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Species‐Specific Variation in Germination Rates Contributes To Received: 7 October 2019 | Accepted: 8 April 2020 DOI: 10.1111/1365-2745.13408 RESEARCH ARTICLE Species-specific variation in germination rates contributes to spatial coexistence more than adult plant water use in four closely related annual flowering plants Aubrie R. M. James1,2 | Timothy E. Burnette3,4 | Jasmine Mack1 | David E. James5 | Vincent M. Eckhart3 | Monica A. Geber1 1Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA Abstract 2School of Biological Sciences, University of 1. Spatial partitioning is a classic hypothesis to explain plant species coexistence, but Queensland, Brisbane, Qld, Australia evidence linking local environmental variation to spatial sorting, demography and 3Department of Biology, Grinnell College, Grinnell, IA, USA species' traits is sparse. If co-occurring species' performance is optimized differ- 4Department of Ecology and Evolutionary ently along environmental gradients because of trait variation, then spatial varia- Biology, University of Kansas, Lawrence, tion might facilitate coexistence. KS, USA 2. We used a system of four naturally co-occurring species of Clarkia (Onagraceae) to 5National Lab for Agriculture and the Environment, USDA/ARS, Ames, IA, USA ask whether distribution patchiness corresponds to variation in two environmen- tal variables that contribute to hydrological variation. We then reciprocally sowed Correspondence Aubrie R. M. James Clarkia into each patch type and measured demographic rates in the absence of Email: [email protected] congeneric competition. Species sorted in patches along one or both gradients, Funding information and in three of the four species, germination rate in the ‘home’ patch was higher National Science Foundation, Grant/Award than all other patches. Number: DEB-1256288 and DEB-1256316 3. Spatially variable germination resulted in the same three species exhibiting the Handling Editor: Shurong Zhou highest population growth rates in their home patches. 4. Species' trait values related to plant water use, as well as indicators of water stress in home patches, differed among species and corresponded to home patch attrib- utes. However, post-germination survival did not vary among species or between patch types, and fecundity did not vary spatially. 5. Synthesis. Our research demonstrates the likelihood that within-community spa- tial heterogeneity affects plant species coexistence, and presents novel evidence that differential performance in space is explained by what happens in the germi- nation stage. Despite the seemingly obvious link between adult plant water-use and variation in the environment, our results distinguish the germination stage as important for spatially variable population performance. KEYWORDS demographic performance, diversity, germination, interspecific trait variation, plant coexistence, plant communities, spatial heterogeneity Journal of Ecology. 2020;00:1–17. wileyonlinelibrary.com/journal/jec © 2020 British Ecological Society | 1 2 | Journal of Ecology JAMES ET AL. 1 | INTRODUCTION consequences on plants in the absence of competition (Adler et al., 2013; Chesson et al., 2004). Studies of plant communities have Of persistent interest in studies of community diversity is how en- demonstrated the relationship between water-use traits, spatial dis- vironmental variation can give rise to species coexistence. In the- tribution and variation, but often focus on dramatic or large-scale ory, spatial heterogeneity can foster coexistence among species in topographic variation in the environment (Dawson, 1990; Lamont, different patches in a community (Pacala & Tilman, 1994), provided Enright, & Bergl, 1989; Richards, Stock, & Cowling, 1995; but see that each species' performance is differentially optimized along Lanuza, Bartomeus, & Godoy, 2018). Studies of finer-scale envi- some gradient (or gradients) in the environment (Hart, Usinowicz, ronmental variation (i.e. within communities) have shown that wa- & Levine, 2017; Tilman & Pacala, 1993). In plant communities, en- ter-use physiology is tightly related to plant performance (Chesson vironmental variation is classically an important mechanism for et al., 2004; Rosenthal, Ludwig, & Donovan, 2005) and even coex- diversity maintenance, and co-occurring plants often exhibit differ- istence (Angert, Huxman, Barron-Gafford, Gerst, & Venable, 2007; ential performance and success according to spatial variation in hy- Angert, Huxman, Chesson, & Venable, 2009; Gremer et al., 2013) in drology. One way to frame the relationship between hydrology and herbaceous plant communities, but are not explicitly spatial—they plant coexistence is hydrological niche segregation (or HNS: Araya do not focus on how variation in space might contribute to varia- et al., 2011; Silvertown, Araya, & Gowing, 2015). Studies of plant tion in performance and coexistence. Still other studies have shown HNS suggest three main responses to hydrological variation in space that plant occurrence or abundance and spatial variation in soil or or time that can affect coexistence: spatial partitioning, which al- hydrology are related to each other (Reynolds, Hungate, Chapin, & lows for source–sink dynamics, where species mutually persist in an D'Antonio, 1997; Silvertown, Dodd, Gowing, & Mountford, 1999), environment due to sources in different patches; water partitioning; but do not investigate the role of plants' water-use traits in these and/or the temporal storage effect. relationships. All three components of HNS implicate variation in plant In this work, we describe the relationship of spatial aggregation water-use traits as a means to minimize interspecific competition, but with two axes of environmental variation—soil texture and proxim- a critical line of evidence to establish trait-based spatial coexistence ity to woody plants—in four herbaceous, sympatric plant species in is to link environmental gradients, plant performance and interspe- the genus Clarkia (family Onagraceae; C. cylindrica ssp. clavicarpa cific trait variation to each other (Adler, Fajardo, Kleinhesselink, & (Jeps.) Lewis & Lewis, C. speciosa ssp. polyantha Lewis & Lewis, Kraft, 2013). In the case of plant communities, spatial coexistence C. unguiculata Lindl., C. xantiana ssp. xantiana A. Gray) in the Kern may be relevant for diversity maintenance if (a) the environment is River Canyon (Kern County, CA, USA; from here: C. cylindrica (C), spatially variable, (b) such variation corresponds to where species C. speciosa (S), C. unguiculata (U), C. xantiana (X)). All four Clarkia co- occur in communities and (c) species performance is highest where flower at the end of the growing season in southern California, after they are most common. If these three criteria are met, then either or many other annuals, have senesced. Within this period, species have both of the major spatial coexistence mechanisms, the spatial storage been observed to flower either early in the season (C. cylindrica and effect (i.e. environment-competition covariance, ∆I) and growth-den- C. unguiculata; Eisen & Geber, 2018) or later in the season (C. speciosa sity covariance (∆K) may affect diversity maintenance (Barabás, and C. xantiana). D’Andrea, & Stump, 2018; Chesson, 2000; Ellner, Snyder, Adler, The first axis of environmental variation we measure is in & Hooker, 2019; Snyder & Chesson, 2004). For both mechanisms, edaphic conditions: soil texture and penetration resistance. Soil tex- demonstrating that spatial partitioning can affect plant coexistence ture is an important aspect for plant water relations; in arid environ- requires measures of species' population growth rates in response ments especially, soil penetration resistance (soil hardness) increases to variation in the environment in the absence of competition. This as soils become finer (Eckhart et al., 2010; To & Kay, 2005), which is because each mechanism is defined in terms of covariance: the can lead to water stress for plants by decreasing water infiltration covariance of population performance with either competition or and soil aeration (Alizai & Hulbert, 1970; Barnes & Harrison, 1982; density. Because of this, accurate estimates of how spatial storage Kinraide, 1984; Sperry & Hacke, 2002). There is some evidence that or growth-density covariance contribute to coexistence first require plant occurrence corresponds to soil textural gradients, including measures of population performance along environmental gradients in the Clarkia system (Beals & Cope, 1964; Eckhart et al., 2017). As independently of competition or density. To further understand the with many Clarkia, these four Clarkia co-occur in multi-species com- specific role of water-use traits in spatial coexistence (as for the role munities more often than they occur alone in their range of overlap of any trait; Adler et al., 2013; Chesson, 2000), we must also demon- (Eisen & Geber, 2018; Lewis & Lewis, 1955). Previous research in strate that plant demographic performance in the absence of com- this system suggests that soil texture is an important axis of varia- petition varies along environmental gradients that (a) are meaningful tion for Clarkia spatial coexistence. In a laboratory environment, the for plants' water economies and (b) correspond to plant water-use two late-flowering species differed in their performance in response traits (Adler et al., 2013; Chesson, 2000). to soil texture, where C. speciosa germinated better in fine-grained Though the literature is replete with examples of how plants soils and
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