10.5061/DRYAD.9KD51C5DT
Menge, Bruce
0000-0002-2981-9517
Oregon State University
Chan, Francis
Oregon State University
Rose, Jeremy
Oregon State University
Sanford, Eric
University of California, Davis
Raimondi, Peter
University of California Santa Cruz
Blanchette, Carol
University of California, Santa Barbara
Gouhier, Tarik
Northeastern University
Data from: Biogeography of ocean acidification: differential field
performance of transplanted mussels to upwelling-driven variation in
carbonate chemistry
Dryad
dataset
2020
National Science Foundation
https://ror.org/021nxhr62
OCE-1041240, OCE-1220338, OCE-0956197, DEB-1-50694
2020-07-28T00:00:00Z
2020-07-28T00:00:00Z
en
https://doi.org/10.1371/journal.pone.0234075
4865433 bytes
2
CC0 1.0 Universal (CC0 1.0) Public Domain Dedication
Ocean acidification (OA) represents a serious challenge to marine
ecosystems. Laboratory studies addressing OA indicate broadly negative
effects for marine organisms, particularly those relying on calcification
processes. Growing evidence also suggests OA combined with other
environmental stressors may be even more deleterious. Scaling these
laboratory studies to ecological performance in the field, where
environmental heterogeneity may mediate responses, is a critical next step
toward understanding OA impacts on natural communities. We leveraged an
upwelling-driven pH mosaic along the California Current System to
deconstruct the relative influences of pH, ocean temperature, and food
availability on seasonal growth, condition and shell thickness of the
ecologically dominant intertidal mussel Mytilus californianus . In 2011
and 2012, ecological performance of adult mussels from local and commonly
sourced populations was measured at 8 rocky intertidal sites between
central Oregon and southern California. Sites coincided with a large-scale
network of intertidal pH sensors, allowing comparisons among pH and other
environmental stressors. Adult California mussel growth and size varied
latitudinally among sites and inter-annually, and mean shell thickness
index and shell weight growth were reduced with low pH. Surprisingly,
shell length growth and the ratio of tissue to shell weight were enhanced,
not diminished as expected, by low pH. In contrast, and as expected, shell
weight growth and shell thickness were both diminished by low pH,
consistent with the idea that OA exposure can compromise shell-dependent
defenses against predators or wave forces. We also found that adult mussel
shell weight growth and relative tissue mass were negatively associated
with increased pH variability. Including local pH conditions with
previously documented influences of ocean temperature, food availability,
aerial exposure, and origin site enhanced the explanatory power of models
describing observed performance differences. Responses of local mussel
populations differed from those of a common source population suggesting
mussel performance partially depended on genetic or persistent phenotypic
differences. In light of prior research showing deleterious effects of low
pH on larval mussels, our results suggest a life history transition
leading to greater resilience in at least some performance metrics to
ocean acidification by adult California mussels. Our data also demonstrate
“hot” (more extreme) and “cold” (less extreme) spots in both mussel
responses and environmental conditions, a pattern that may enable
mitigation approaches in response to future changes in climate.
Mussel transplants Using a standard protocol, performance of California
mussels (30-45 mm total length) was quantified during 2011 and 2012
upwelling seasons [61,62,64]. We first collected mussels for pre-study
measurements and individual tagging. Under permits from the Oregon
Department of Fisheries and Wildlife and the California Department of Fish
and Game (Oregon Department of Fish and Wildlife, 2010 permit #15122 and
California Department of Fish and Wildlife S-183160003-18316-001), mussels
were haphazardly collected from the vertically middle portion of M.
californianus beds. In 2011 but not 2012, to assess genetic or persistent
phenotypic influences on mussel performance, we translocated intermingled
local-source (i.e., those from each site) and common-source (mussels from
a single site, Bob Creek, Oregon, USA). To distinguish them from
local-source mussels, common-source mussels were also marked with a bead
of epoxy. In the lab, translocation mussels were marked with a 1-2 mm
triangular notch filed on the posterior shell edge (growing lip) to
establish an indicator of initial length. Pre-outplant shell weight was
estimated using a buoyant-weight method similar to [65]. Briefly, the
process involved collecting separate mussel samples for model calibration
at Bob Creek, Bodega Marine Reserve (northern California), Sandhill Bluff
in central California and Lompoc Landing (southern California). The
buoyant weight of each “calibration” mussel was measured by placing the
live mussel on a platform submerged in water. The shells of each mussel
were pinched closed during transfer through air, to prevent the
confounding effect of air intake on buoyancy. Thus, submerged weight was
an estimate of the negatively-buoyant shell weight. Soft tissue was then
dissected from the shell and, after drying, shell weight was directly
measured. The site-specific relationship between buoyant weight and dry
shell was modeled using linear regression. The slope and intercept of each
model was then used to estimate pre-study shell weight for translocated
mussels. The Bob Creek regression model was used for Fogarty Creek and
Strawberry Hill mussels, the Bodega Marine Reserve model for Van Damme and
Bodega Marine Reserve, the Sandhill Bluff model for Terrace Point and
Hopkins Marine Station, and the Lompoc Landing model for Lompoc Landing
and Alegria. Mussel translocation After pre-outplant processing, mussels
were translocated back to the field for the April through October
upwelling season. In 2011, mussels were sorted into 5 replicate groups of
50 per site, with each group consisting of 25 local- and 25 common-source
individuals. For the 2012 season, mussels were sorted into 5 replicate
groups of 30 per site. Mussel translocation used established methods
[59]. Briefly, at each site, mussels were placed ventral side down in
cleared plots 2-5 m apart within existing mussel beds. Because bed
heights varied among sites along the coast, tidal height of transplants
varied (Table 1). We accounted for these differences by using tidal height
as a covariate in data analyses. Mussels were held in place with plastic
mesh (1-cm x 1-cm mesh) that was fastened using stainless steel lag screws
inserted into pre-drilled holes with wall anchors. Two to four weeks
later, the mesh was loosened to encourage more byssal thread production,
and then 2-4 weeks later loosened further into a “dome” to allow space for
growth while protecting the mussels from predation. Sample processing and
growth measurements Within 12 hours of collection, all mussels were placed
in seawater tables, then within two days of collection, frozen at -20oC.
During processing, mussels were thawed, measured (length, width, and depth
to the nearest 0.01 mm. Epibionts and byssal threads were removed from the
shell exterior, and mussels were then dissected into two constituent parts
– shell and soft tissue. These were dried separately at 80ºC for ≥ 5 days
then weighed to the nearest mg. Shell-length growth was measured as mm
new shell accumulated between the pre-study notch and the growing edge of
the shell. Growth was standardized by dividing by initial length.
Shell-weight growth was measured as the difference in pre- and post-study
shell weight (g), standardized to the individual’s estimated pre-outplant
shell weight and the study-season duration at each site. Shell-weight
growth of each mussel was calculated as the difference between the
measured dry shell weight at the end of the season and the pre-season
shell weight as determined by the previously described buoyant weighting
method. The condition index (unitless) of each mussel was measured as the
dry tissue mass per total (tissue + shell) dry mass. Higher condition
index mussels have proportionately more soft tissue mass and may reflect
energy allocation favoring tissue development [66,67]. Higher condition
index may also reflect higher resource quality for mussel predators. Mean
shell thickness index (mg/mm2) was estimated by calculating the dry shell
mass per shell surface area, with surface area (A ) calculated by the
ellipsoid model A=l×h2+w21/2×π÷2 , where l , h , and w are mussel length,
height and width, respectively [68]. All shell dimensions were measured to
the nearest 0.1 mm, and shell weight was measured to the nearest 0.01g.
The resulting index assumes a constant crystalline density of the shell
structure. Major predators of M. californianus include Nucella whelks
consume mussels through holes drilled their shells. Therefore, mean shell
thickness index may correspond to drilling susceptibility [69].
Temperature Temperature data were obtained using mussel biomimetics, which
mimic the thermal properties of living mussels [70,71]. Each logger
consisted of a thermistor-based temperature recorder (Tidbit logger, Onset
Computer Corp., Bourne, MA) embedded in an epoxy mold shaped like an adult
mussel. Using Z-spar epoxy, one to two loggers were deployed per site near
replicate mussel plots, then covered with a plastic mesh cage to mimic
conditions experienced by the transplanted mussels. Loggers recorded
temperatures at 10-minute increments. Air and water temperature data were
separated [72] and used to calculate mean temperatures by site and
upwelling year. Phytoplankton abundance Phytoplankton are the primary food
of M. californianus [73]. Food availability was quantified using
chlorophyll-a concentrations ([Chl-a]) as a proxy for phytoplankton
abundance. Chl-a was measured by periodically collecting water samples in
opaque bottles during low tide at each site [74-76]. Replicate (n=3)
bottle samples were collected at low tide from the shore at ~0.5m below
the water surface. In the field, fifty ml of water was passed through
25-mm pre-combusted 0.7-µm Whatman GF/F glass-fiber filters. Filters were
placed on ice and taken to the lab where Chl-a concentrations were
quantified using a fluorometer. Because discrete sampling was not
consistently conducted at all study sites in both study years, for
analysis we averaged all bottle samples across all sample years creating
site-specific long term mean summaries of Chl-a data. Prior research has
shown spatial variability but temporal consistency in the levels of Chl-a
among subsets of the sites used in this study [74,77]. pH measurements pH
data were collected at 10-minute intervals using autonomous sensors
deployed at each site within 20 meters from the mussel plots. Sensors were
attached to the rock using methods similar to the mussel translocations
except that they were held down with stainless steel mesh. Care was taken
to ensure that the sensing electrode remained wet even at low tide.
Details on these custom-designed sensors can be found elsewhere [49,78],
but briefly each was based on an ion-sensitive Honeywell Durafet® with an
integrated data logger and power supply [79]. Sensors were calibrated
either directly against certified reference materials or indirectly using
spectrophotometric pH samples that were calibrated using certified
reference materials. pH is reported on the total hydrogen ion
concentration scale [80]. Calibrations occurred pre- and post-deployment
for all sensors. To spot-check sensor performance, sensor data were
periodically (2-4 weeks) compared to discrete water samples collected at
all sites except at the two southern California sites in 2012 (Lompoc
Landing and Alegria ). To investigate how different aspects of the pH
environment might influence mussel performance at each site and in each
study year, we compiled summary statistics for the pH mean, standard
deviation, and percentages of exposure below two thresholds: pH 7.8 and pH
7.7. These thresholds were chosen for their alignment with model
predictions of average global pH conditions by the year 2100 [4,5,6].
Using tide tables, sensor data collected when tides were below the sensor
were excluded from analysis.
Robomussel temperature data Field Descriptors datetime Calendar date and
time of sensor measurement yearday Julian day and time of sensor
measurement temp_c Measured temperature in degrees Celsius tide_m Tidal
height (to nearest 0.01 meters) at time of measurement air20/water0
Boolean notation indicating if mussel sensor was exposed to air (“20”) or
under water (“0”) at time of measurement cutoff_m Tidal height (to nearest
0.01 meters) at which sensor was located in the field Site information;
NA=no data Field Descriptors Site Location where mussels were transplanted
during study duration; FC=Fogarty Creek, SH=Strawberry Hill, VD=Van Damme
State Park, BM=Bodega Marine Reserve, TP=Terrace Point, HM=Hopkins Marine
Station, LL=Lompoc Landing, AL=Alegria Lat Latitude of study site Long
Longitude of study site outplant.date Calendar date that mussels were
transplanted to the field at study outset recover.date Calendar date that
mussels were recovered from the field at the end of the study season
days.exposed The duration in days for which mussels were exposed to field
conditions Year Year of study – 2011 or 2012 chla.mean Long-term mean of
chlorophyll-a concentration, measured by bottle sampling chla.sd Long-term
variability of chlorophyll-a concentration, measured by bottle sampling
chla.n Total number of bottle samples collected to establish mean and sd
tidal.height.mean Average tidal height (to nearest 0.001 meters) of
transplant replicates Regression mussels; NA=no data Field Descriptors
ID Unique numerical identifier site Site of origin; BC=Bob Creek,
BY=Bodega Marine Reserve, LP=Lompoc Landing, SB=Sandhill Bluff buoyant_wt
Weight (to nearest 0.01 grams) of live mussel when suspended in seawater
length Total length of mussel shell (to nearest 0.1mm) measured from umbo
to posterior shell margin width Maximum width of mussel shell (to nearest
0.1mm) measured from dorsal to ventral margins girth Maximum breadth of
mussel shell (to nearest 0.1mm) measured across the breadth of both shell
halves when closed tin_wt Weight (to nearest 0.01 grams) of tin dish in
which mussel soft tissue was dried shell_wt Weight (to nearest 0.01 grams)
of dry mussel shell tissue_dry_wt Weight (to nearest 0.01 grams) of dry
soft tissue; Includes tin dish weight since dish was inseparable from
desiccated tissue. Transplant mussels; NA=no data Field Descriptors ID
Unique numerical identifier Site Location where mussels were transplanted
during study duration; FC=Fogarty Creek, SH=Strawberry Hill, VD=Van Damme
State Park, BM=Bodega Marine Reserve, TP=Terrace Point, HM=Hopkins Marine
Station, LLPU=Lompoc Landing, AL=Alegria year Year of study – 2011 or 2012
replicate Experimental transplant replicate source Identifies if mussel
was sourced from the local (“L”) transplant site (see “site” field) or
common-source (“C”) site of Bob Creek, OR init_length Length of mussel
shell (to nearest 0.1mm) measured from umbo to the notch filed on the
posterior margin before transplanting mussel to the field post_length
Total length of mussel shell (to nearest 0.1mm) measured from umbo to
posterior shell margin after mussel was recovered from the field growth
Shell length (to nearest 0.1mm) between pre-study notch and post-study
posterior margin of the shell post_height Maximum width of mussel shell
(to nearest 0.1mm) measured parallel to line from umbo to the opposite
shell margin after mussel was recovered from the field post_girth Maximum
breadth of mussel shell (to nearest 0.1mm) measured across the breadth of
both shell halves when closed after mussel was recovered from the field
tin_wt Weight (to nearest 0.01 grams) of tin dish in which mussel soft
tissue was dried shell_wt Weight (to nearest 0.01 grams) of dry mussel
shell after mussel was recovered from the field tissue_dry_wt Weight (to
nearest 0.01 grams) of dry soft tissue after mussel was recovered from the
field; Includes tin dish weight since dish was inseparable from desiccated
tissue.