DOI: 10.6078/d1tm66
title: Seasonal growth potential of Oncorhynchus mykiss in streams with contrasting prey phenology and streamflow

description: The growth of any organism depends on habitat conditions, food
 availability, and their seasonal interactions. Yet in vast literature on
 Pacific salmon (Oncorhynchus), the seasonal interaction between habitat
 conditions and food availability has received relatively little attention.
 We examined juvenile O. mykiss rearing, physical habitat, and resource
 phenologies in two Mediterranean coastal streams – one perennial, cool,
 and shaded; the other intermittent, seasonally warm, and sunny. We used a
 bioenergetics model to investigate the timing and magnitude of growth
 potential for drift foraging O. mykiss during the spring and summer in
 both systems. Growth potential peaked at least two months earlier in the
 intermittent stream than in the perennial stream. By early summer (June),
 growth potential had declined in the intermittent stream, whereas growth
 rates were peaking in the perennial stream. However, the mid-July lipid
 content of juvenile O. mykiss in the intermittent stream was nearly twice
 that of fish in the perennial stream. By late summer (August), foraging
 profitability declined in both streams, as abiotic conditions in the
 intermittent stream approached lethal. In contrast, the perennial stream
 maintained suitable abiotic conditions even though growth rate was low. We
 suggest that the divergent resource phenologies and seasonal mortality
 risks experienced by anadromous O. mykiss rearing in these streams could
 drive diversification of traits governing size, age, and timing of
 outmigration.
description: <strong>Study sites</strong> Elder
 and Porter Creeks both flow through the Northern California Coast Range
 (Fig. 2). Elder Creek is a 16.7 km<sup>2</sup> tributary of
 the upper South Fork Eel River in Mendocino County, California within the
 University of California Angelo Coast Range Reserve (39.7181° N, 123.6527°
 W, Fig. 2). Elder Creek’s channel is dominated by cobbles and boulders,
 with streambed gradients ranging from 2% - 5%  (McBain and Trush 2000).
 The stream is shaded by a dense riparian canopy, primarily comprised of
 white alder (<em>Alnus rhombifolia</em>), with some bigleaf
 maple (Acer macrophyllum) and Oregon ash (<em>Fraxinus
 latifolia</em>). Elder Creek experiences a characteristic
 Mediterranean-climate flow recession between April and October (Dralle et
 al. 2017). However, the basin is underlain by deep water-holding argillite
 shales of the Northern California Coastal belt, which sustain perennial
 flow even during prolonged drought (Lovill et al. 2018, Rempe and Dietrich
 2018), so dry season low flows rarely drop below 0.015 to 0.03
 m<sup>3</sup>/s.  Porter Creek is a 19.4
 km<sup>2</sup> tributary to the Russian River in Sonoma
 County, California (38.5279° N, 122.8992° W, Fig. 2). Porter Creek’s
 channel (0.5% to 3%) is lower gradient then Elder Creek with a pebble and
 gravel dominated bed.  The riparian community is a mix of alders
 (<em>Alnus </em>spp.), buckeye (<em>Aesculus
 californica</em>), willow (<em>Salix</em> spp.), Oregon
 ash, and coast redwood (<em>Sequoia sempervirens</em>) as well
 as invasive shrubs such as Himalayan blackberry (<em>Rubus
 armeniacus</em>). Except in the wettest years, Porter Creek becomes
 intermittent during the dry season for much of its length, although the
 headwaters are typically perennial.  The Franciscan mélange geology of the
 Porter Creek basin (Jennings 1977) has much lower hydraulic infiltration
 capacity and a shallower Critical Zone than Elder Creek, leading to low
 storage of winter precipitation and greater flow intermittency during the
 dry summer (Hahm et al. 2019). <strong>Sampling
 regime</strong> Four riffle-pool habitat units
 were selected in each stream as study units (Fig. 3). The riffle-pool unit
 is a dominant geomorphic feature in most alluvial streams. During
 low-flow, they can be partially or completely isolated from each other, so
 provide discrete habitats for evaluating juvenile salmonid rearing and
 foraging (Naman et al. 2018, Rossi et al. 2021a). We selected riffle-pool
 units that supported multiple age classes of foraging salmonids and were
 separated from each other by at least two pools. We
 measured the following variables each month between late-April and August:
 (1) streamflow, dissolved oxygen, and water temperature; (2) hydraulics in
 riffles and pools (depth, velocity, width); (3) epibenthic primary
 productivity and algal standing crop; and (4) seasonal invertebrate drift,
 standing crop, and infall (these data were only collected in three of the
 four pools in each stream due to sampling constraints). We also captured
 juvenile <em>O. mykiss</em> to estimate growth and lipid
 content. With these data, we developed a drift-foraging bioenergetics
 model to predict the seasonal change of <em>O. mykiss</em>
 growth potential in three pools in each stream.  Data collection and
 statistical methods are described below and in Appendices S1-S5.
 <strong>Seasonal gradients in water quality and stream
 hydraulics</strong> <em>Streamflow,
 dissolved oxygen, and water temperature</em> — Streamflow (Q, Table
 1) for Elder Creek was retrieved from USGS gaging station 11475560 “Elder
 Creek near Branscomb CA,” which is 0.6 km upstream from the Elder Creek’s
 confluence with the SF Eel River. All of our Elder Creek study sites were
 within 0.4 km of this gage, with no intervening tributaries. In Porter
 Creek, streamflow was retrieved from gaging data collected by Trout
 Unlimited, following methods of Rantz (1982) and (CDFW 2013).
 Dissolved oxygen and water temperature are primary abiotic
 factors controlling habitat quality for salmonids (Bjornn and Reiser.
 1991). We measured dissolved oxygen and stream temperature using
 continuous HOBO U26 data loggers in one Elder Creek and one Porter Creek
 pool. The dissolved oxygen loggers were calibrated prior to deployment,
 and the output data were corrected using HOBOware Pro's Dissolved
 Oxygen Assistant software. Calibration measurements were taken using a
 handheld YSI Pro20 in each pool. In addition, we collected monthly, manual
 water temperature and dissolved oxygen measurements in each pool when we
 measured primary productivity using the handheld YSI Pro20. Hand
 measurements were taken between 11:00 am and 2:00 pm.
 <em>Riffle-pool hydraulics</em> —Measurements of
 velocity, riffle depth and width were used to differentiate the seasonal
 patterns in hydraulics between streams. We installed a cross-stream
 transect midway through the upstream riffle (XS1), and three cross-stream
 transects in the downstream pool of each study site. Pool transects were
 placed where the riffle enters the pool (XS2), a second in the pool head
 patch were salmonids were observed drift foraging (XS3), and a third over
 the maximum depth of the pool (XS4), Fig. 3. Depth and velocity (Table 1)
 were measured at 0.25-m increments along each cross section. Velocity was
 measured with a Marsh-McBirney Flo-Mate 2000 Electro-magnetic Flow Meter
 at 0.6 depth from the water surface. <strong>The
 phenology of O. mykiss prey</strong>
 <em>Primary production and algal standing crop</em> —
 In California coastal streams, benthic algae and periphyton are the
 primary source of carbon for many benthic invertebrates (Finlay et al.
 2002). Thus, seasonal changes in the standing crop of benthic algae affect
 energy flow to salmon and the phenology of salmon prey abundance. To track
 the seasonality of primary production, we estimated primary productivity
 in pools, by measuring net primary productivity (NPP) and respiration (R)
 from attached algae on individual cobbles using the light/dark incubation
 method of Hall and Moll (1975). We estimated benthic algal standing crop
 using two methods, ash free dry mass (AFDM) and Chlorophyll-a (Chl-a)
 analysis. We also quantified the presence of filamentous green algae by
 presence/absence counts on 0.25-m increments along each cross section.
 Detailed methods for primary production and algal standing crop are
 described in Appendix S1 and S2, respectively.
 <em>Invertebrate drift, standing crop, and
 infall</em> — To quantify the phenology of invertebrate salmonid
 prey, we measured invertebrate drift from riffles entering pools, the
 standing crop of benthic invertebrates on riffle and pool cobbles, and the
 infall of terrestrial and adult aquatic invertebrates onto the surface of
 pools. Invertebrates were sampled at six total sites (3 Elder Creek pools
 and 3 Porter Creek pools) on five dates over the summer. Detailed methods
 for invertebrate data collection are included in Appendix S3.
 All invertebrate samples (drift, standing crop, and infall) were
 preserved in the field in labeled 50ml centrifuge tubes filled with 90%
 ethanol. In the laboratory, drift and benthic samples were sorted and
 invertebrates identified to family or genus (Merritt et al. 2008) under
 10X magnification. Each invertebrate was measured to the nearest 0.5mm
 under a dissecting scope and biomass (mg dry mass) was estimated from
 family or order-specific length-weight regressions (Benke et al. 1999,
 Sabo et al. 2002).  These data were used to define energy content
 (joules/mg) in the bioenergetic model following Rosenfeld and Taylor
 (2009). <em>Bioenergetics</em> — The
 seasonal change in growth potential for drift foraging O. mykiss was
 estimated using a drift foraging bioenergetic model (Caldwell et al. 2018,
 Rosenfeld and Taylor 2009). The model was developed in R version 3.5.1.
 and is based on equations from Rosenfeld and Taylor (2009) and Hayes et
 al. (2000) and is the same model used in Rossi et al. (2021b). Growth
 potential was inferred from the modeled Net Rate of Energetic Intake
 (NREI, joules time-1), estimating the energy acquired by a juvenile fish
 for growth (gross energy intake – swimming and other metabolic costs).
 Gross energetic intake is a function of drift concentration
 (mg/m<sup>3</sup>), discharge rate through the foraging
 volume, fish size, prey size and capture probability (Caldwell et al.
 2018, Rosenfeld and Taylor 2009). Swimming costs are a function of fish
 size and focal point flow velocity and water temperature (Caldwell et al.
 2018, Rosenfeld and Taylor 2009). Water temperature was incorporated into
 the swimming costs (Rosenfeld and Taylor 2009); however, we assumed a
 constant energy assimilation efficiency of 0.6 (Tucker and Rasmussen
 1999). The fish focal point velocity (measured at 6/10ths depth) and drift
 concentration were measured at the thalweg location on cross section 2 at
 the head of each pool (Fig. 3). This depth was chosen based on our
 qualitative observations of <em>O. mykiss</em> foraging focal
 point depth which was primarily in the lower half of the water column in
 both streams. We maintained this depth for consistency across the
 seasons. We modeled NREI for a 100mm (fork length)
 drift-foraging <em>O. mykiss</em> at a single foraging
 location in the channel thalweg. We considered the head of the pool the
 best indicator of changing drift foraging profitability for seasonal
 comparisons of drift foraging growth potential across streams (Harvey et
 al. 2006, Smith and Li 1983 Van Leeuwen et al. 2011, Rossi et al. 2021b)
 and 100mm was representative of the 1+ fish that most commonly occupied
 the head of the pool. We only modeled one size class of trout since our
 objective was to model seasonal changes in NREI rather than size-specific
 growth potential. Caldwell et al. (2018) also noted that NREI for
 different size classes of drift foraging <em>O. mykiss</em>
 and foraging locations downstream from the head of the pool locations
 followed a similar seasonal pattern over the hydrograph recession,
 although the magnitudes changed. The model was run for n = 3 pools in each
 stream, and n = 5 dates for a total of 30 model runs (3 pools × 2 streams
 × 5 dates).  Other factors affecting growth potential (e.g. non-drifting
 prey and impacts from dissolved oxygen) were described qualitatively (see
 Discussion). <em>Growth, and lipid
 allocation</em> — Since growth potential (modeled NREI) may differ
 from realized growth (Hughes et al. 2003, Piccolo et al. 2014), we caught
 pool-dwelling steelhead to evaluate seasonal changes in the size
 distributions and fish density, and to collect individual growth and lipid
 content data. Fish were collected using three-pass backpack electrofishing
 from 3 study pools in each stream (Smith-Root backpack electrofisher model
 LR24). All recaptured fish were remeasured for length and mass, allowing
 us to estimate June to July growth.  We did not recapture enough fish
 during  the April - May interval or the July - September  interval  to
 estimate growth. In addition to growth, lipid content was estimated using
 a non-invasive handheld device, the Distell Model 992 Fish Fatmeter
 (Distellc Inc., West Lothian, Scotland—https://www.distell.com). Lipid
 allocation in salmonids is used as indicator of stored energy
 availability. In O. mykiss, lipid levels have been correlated to survival
 during periods of resource scarcity (Biro et al. 2004). A detailed
 description of fish mark and recapture for growth, density, and estimation
 and lipid estimation is included in Appendix S4.
 <strong>Data Analysis</strong> We
 used descriptive statistics to quantify the habitat, food web, and
 resultant growth potential phenologies for <em>O. mykiss</em>
 in Elder and Porter Creek and to compare seasonal trends in both streams
 against our directional predictions. We also compared these seasonal
 patterns against our graphical model (Fig. 1).  In addition we used a
 post-hoc bioenergetic analysis to evaluate our predictions about the
 trends and drivers modeled seasonal of growth potential(1-4). We extracted
 the modeled swimming costs and energy intake to determine their seasonal
 variance and relative influence on patterns of growth potential.
description: Files are .csv of tabulated data. For details, see Methods.