DOI: 10.5061/dryad.k6djh9wgj
title: Marine Protection and Environmental Forcing Influence Fish-Derived Nutrient Cycling in Kelp Forests

description: Animal consumers excrete dissolved inorganic nitrogen, an essential
 nutrient for regulating primary production and macroalgal growth in the
 ocean. Often overlooked in attempts to explain kelp forest productivity,
 relatively little is known about the role of consumers in nutrient cycling
 in temperate systems, such as the magnitude of nutrients excreted and the
 factors that influence spatial and temporal variability in
 consumer-derived nutrients. To investigate the supply of ammonium (NH4+)
 excreted by the dominant members of the nearshore rocky reef fish
 community, we combined empirically-measured relationships between
 excretion rate and body mass with data on fish density and size structure
 from visual SCUBA surveys conducted from 2005-2018 in the northern Channel
 Islands, California, USA. The fish community excreted a substantial amount
 of ammonium to the kelp forest (mean: 95.5-131.3 µmol·m-2·hr-1), however
 excretion varied substantially among sites and over time (range:
 23.1–247.9 µmol·m-2·hr-1). The ammonium supply was influenced by the
 establishment of marine protected areas (MPAs) that restricted fishing
 activities and environmental characteristics that influenced geographic
 and temporal shifts in the overarching fish community structure.
 Fish-derived ammonium excretion rates were 50-80% greater inside MPAs
 compared to areas open to fishing, while environmental and habitat
 characteristics (e.g., habitat vertical relief, kelp biomass, wave
 exposure, chlorophyll a) explained 85% of the spatial variation in
 community excretion rates. In contrast, large-scale oceanographic
 phenomena (e.g., North Pacific Gyre Oscillation index) and past patterns
 of fish recruitment explained 57% of the temporal variation in nutrient
 excretion over the 14-year time series. Results suggest that fish-derived
 ammonium may provide an important and underappreciated nutrient source to
 kelp beds, particularly during low-nutrient periods (e.g., seasonal
 reductions in upwelling or El Niño-Southern Oscillation events), and that
 fishing disrupts these nutrient cycling pathways. Fishes likely play a
 critical role in supporting the resiliency of kelp forest ecosystems by
 supplying a relatively constant source of reduced nitrogen that can be
 utilized by giant kelp and other macroalgae to fuel primary production of
 biogenic habitat.
description: <em>Study system</em> The
 northern Channel Islands, California, USA, are located in the middle of a
 dynamic oceanographic boundary formed by the cold California Current to
 the west and the warmer Southern California Countercurrent to the east.
 The convergence and mixing of the currents result in substantial variation
 in productivity and the formation of strong thermal gradients from west to
 east that influence benthic community structure across four islands,
 covering a scale of approximately 100 km. These kelp forests support
 diverse assemblages with many invertebrates and fishes that rely on the
 modification of the habitat by the canopy forming giant kelp
 (<em>Macrocystis pyrifera</em>).<em> </em>In
 addition, spatial variation in fish biomass throughout the wider Southern
 California Bight, including the northern Channel Islands, is strongly
 associated with physical environmental and habitat characteristics. Fish
 abundance and biomass has also been observed to vary across the Channel
 Islands in response to the establishment of a network of MPAs, with
 biomass nearly doubling for species targeted by fishing activities since
 2003. <em>Fish Community Survey
 Methodology</em> Visual surveys of kelp forest
 assemblages conducted by the Partnership for Interdisciplinary Studies of
 Coastal Oceans (PISCO) during summer/fall were used to quantify fish
 abundance and biomass, in order to estimate nutrient excretion by the fish
 community. Sampling effort has changed over time, but included n=46 sites
 in the northern Channel Islands at the peak of effort, with sites inside
 and outside MPAs. At each site, PISCO divers conducted n=8 to 12 fish
 transects (30 m long × 2 m wide × 2 m high) at multiple levels in the
 water column: benthic, midwater, and canopy in depths from 0-20 m.
 Transects were laid out in a stratified-random design, with multiple
 non-permanent transects located in fixed strata (i.e., outer, middle, and
 inner edges of the reef). At each level in the water column, one diver
 counted and sized the total length (in centimeters) of all the fishes per
 transect (excluding small cryptic species). Experienced underwater
 observers are accurate to 1 cm in their visual estimates. Although PISCO
 surveys started in 1999, we included only the year 2005 onwards in order
 to encompass when the survey effort expanded to include sufficient sites
 for analysis over time. To focus only on resident kelp forest species, we
 excluded elasmobranchs and highly migratory species. Although over 125
 species associate with rocky reefs in the Southern California Bight, we
 focused on the 50 resident species comprising 95% of the bony fish biomass
 in the northern Channel Islands.  <em>Estimating
 fish community excretion</em> To estimate
 nitrogen excretion by the fish community on an areal scale, we calculated
 the mass of ammonium excreted by each individual observed on a transect
 (NH<sub>4</sub><sup>+</sup>
 µmol·m<sup>-2</sup>·hr<sup>-1</sup>) using the
 family-level mass-specific equations determined in Shrestha et al. (2024).
 The formulas estimate ammonium excretion by fish weight (both log
 transformed); thus, we converted the estimated lengths of each fish
 observed on a transect to weight (in grams, wet mass) using published
 weight-length formulas. We then summed the excretion of each individual
 observed on a transect over the three levels of the water column (bottom,
 midwater, canopy) to estimate total ammonium excreted by all fish per
 transect per area of benthos. The total rate of excretion per unit area at
 each site was then averaged across transects each year, with the mean
 excretion in a site-year as the lowest level of replication.
 <em>Testing spatial and temporal variability in fish
 community excretion </em> We first evaluated
 spatial differences in the supply of ammonium by fishes among islands due
 to MPA protection, using data from n=33 sites (15 MPA and 18 non-MPA)
 surveyed for at least 3 years (all sites). We also explored spatial and
 temporal patterns in excretion using data from a subset of n=19 sites (10
 MPA and 9 non-MPA) surveyed concurrently from 2005-2018 (long-term
 sites).
description: # Marine protection and environmental forcing influence fish-derived
 nutrient cycling in kelp forests
 [https://doi.org/10.5061/dryad.k6djh9wgj](https://doi.org/10.5061/dryad.k6djh9wgj) ## Description of the data and file structure Data set consists of fish community surveys using SCUBA at the Channel Islands, USA and estimates of ammonium excretion for each fish counted and sized on each underwater visual transect. The data set also includes fish length-weight conversions used to calculate fish biomass from SCUBA surveys, allowing estimates of ammonium excretion. ### Files and variables #### File: Shrestha_fish_excr_data_Channel_Islands_all.csv **Description:** Fish ammonium excretion estimates for sites at the Channel Islands, USA from 2003-2018. Includes data from 33 sites surveys for at least 3 years between 2003-2018. #### File: Shrestha_fish_excr_data_Channel_Islands_longterm_sites.csv **Description:** Fish ammonium excretion estimates for sites at the Channel Islands, USA from 2003-2018. Includes data from 19 sites surveyed from 2005-2018. ##### Variables * Year - Year of the survey * Month - Month of the survey * Day - day of the survey * Site - Location of the survey * Side - Sites can be split into two or three areas to stratify the sampling. W = west, Cen = central, E = East * Zone - Location of the visual transects from the outer (deep) to inner (shallow) areas of each kelp bed / site. Outer - deepest (20 m), Outmid - next deepest (15 m), Inmid - next deepest (10 m), Inner - shallowest (5 m) * Transect - ID number of each transect in a particular zone per side of a site * Classcode - Fish species ID code (first letter of genus and first three letters of the species name) * fish_tl.cm - Fish total length in cm * estimated.wt.g - Fish weight estimated from published Length-Weight relationships for each species * EXCR_IND - Estimated ammonium excretion per individual per hour, using species-specific relationships between body size and excretion * Count - The number of fish per species per size class counted on that transect * Transect area - area of each fish transect is 60 m2 (30 x 2 m) * EXCR_M2 - Estimated ammonium excretion per fish of that body size and species observed on the transect per unit area (m2) * density.indiv.m.2 - The density of fish per m2 of rocky reef habitat * Family - Taxonomic family for that fish species * Genus - Taxonomic grouping at genus level * Species - Taxonomic grouping at species level * Notes * MPAGroup - Name of the Marine Protected Area (if any) associated with that site * MPA_Status - Whether the site is a reference area (open to fishing), SMR (state marine reserve and fully no-take), or SMCA (state marine conservation area that may allow take of some species) * Reserve - whether a site is IN or OUT of an MPA of any kind * MLPA_region * Region - location in the greater Southern California Bight * Subregion - Island where the site is located. ANA - Anacapa Island, SCI - Santa Cruz Island, SRI - Santa Rosa Island, SMI - San Miguel Island * LAT_WGS84 - Latitude * LON_WGS84 - Longitude * YEAR_MPA_Est. - Year the MPA was established. Values of zero reflect a non-MPA site * MPAAreaNM2 - MPA area in nautical miles squared * MPA_Shore_length_NM - Length of shoreline in the MPA in nautical miles #### File: Shrestha_fish_length-weight_conversion_table.csv **Description:** Fish length-weight and length-length conversions used in the estimation of fish biomass for ammonium excretion calculations for common southern California kelp forest fish species included in the publication. ##### Variables * pisco_classcode - Currently used PISCO classcode, usually first letter of genus, first three letters of species with exceptions for overlapping codes and species groupings * genus - Currently accepted genus * species - Currently accepted species * common_name - Common name * ScientificName_accepted - Full WoRMS accepted scientific name * Family - Taxonomic Family * WL_a - Length to weight parameter a (Weight = a*Length^b) * WL_b - Length to weight parameter b (Weight = a*Length^b) * WL_W_units - Output weight units (g, kg) * WL_L_units - Input length units (mm, cm) * WL_input_length - Input length type (SL=standard length, FL=fork length, TL=total length) * WL_Reference_Notes - Primary source for length-weight parameters, and additional notes (e.g. when a similar species was used). RecFIN refers to the Recreational Fisheries Information Network, which is the source for some conversion parameters. * LC.a._for_WL - Length conversion parameter a (note only needed when input length type is not total length) * LC.b._for_WL - Length conversion parameter b (note only needed when input length type is not total length) * LC_type_for_WL - Length conversion type (typical, reverse) (note only needed when input length type is not total length) * LL_Reference_Notes_for_WL - Source for length-length conversion parameters * LL_Equation_for_WL - Equation for length-length conversion ## Access information Other publicly accessible locations of the data: Data was derived from the following sources: * Malone DP, Davis K, Lonhart SI, Parsons-Field A, Caselle JE, Carr MH (2022) Large-scale, multidecade monitoring data from kelp forest ecosystems in California and Oregon (USA). Ecology 103:e3630. [https://doi.org/10.1002/ecy.3630](https://doi.org/10.1002/ecy.3630) * Shrestha J, Coale KH, Hamilton SL (2023) Empirical measurements of ammonium excretion in kelp forest fishes: effects of body size, taxonomy and trophic guild. Journal of Experimental Marine Biology and Ecology 569:151956.[https://doi.org/10.1016/j.jembe.2023.151956](https://doi.org/10.1016/j.jembe.2023.151956)