DOI: 10.25338/b89356
title: Extending trait dispersion across trophic levels: predator assemblages act as top-down filters on prey communities

description: Studies of community assembly typically focus on the effects of abiotic
 environmental filters and stabilizing competition on functional trait
 dispersion within single trophic levels. Predation is a well-known driver
 of community diversity and composition, yet the role of functionally
 diverse predator communities in filtering prey community traits has
 received less attention. We examined functionally diverse communities of
 predators (fishes) and prey (epifaunal crustaceans) in eelgrass (Zostera
 marina) beds in two Northern California estuaries to evaluate the
 filtering effects of predator traits on community assembly, and how
 filters acting on predators influence their ability to mediate prey
 community assembly. Fish traits related to bottom orientation selected for
 more clustered epifauna communities, and epifauna were generally
 overdispersed while fishes were clustered, suggesting that prey may be
 pushed to disparate areas of trait space to avoid capture by benthic
 sit-and-wait predators. We also found correlations between the trait
 dispersions of predator and prey communities that strengthened after
 accounting for the effects of habitat filters on predator dispersion,
 suggesting that habitat filtering effects on predator species pools may
 hinder their ability to affect prey community assembly. Our results
 present compelling observational evidence that specific predator traits
 have measurable impacts on the community assembly of prey, inviting
 experimental tests of predator trait means on community assembly, and
 explicit comparisons of how the relative effects of habitat filters and
 intraguild competition on predators impact their ability to affect prey
 community assembly. Integrating our understanding of traits at multiple
 trophic levels can help us better predict the impacts of community
 composition on food web dynamics as regional species pools shift with
 climate change and anthropogenic introductions.
description: We sampled fish and epifaunal communities in 6 eelgrass beds in
 Bodega Harbor and Tomales Bay in the summers of 2019 and 2021. We sampled
 fishes in 6 sets of a custom beach seine net when the water level was at
 or below 1 m above the seafloor. The seine sampled a circular area of 11
 m<sup>2</sup>. We counted, identified to the lowest possible
 taxonomic level (typically species), and released animals retained in the
 seine. We sampled epifauna at 12 locations within each
 site separated by at least 10m and spanning a depth gradient of intertidal
 to shallow subtidal. We collected each sample by everting an open-mouth
 drawstring mesh bag (500 µm mesh size) over a clump of shoots in the
 eelgrass bed so that the mouth of the bag was flush with the sediment
 surface, cutting the shoots, and closing the drawstring to capture shoots,
 macroalgae, and associated animals. We transferred the shoots to the
 laboratory on ice, rinsed, and hand-inspected them to dislodge the
 epifauna, which we then passed through a 500 µm sieve and ultimately
 transferred into 70% ethanol. We then identified epifauna to the lowest
 possible taxonomic level (typically species). We also quantified the
 biomass of macroalgae in each epifaunal sample. We also measured water
 temperature, total eelgrass shoot density m<sup>-2</sup>,
 flowering shoot density m<sup>-2</sup>, percent cover, canopy
 height, and epiphyte dry weight mm<sup>-2</sup> eelgrass as
 described by Aoki et al. (2022). For the 23 most
 abundant species of peracarids in our surveys, we assigned values for 11
 traits putatively related to predator avoidance and microhabitat niche. We
 collected three of these traits (maximum body size, shape, and living
 habit) from the literature. We determined the tube fidelity for each
 species according to observations of living and preserved specimens along
 a four-point ordered scale as follows: none (species lacks silk glands to
 build tubes), low (species has silk glands but was never observed in a
 tube alive or preserved in ethanol), medium (species has silk glands and
 was observed in tubes when alive but readily flees tube when exposed to
 ethanol), and high (species has silk glands, is tubicolous when alive, and
 is regularly found inside tubes after preservation in ethanol). We
 measured mean body size (length from rostrum to telson), relative eye
 diameter, and relative antenna lengths from 10-20 preserved individuals
 collected across sites and years. We measured activity levels as fractions
 of time spent swimming, walking, and still (unmoving) from one-minute
 video recordings of 10-20 live individuals per species across sites and
 years. We log-transformed peracarid traits where appropriate to conform to
 a normal distribution. We assigned two categorical
 (vertical position and foraging mode) and one continuous trait (trophic
 level) to the 16 most abundant fishes based on the literature. We
 fuzzy-coded vertical position and foraging mode among 5 and 3 levels,
 respectively, to accommodate species that could be classified among
 multiple levels. We collected linear morphometric measurements of fishes
 (body and head dimensions, fin lengths, eye size and position, and mouth
 height and protrusion) from 2-26 specimens per species and size class
 collected from seines, and standardized them for ease of comparison across
 species. This dataset includes average trait data for
 both peracarids and fishes. To address the potential
 effects of evolutionary history on peracarid community responses to
 predators, we built a phylogeny of our species by subsetting from the
 ultrametric peracarid supertree published by Ashford et al. (2018). For
 species in our dataset that were not included in the supertree we
 substituted congeners or confamilials as needed. Tables
 S1-S3 (on Zenodo) show modeled responses of residual peracarid community
 trait and phylogenetic dispersion to fish community-weighted mean trait
 values (Table S1), total fish community trait dispersion (Table S2) and
 residual fish community trait dispersion after accounting for habitat
 filters (Table S3).
description: Code file is written in R; data files are .csv files that can be
 opened and viewed with Microsoft Excel; phylogeny is a .txt that can be
 opened in a text editor and manipulated and analyzed in R. Supplementary
 Tables 1-3 are an .xlsx file viewable in Microsoft Excel. 
description: # Extending trait dispersion across trophic levels: predator assemblages
 act as top-down filters on prey communities ## Description of the data and
 file structure Environmental and species abundance data collected in
 summer (June-August) 2019 and 2021 from eelgrass beds in Northern
 California. **NOTE**: Version created Apr 2024 added file #7. This dataset
 consists of 7 data files: 1. Epifauna.list.csv, created July 19, 2023.
 Invertebrates collected from grab samples of eelgrass (Zostera marina)
 from 8 sites across the two sampling years (only 6 sites were used in
 analyses). * Sample: The code used to identify an individual grab sample,
 read as: subsite_tidal height, transect number_sample along transect_year
 * Bay: The estuary where the samples were collected (BH = Bodega Harbor,
 DE = Drakes Estero, TB = Tomales Bay) * Subsite: The site code used to
 define a community of epifauna (BL = Blake's Landing, CC = Campbell
 Cove, MM = Mason's Marina, MP = Millerton Point, NC = Nick's
 Cove, SB = Schooner Bay, SL = Sacramento Landing, WP = Westside Park) *
 Year: Year sampled (2019 or 2021) * Date: Date sampled (m/dd/yy) * Tidal
 height: Height of transect relative to tidal regime; "upper" =
 intertidal transects 1-3 that were fully emersed, "lower" =
 subtidal transects 4-6 that were always immersed. * Grab bag: The
 individual grab sample. U = upper, L = lower. First number refers to the
 transect, second refers to 1 of 2 samples along the transect. * Species:
 Finest taxonomic resolution available for an organism observed in samples
 * Count: The number of individuals of each species * Epifaunal: Does the
 animal live on eelgrass blades or was it incidentally collected from the
 sediment? * Mobile: Is the animal mobile or sessile? * Peracarid: Is the
 animal an amphipod, isopod, or tanaid? 2. Fish.list.csv, created July 19,
 2023. Fishes collected from seine sets in eelgrass from 8 sites across the
 two sampling years (only 6 sites were used in analyses). * Sample: The
 code used to identify an individual seine sample, read as:
 subsite_seine_year * Bay: The estuary where the samples were collected (BH
 = Bodega Harbor, DE = Drakes Estero, TB = Tomales Bay) * Subsite: The site
 code used to define a community of epifauna (BL = Blake's Landing, CC
 = Campbell Cove, MM = Mason's Marina, MP = Millerton Point, NC =
 Nick's Cove, SB = Schooner Bay, SL = Sacramento Landing, WP =
 Westside Park) * Date: Date sampled (m/dd/yy) * Time: Time (24 hr) when
 the seine was set. * Species: Common name of species in seine * Length:
 Standard length in millimeters measured in situ * Count: Number of
 individuals of a species with a given standard length * Size: For species
 with discrete size cohorts, is it larger or smaller? 3. Fish.traits.csv,
 created June 1, 2023. Mean traits collected from individual fishes
 collected in the field and from published literature. Morphometric
 measurements are shown in Figure S1 of Appendix S1. * Species: Fish common
 name and size class (if applicable) * Standard_Length_mm: Length in mm
 from the tip of the snout to the end of the caudal peduncle *
 Mouth_Height: Distance in mm from distal tip of the premaxilla to the
 distal tip of the dentary with the jaws fully extended, divided by
 standard length. * Mouth_protrusion: Length in mm from distal tip of the
 premaxilla to the eye pupil with jaws fully extended, divided by head
 length. * Dorsal_fin_length: Straight length in mm from the anterior to
 posterior end of the dorsal fin (summed where dorsal fins were
 discontinuous), divided by standard length. * Pectoral_fin_length: Length
 in mm from base to the tip of the longest pectoral ray, divided by
 standard length. * Eye_position: Vertical distance in mm from the pupil to
 the top of the head, divided by head depth. * Snout_length: Distance in mm
 from eye pupil to distal tip of the premaxilla, with the mouth closed,
 divided by head length. * Head_depth: Vertical distance in mm from the top
 of the head to the bottom of the head, passing through the eye pupil,
 divided by body depth. * Eye_diameter: Horizontal distance in mm across
 the eye passing through the pupil, divided by head length. * Head_length:
 Distance in mm from posterior margin of the operculum to the distal tip of
 the premaxilla with the jaws closed, divided by standard length. * BDBM:
 Greatest vertical distance in mm below a horizontal line drawn from the
 tip of the snout to the end of the caudal peduncle, divided by body depth.
 * Body_depth: Greatest vertical distance in mm from the top of the fish to
 the bottom, divided by standard length. * Anal_fin: Straight length in mm
 from the anterior to posterior end of the anal fin, divided by standard
 length. * Caupe_L: Horizontal distance in mm from the end of the caudal
 peduncle to the end of the anal fin, divided by standard length * Caupe_D:
 Vertical distance in mm across the narrowest portion of the caudal
 peduncle, divided by body depth. * CauF_L: Straight distance in mm from
 the end of the caudal peduncle to the distal tip of the longest caudal fin
 ray, divided by standard length. * pursuit_predator: Suite of behaviors
 associated with feeding and foraging. Fuzzy-coded across 5 levels. *
 benthic_browser: Suite of behaviors associated with feeding and foraging.
 Fuzzy-coded across 5 levels. * epifaunal_browser: Suite of behaviors
 associated with feeding and foraging. Fuzzy-coded across 5 levels. *
 planktivore: Suite of behaviors associated with feeding and foraging.
 Fuzzy-coded across 5 levels. * sit_and_wait: Suite of behaviors associated
 with feeding and foraging. Fuzzy-coded across 5 levels. * benthic: The
 orientation of the fish in the water column. Fuzzy-coded across three
 levels. * pelagic: The orientation of the fish in the water column.
 Fuzzy-coded across three levels. * benthopelagic: The orientation of the
 fish in the water column. Fuzzy-coded across three levels. *
 Trophic_level: The average trophic level of the species, estimated from
 food items. 4. Peracarid.traits.csv, created October 5, 2022. Mean traits
 collected from individual peracarids collected in the field and from
 published literature. Morphometric measurements are shown in Figure S3 of
 Appendix S1. * Species: The binomial name of the peracarid species. *
 Perc_swimming: Percentage of total video frames during which pleopod-
 driven locomotion occurred. * Perc_walking: Percentage of total video
 frames during which pereopod-driven locomotion in contact with the cup
 surface occurred. * Perc_still: Percentage of total video frames during
 which no forward locomotion occurred. * Eye_diameter: Diameter in mm of a
 circle with an area equal to that of the eye (eyes are often
 irregurlarly-shaped), divided by body length. * Antenna_length_1: Distance
 in mm from the base to the distal tip of antenna 1, divided by body
 length. * Antenna_length_2: Distance in mm from the base to the distal tip
 of antenna 2, divided by body length. * Tube_fidelity: The degree of
 association with constructed silk tubes. * Body_size_observed: Body length
 in mm measured from the tip of the rostrum to the tip of the telson across
 individuals collected during sampling. * Body_size_literature: Body length
 in mm measured from the tip of the rostrum to the tip of the telson as
 described in Carlton (2007). * Shape: Overall body shape. * Living_habit:
 Mode of contact with habitat substrate (eelgrass). 5. Peracarid.tree.txt,
 created July 19, 2023. Ultrametric phylogeny of peracarid species observed
 in our grab samples, based on the Ashford et al. 2018 peracarid supertree
 (doi: 10.1098/rspb.2018.0923). Some of our species were not included in
 the supertree, so we made the following substitutions: Amphilochus
 tenuimanus --&gt; Apolochus barnardi, Paracorophiini spp. --&gt;
 Paracorophium sp., Ericthonius sp.--&gt; Ericthonius brasiliensis, Photis
 sp. --&gt; Photis brevipes, Leptochelia dubia --&gt; Leptochelia sp.,
 Sphaeroma quoianum --&gt; Gnorimosphaeroma sp., Munnidae spp. --&gt;
 Uromunna ubiquita, Corophium sp. --&gt; Americorophium spinicorne, Lembos
 spp. --&gt; Paramicrodeutopus schmitti 6. Site.data.csv, created July 19,
 2023. Environmental data collected from sites in 2019 and 2021. * Bay: The
 estuary where the samples were collected (BH = Bodega Harbor, DE = Drakes
 Estero, TB = Tomales Bay) * Subsite: The site code used to define a
 community of epifauna (BL = Blake's Landing, CC = Campbell Cove, MM =
 Mason's Marina, MP = Millerton Point, NC = Nick's Cove, SB =
 Schooner Bay, SL = Sacramento Landing, WP = Westside Park) * Year: Year
 sampled (2019 or 2021) * Site.Year: Unique site-by-year combination. *
 Eelgrass.wet.g: Wet weight (g) of eelgrass collected in epifauna grab
 sampling * Algal.wet.g: Wet weight (g) of macroalgae collected in epifauna
 grab sampling * Macrophyte.wet.g: sum of eelgrass and macroalgal weight
 (g) from epifauna grab samples * Salinity.psu: In-situ refractometer
 measurements of salinity (psu) * Mean.shoots.m2: The mean number of total
 eelgrass shoots per square meter at each site. * Mean.flowering.m2: The
 mean number of flowering eelgrass shoots per square meter from 24 quadrats
 at each site. * Mean.perc.cover.grass: The average percent cover of
 eelgrass from 24 0.25 square meter quadrats at each site. *
 Mean.perc.cover.macroalgae: The average percent cover of macroalgae from
 24 0.25 square meter quadrats at each site. * Mean.perc.cover.bare: The
 average percent cover of unvegetated sediment from 24 0.25 square meter
 quadrats at each site. * Mean.canopy.height.cm: The average length of the
 longest eelgrass blade from 30 shoots at each site. * Mean.epiphyte.g.cm2:
 The average dry weight of epiphytes per square centimeter of eelgrass
 blade, calculated from 30 3rd-rank blades per site. * Mean.summer.temp.C:
 The average summer temperature measured across the season from pendant
 Hobo loggers at upper intertidal transects. 7. Supplementary Tables
 1-3.xlsx, created Jul 24, 2023. Effect sizes of fish community-weighted
 mean traits and trait dispersion on peracarid trait and phylogenetic
 dispersion. Three data tabs: * Table S1. Effect sizes of
 community-weighted mean fish traits on peracarid community trait and
 phylogenetic dispersion. Bolded cells indicate values significant at the
 alpha level indicated; the first 103 rows are models for which results are
 presented in the main text. Italicized rows represent posthoc tests of
 individual peracarid community response traits. Rows are colored according
 to the direction and magnitude of the effect size; red indicates a
 negative effect while blue indicates a positive effect, and color
 saturation is proportional to R2. * Table S2. Effect sizes of fish
 community trait dispersion on residual peracarid community trait and
 phylogenetic dispersion, not accounting for the effects of habitat filters
 on fish dispersion. Bolded cells indicate values significant at the
 specified alpha level; the first 30 rows are effects for which results are
 presented in the main text. F statistics are on 1 and 10 degrees of
 freedom. Rows are colored according to the direction and magnitude of the
 effect size; red indicates a negative effect while blue indicates a
 positive effect, and color saturation is proportional to R2. * Table S3.
 Effect sizes of fish community trait dispersion on residual peracarid
 community trait and phylogenetic dispersion, controlling for the effects
 of habitat filters on fish dispersion. Bolded cells indicate values
 significant at the specified alpha level; the first 30 rows are effects
 for which results are presented in the main text. Rows are colored
 according to the direction and magnitude of the effect size; red indicates
 a negative effect while blue indicates a positive effect, and color
 saturation is proportional to R2. ## Sharing/Access information * Data was
 derived from the following sources: Species abundance and environmental
 parameters were collected according to protocols described in Gross &
 Stachowicz in prep. for Ecology and Aoki et al. 2022 (doi:
 10.1002/lno.12152). Trait data was compiled from literature and measured
 individuals as described and cited in the Appendix of Gross &
 Stachowicz in prep. Phylogenetic tree was subsetted from the Ashford et
 al. 2018 peracarid supertree (doi: 10.1098/rspb.2018.0923) ##
 Code/Software Gross.Stachowicz.R is a script containing all of the
 analyses conducted in the manuscript. A brief outline is as follows: Load
 packages tidyverse, ggfortify, ggvegan, vegan, picante, and FD. Packages
 tidyselect, gawdis, ggpointdensity, and gridExtra are used incidentally
 and are called using the double colon (::) in context. 1. Load data on
 traits and communities, calcluate distances and community weighted means
 1. Load environmental data 2. Load epifaunal data 3. Peracarid trait data
 1. Peracarid trait distances 2. Peracarid community-weighted means D. Load
 fish data E. Fish trait data 3. Fish community-weighted means 4. Fish PCA
 5. Fish trait distances 2. Calculate standard effect sizes for fish and
 peracarid communities 1. Calculate peracarid dispersion for each SES,
 permutation algorithm, and trait. 1. Calculate residual peracarid
 dispersion for SES_MNTD_ts 2. Calculate residual peracarid dispersion for
 SES_MNTD_is 3. Calculate residual peracarid dispersion for SES_MPD_ts 4.
 Calculate residual peracarid dispersion for SES_MPD_is 2. Calculate fish
 dispersion for each SES, permutation algorithm, and trait. 1. Calculate
 total fish dispersion for SES_MNTD_ts 2. Calculate total fish dispersion
 for SES_MNTD_is 3. Calculate total fish dispersion for SES_MPD_ts 4.
 Calculate total fish dispersion for SES_MPD_is 3. Calculate residual fish
 dispersion for each SES, permutation algorithm, and trait. 1. Calculate
 residual fish dispersion for SES_MNTD_ts 2. Calculate residual fish
 dispersion for SES_MNTD_is 3. Calculate residual fish dispersion for
 SES_MPD_ts 4. Calculate residual fish dispersion for SES_MPD_is 3. Model
 peracarid dispersion as a function of fish dispersion and
 community-weighted means 1. make.models() function 2. Model residual
 peracarid dispersion as a function of fish community-weighted means 3.
 Model residual peracarid dispersion as a function of total fish dispersion
 D. Model residual peracarid dispersion as a function of residual fish
 dispersion.