DOI: 10.5061/dryad.79cnp5j11
title: Does a history of population co-occurrence predict plant performance, community productivity, or invasion resistance?

description: A history of species co-occurrence in plant communities is hypothesized to
 lead to greater niche differentiation, more efficient resource
 partitioning, and more productive, resistant communities as a result of
 evolution in response to biotic interactions. A similar question can be
 asked of co-occurring populations: do individual species or community
 responses differ when communities are founded with plants sharing a
 history of population co-occurrence (sympatric) or originating from
 different locations (allopatric)? Using shrub, grass, and forb species
 from six locations in the western Great Basin, USA, we compared
 establishment, productivity, reproduction, phenology, and resistance to
 invaders for experimental communities with either sympatric or allopatric
 population associations. Each community type was planted with six taxa in
 outdoor mesocosms, measured over three growing seasons, and invaded with
 the annual grass Bromus tectorum in the final season. For most
 populations, the allopatric or sympatric status of neighbors was not
 important. However, in some cases, it was beneficial for some species from
 some locations to be planted with allopatric neighbors, while others
 benefited from sympatric neighbors, and some of these responses had large
 effects. For instance, the Elymus population that benefited the most from
 allopatry grew 50% larger with allopatric neighbors than in single origin
 mesocosms. This response affected invasion resistance, as B. tectorum
 biomass was strongly affected by productivity and phenology of Elymus
 spp., as well as Poa secunda. Our results demonstrate that while community
 composition can affect plant performance in semi-arid plant communities,
 assembling communities from sympatric populations is not sufficient to
 ensure high productivity and invasion resistance. Instead, we observed an
 idiosyncratic interaction between sampling effects and evolutionary
 history, with the potential for seed source of individual populations to
 have community-level effects.
description: Target species were selected after conducting plant surveys in 21
 locations in western Nevada, eastern California, and southeastern Oregon,
 with the goal of identifying the most commonly co-occurring plant
 community dominants. We selected six of the most common native plant
 species representing a variety of life forms. Species included three
 perennial grasses (<em>Elymus</em> spp. L.,
 <em>Achnatherum thurberianum</em> (Piper) Barkworth,
 <em>Poa secunda</em> J. Presl), two deep-rooted, long-lived
 shrubs (<em>Artemisia tridentata </em>Nutt. and
 <em>Ericameria nauseosa</em> (Pall. ex Pursh) G.L. Nesom
 & Baird), and one annual/biennial forb (<em>Chaenactis
 douglasii </em>(Hook.) Hook. & Arn.). We included sites
 where <em>Elymus elymoides</em> (Raf.) Swezey and <em>E.
 multisetus </em>M.E. Jones co-occur and likely hybridize, given
 their shared distribution in the western Great Basin (Barkworth et al.,
 2007). For simplicity, we refer to <em>Elymus</em> taxa
 jointly as a “species”, even though <em>Elymus</em>
 collections may include two hybridizing species; the Austin site was the
 only location where either no <em>E. multisetus</em> was
 observed in the field and all seed-grown plants were confirmed as
 <em>E. elymoides</em>, which is consistent with the more
 western Great Basin distribution of <em>E.
 multisetus</em>. We identified six collection
 sites within the Cold Deserts ecoregion where all focal species occurred
 (Omernik & Griffith, 2014). Sites were primarily mid-elevation,
 sagebrush steppe communities, with average annual precipitation between
 237 and 384 mm and elevation ranging from 1395-2055 m (PRISM Climate
 Group, 2004). We bulk-collected mature seeds for each species in each
 location from a minimum of 50 individual plants, with a minimum of 1 m
 separating individuals, between 1 June and 15 December of 2015. We
 prepared 90 mesocosms (200L) outside of the Valley Road Greenhouse Complex
 at the University of Nevada, Reno (39.537924, -119.804757). Each mesocosm
 was filled with locally sourced topsoil to 0.9m depth (soil surface area =
 0.25m<sup>2</sup>, soil volume =0.3m<sup>3</sup>).
 Seeds were examined on a light table to ensure seed fill, and planted in
 November 2016, following the same orientation and planting design in each
 mesocosm. Each mesocosm included two replicates of
 <em>Elymus</em> spp. and <em>A. thurberianum</em>,
 six replicates of <em>P. secunda</em>, and one replicate of
 <em>C. douglasii</em>, <em>E. nauseosa</em>, and
 <em>A. tridentata</em> to approximate a dense natural
 community, and two seeds were sown into each planting position to increase
 the chances of seedling emergence. In cases where seedlings from both
 seeds established, each planting position was thinned to one seedling
 based on a random coin flip. To augment direct seeding, plants of each
 species and site were also grown in the greenhouse to serve as
 replacements for plants failing to establish directly from seed. By
 species, this was 45.5% of <em>Elymus</em> spp., 76.7% of
 <em>A. thurberianum</em>, 73.3% of <em>P.
 secunda</em>, 100% of <em>C. douglasii </em>(an annual
 or biennial, so all were transplanted at least once over the three-year
 period), 83.3% of <em>E. nauseosa</em>, and 100% of
 <em>A. tridentata</em> (a small-seeded shrub that necessitated
 transplanting to ensure controlled placement) were transplanted.
 We created two treatment types, sympatric or allopatric, with six
 different combinations for each treatment. As discussed above, the terms
 sympatric and allopatric are often used to describe species, rather than
 populations, but we follow the terminology of Grady et al. (2017) and use
 these terms to describe population history. In the sympatric treatments,
 seeds of all six species from one of the six locations were sown together.
 In the allopatric treatments, seeds from each species and location were
 randomly assigned to one of six allopatric mixes, with one representative
 species from each location in each allopatric mix. This led to a total of
 12 unique communities, which were each planted with seven or eight
 replicates, for a total of 90 mesocosms. Mesocosm soil
 was initially watered to maximum water holding capacity and lightly
 watered once weekly if no natural precipitation had occurred. Each
 mesocosm was monitored for seedling emergence from November 2016 to May
 2017, and seedlings were thinned as needed. In May 2017, for any plants
 that failed to recruit from seed, individuals were transplanted from seeds
 sown in the greenhouse. At the end of August 2017, when many of the
 perennial grasses had become senescent, every plant was assessed for
 height, crown size (length ✕ width), senescence index (a visual estimate
 using a continuous integer between 0-3; 0 = no live tissue and 3 =
 &gt;75% green tissue), and the number of inflorescences. Starting in
 late September 2017, the second growing season, a new round of monitoring
 began following several rainstorms. We tracked new leaf growth and
 survival through May 2018. As in the previous year, in May 2018, we
 replaced any dead individuals. From May to October 2018, we noted whether
 plants had green tissue (0/1) on a weekly basis and used this information
 to estimate the number of days a given plant had potentially
 photosynthetically active tissue during the growing season. At the end of
 August 2018, each plant was assessed for crown size, height, senescence
 index, and the number of inflorescences. In October
 2018, each mesocosm was invaded with 130 <em>B. tectorum</em>
 seeds to test invasion resistance, with seeding density based on a field
 survey of seed production in a moderately invaded site. Seeds were lightly
 raked into the soil surface, in interspaces between plants. All plants
 were grown through August 2019 and watered as needed as in previous years.
 In August 2019, the aboveground biomass of all plants was harvested,
 oven-dried, and weighed. Annual productivity was
 estimated from measurements of native plant volume in years 1 and 2
 (calculated as crown size multiplied by plant height) and from aboveground
 biomass in 2019, and reproductive output was estimated as the number of
 inflorescences per plant. Overall survival was measured from the number of
 transplants used to replace dead plants required at any planting location
 in a mesocosm over all three growing seasons. The total mass of
 <em>B. tectorum</em> per mesocosm was used as the indicator of
 invasion resistance. For species that have senescence as part of their
 life history strategy (all but <em>A. tridentata</em>),
 phenology was evaluated in two different ways: 1) the total number of days
 that a given plant had green tissue from fall through spring (September
 through May), or 2) the senescence index measured in August.
description: We first used community composition models to analyze overall
 community composition and plant survival in each year, using linear models
 implemented in R version 4.1.0 (R Core Team, 2021). These models included
 species, community, and a species x community interaction as fixed effects
 with survival, plant volume, or biomass as response variables. Response
 variables were transformed as needed to better fit model assumptions. F
 statistics and p-values were calculated using the R package
 ‘<em>car</em>’ (Fox & Weisberg, 2019). The goodness of
 fit (R2-values) was calculated with the R package ‘MuMIn’ (Barton, 2020)
 for this and all glm models and post-hoc contrasts were generated using
 the Tukey honest significant differences method with the ‘agricolae’ R
 package (de Mendiburu & Yaseen, 2020). Residual histograms and
 scatterplots of predictors and response variables were created to verify
 model assumptions of normality, homogeneity of variances, and linearity of
 relationships. Q1: Do plants perform differently when
 grown with sympatric or allopatric neighbors, and do responses differ
 among species or populations? We created a main
 effects model asking whether individual plants had responses to sympatric
 or allopatric neighbors, using linear models with species, collection
 site, and treatment (allopatric or sympatric) as fixed effects. For grass
 species, we used linear mixed models that included mesocosm as a random
 (intercept) effect, as they had multiple replicates in a mesocosm (Bates
 et al., 2015). Response variables included survival, size, reproduction,
 and phenological variables. Based on our previous work, we expected
 considerable variation among species, thus we also built species-specific
 models asking whether there were species- or location-specific differences
 in response to sympatric or allopatric neighbors. First, we first created
 linear mixed models for each species that included survival as response
 and collection site, treatment, and the interaction between site and
 treatment as fixed effects. Then, we asked whether surviving plants of
 each species differed in size, phenology, or reproduction in allopatric or
 sympatric communities using the same model structure described above, but
 also included plant age (days since transplanting) as a covariate;
 response variables were transformed as needed. Q2: Do
 community-level responses differ among allopatric or sympatric
 treatments? We then quantified whether community-level
 responses (total productivity, total survival, inflorescence production,
 or <em>B. tectorum</em> suppression) differed among unique
 communities or by allopatric/sympatric treatment using linear models on
 the aggregated community level values per mesocosm. Total responses were
 calculated by summing response values across all individual plants in each
 mesocosm. Models included treatment (allopatric/sympatric) and unique
 community (one of the 12 allopatric or sympatric combinations, nested
 within treatment) as fixed effects, and separate models were created for
 each response variable and each year of measurement, with transformations
 as needed. Means were again compared using the Tukey honest significant
 differences method for multiple comparisons. Q3: Can
 we identify factors that can predict differences in invasion
 resistance? After assessing whether communities
 differed in key performance metrics, we sought to identify factors that
 might explain the observed differences in <em>B. tectorum</em>
 invasion resistance. For this, we asked whether any individual species was
 having an outsized predictive effect on <em>B. tectorum</em>
 biomass. We took a tiered model building approach. First, we considered
 potential explanatory variables (survival, inflorescence production,
 volume, senescence level of native plants prior to invasion, and the
 number of live green days experienced during the fall-winter of invasion)
 separately for each species. For grass species, we summed the values
 across the replicates within a community to represent the total
 performance of a species. We ran a set of generalized linear models
 separately for each metric of performance and each species, considering
 whether any individual response for an individual species predicted
 <em>B. tectorum</em> biomass, log transformed for analysis. We
 then retained a subset of variables for a multiple regression model, which
 included the most impactful explanatory variables (p &lt; 0.05) from
 the previous analyses, further reducing as needed to ensure no variable in
 the model had a VIF greater than 3 (Fox & Weisberg, 2019).
 Finally, we retained significant variables to create a final multiple
 regression model of species-level responses that best explained
 <em>B. tectorum</em> biomass.