise, mutualistic and 49 antagonistic biotic interactions with herbivores (Hulme 1996; Olff & Ritchie 1998), 50 soil biota (Bever 2003; Bennett et al. 2017; Teste et al. 2017), pathogens (Mordecai 51 2015; Parker et al. 2015), and floral visitors (Bastolla et al. 2009; Carvalheiro et al. 52 2014; Weber & Strauss 2016) can profoundly impact plant performance. It is 53 obvious that outcrossing plants directly depend on their mutualistic floral visitors to 54 maximize their reproductive success (Morris et al. 2010; Ollerton et al. 2011). 55 Subtler is the fact that floral visitors indirectly mediate competition among plants 56 through a wide variety of density-dependent processes including variation in the 57 number and diversity of floral visitors as well as heterospecific pollen deposition 58 (Moeller 2004; Arceo-Gómez & Ashman 2011; Runquist & Stanton 2013). 59 Despite the fact that variation in soil conditions and multitrophic biotic interactions 60 occurs simultaneously in nature, evaluations of their effects on modulating the 61 strength and sign of plant competition have been explored individually. It remains 2 62 unknown how these drivers can jointly maintain plant diversity. Theoretical work 63 has advocated that both types of interactions should be viewed symmetrically as 64 they have equivalent potential to limit or promote diversity (Chesson & Kuang 65 2008). Although empirical tests of this prediction have remained so far elusive, we 66 can progress by framing our research within recent advances of coexistence theory 67 (Chesson 2000), and by learning from prior work applying these theoretical 68 advances to multitrophic antagonistic interactions, mainly predators and pathogens 69 (Chesson & Kuang 2008; Kuang & Chesson 2010; Stump & Chesson 2017). 70 ccordingtoChesson’s(2000)framework,bothsoilconditionsandfloralvisitors 71 can promote the stabilising niche differences that favour plant coexistence, which 72 occur when intraspecific competitive interactions exceed interspecific competition, 73 and the average fitness differences that favour competitive exclusion and determine 74 the competitive winner in the absence of niche differences. Ecologists have paid 75 much more attention to the relationship of these two factors with fitness differences 76 (e.g. soil conditions (Tilman 1982; Casper & Jackson 1997; Rees 2013); floral 77 visitors (Herrera 2000; Waites & Ågren 2004; Arceo-Gómez & Ashman 2011)) than 78 with niche differences (Silvertown 2004; Levine & HilleRisLambers 2009) and this 79 is particularly evident for floral visitors (Pauw 2013). Most likely both drivers 80 modify niche and fitness differences simultaneously, yet the extent of such 81 modifications is poorly understood. Therefore, a rigorous evaluation of the 82 equivalent potential of soil conditions and floral visitors on maintaining plant 83 diversity can only be done by a mechanistic understanding of how these two types 84 of interactions relatively modify the determinants of competitive outcomes. 85 When relating theory to field experiments, it is important to consider two critical 86 aspects. One is selecting ecological systems that are relatively easy to observe. For 87 example, recent work in Mediterranean annual grassland (Godoy & Levine 2014) 88 has described how niche and fitness differences influence species' population 89 dynamics. Some of these grasslands are subjected to strong variation in soil salinity, 90 which negatively correlates with soil fertility (Olff & Ritchie 1998; Hu & 91 Schmidhalter 2005). Moreover, floral visitor assemblages in these Mediterranean 92 environments are particularly interesting because they are composed of an array of 93 insects including solitary bees, hover flies, beetles, and butterflies. While some of 94 these floral visitor types act as true mutualisms (Pauw 2013), others rob plant 95 nectar or pollen or damage flowers (Morris et al. 2003). The second aspect is that 96 these drivers of plant competition tend to show spatial structure (Tilman 1994; 97 Weber & Strauss 2016). Coexistence theory predicts that plant diversity can be 98 maintained at the neighbourhood scale when species niche differences overcome 99 fitness differences. This can occur when either plant competitor equalises its fitness 100 differences, increases its niche differences, or a combination of both. If not, the 101 superior competitor excludes the inferior species (Chesson 2000). However, 102 competitive exclusion outcomes can also maintain plant diversity at larger scales if 103 the spatial structure of variation in soil salinity and floral visitors change the 104 identity of the superior competitor across locations. This latter process might be the 3 105 cause of reported turnover patterns of species and functional attributes across soil 106 salinity gradients (Bertness 1991; Pavoine et al. 2011). 107 Here, we considered three layers to test how the belowground environmental 108 conditions (i.e. soil conditions) and the aboveground trophic interactions (i.e. floral 109 visitors) influence coexistence of the middle layers (i.e. plant species). We 110 specifically focus on three questions: (1) How do soil salinity and floral visitors 111 modify species' population dynamics via direct changes in per capita seed 112 production and indirect changes in species' responses to competitive interactions? 113 (2) Do these direct and indirect effects modify niche and fitness differences between 114 plant species?, and finally, (3) At which spatial scale are these modifications on the 115 determinants of competitive outcomes limiting or promoting diversity? 116 We answered these three questions by first parameterizing a general plant 117 competition model from which the stabilising niche differences and average fitness 118 differences were quantified. To parameterise these models of pairwise competition 119 between six annual native grassland species, we quantified their vital rates and 120 competition coefficients in field plots relating seed production of focal individuals to 121 a density gradient of numerous different competitors. We then assessed how 122 seasonal and spatial variation in the number of floral visits and in soil salinity 123 changes species fecundity and their responses to competition (Question 1). Once, 124 the model was parameterised, we estimated niche and fitness differences with and 125 without considering
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