DISCUSSION
Realistic assemblages of the intertidal canopy-forming rockweed,Silvetia , and its understory, exhibited season-specific responses
to ocean climate change. Future climate scenarios similar to those
projected by the IPCC acted to suppress Silvetia growth, reduceSilvetia photosynthetic efficiency (measured by quantum yield),
and shift the understory seaweed communities. These effects, however,
were season-specific; both future climate scenarios (RCP 2.6 & 4.5)
indirectly influenced the understory by reducing Silvetia cover
in summer, but only the more severe scenario (RCP 4.5) produced the same
effect in the winter. Similarly, future climate reduced Silvetiaphotosynthetic efficiency in the summer but not the winter. The
summertime reductions in Silvetia cover under future climate
scenarios were then associated with shifts in the understory
communities. Specifically, future climate scenarios reducedCentroceras and Corallina cover but had season-specific
impacts on Chondracanthus and Laurencia (e.g.,Chondracanthus increased in summer but decreased in winter).
Similarly, field removals of Silvetia shifted the understory
community, but only in the fall when the understory was intact.
Season-specific impacts of climate change (e.g., in the mesocosm trials,
RCP 2.6 suppressed Silvetia and shifted the understory during the
summer trial but not in the winter trial) suggest that seasonal factors
may determine how climate change affects intertidal algal communities.
This phenomenon has been observed for various taxa such as insects
(Johansson et al. 2020), plants (Gordo & Sanz 2010), and migratory
animals (Robinson et al. 2009). Season-specific impacts are commonly
attributed to the intersection of climate change induced warming with
critical, season-dependent phenological periods such as mating,
flowering, or migration. With Silvetia , climate change may
exacerbate mortality during the summer when it encounters temperatures
near its thermal maximum, which may then reduce reproduction and
recruitment in the winter (Moeller 2002). In support of this hypothesis,Silvetia only grew in our mesocosms during the winter trial when
photosynthetic quantum yields were higher and abiotic conditions were
more benign. In summer, relative to winter, seawater pH was lower,
seawater temperatures and irradiances were higher, and peak irradiance
coincided more frequently with periods of low tide, all of which may
have suppressed Silvetia biomass during the summer trial.
The season-specific impacts of RCP 2.6 versus the consistent impacts of
RCP 4.5 on
Silvetia suggests the potential for recovery from climate change
effects if less intense climate change scenarios are realized. For
example, Silvetia encountering biomass loss under RCP 2.6
conditions in the summer may be able to recover in the winter, though
whether other processes such as reproduction will also recover remains
untested. In support of this hypothesis, we only observedSilvetia growth in the winter trial when Silvetia was
exposed to Ambient and RCP 2.6 climates. The realization of RCP 2.6,
which hinges on extensive and immediate mitigation of greenhouse
emissions, is unlikely given current trends while RCP 4.5, which calls
for substantial mitigation efforts by the year 2040, appears more
realistic. Consequently, the potential for recovery from season-specific
impacts of future climates may be rapidly waning. However, becauseSilvetia individuals were replaced between trials, it is unclear
if Silvetia is capable of net growth, or perhaps longer-term
acclimation, when it experiences future climate conditions through
consecutive seasons. More comprehensive conclusions would be drawn from
experiments assessing year-round climate change impacts on the same
individuals of Silvetia .
Taxa resistant to direct effects of climate change may be susceptible to
indirect effects via changes to canopy-forming species (Edwards &
Connell 2012). For example, ocean acidification and warming can
negatively affect canopy-forming species (Brown et al. 2014, Shukla &
Edwards 2017) but often do not directly impact turfing algae, such asCentroceras (Ober et al. 2016, Christie et al. 2019). Consistent
with this finding, Centroceras increased under future climate
scenarios relative to Ambient in the absence of Silvetia during
the winter mesocosm trial. In summer, however, Centrocerasrequired a Silvetia canopy for survival regardless of climate
treatment (Fig. S1). This demonstrates how the climate-mediated loss of
canopy-forming species may impair members of the understory assemblage
which are otherwise resistant to the direct effects of climate change
and that this interaction may only occur seasonally.
Understory seaweeds that are sensitive to direct impacts of ocean
acidification, such as calcifying taxa like Corallina , may be
particularly prone to climate change because of both direct (Kim et al.
2020) and indirect effects. Ocean acidification can directly reduce
growth and performance of calcifying seaweeds, in part because of
reductions in calcification rates (Cornwall et al. 2022). Ocean
acidification can also indirectly affect these understory species by
reducing the cover provided by canopy-forming species, thereby
increasing desiccation, photoinhibition, and pH stress (Irving et al.
2004, Schmidt et al. 2011, Hirsh et al. 2020, Fales & Smith, 2022).
Although we are unable to parse out all these effects here, the trend
for Corallina loss under future climate scenarios in the presence
of Silvetia (that occurred in both seasons) and a weak or lack of
a trend in the absence of Silvetia suggest that some of theCorallina declines were indirect effects of canopy loss unrelated
to an increase in photic or desiccation stress.
The effects of climate on fleshy algae such as Laurencia andChondracanthus followed different patterns relative to turf and
calcifying algae. For example, during the winter trial,Chondracanthus and Laurencia both exhibited declines under
future climate scenarios relative to Ambient when without a canopy,
while Centroceras increased under these conditions. This decline
in Laurencia and Chondracanthus could have resulted from a
lower thermal tolerance threshold, the lack of a biomechanism to utilize
high concentrations of CO2 such as carbonic anhydrase,
or a heavier reliance on canopies for physical and chemical amelioration
(Jueterbock et al. 2013, Kim et al. 2016, Hirsh et al. 2020). These
patterns, potentially driven by physiological differences and species
interactions, indicate a differing response between seaweed functional
groups to canopies, seasonality, and the interaction of these factors
with climate change.
Under natural field conditions, assemblages also shifted in response toSilvetia loss depending on the season and successional stage. In
the fall, the assemblages in the Understory Cleared plots did not differ
between Silvetia Present vs. Absent treatments, indicating a lack
of reliance on Silvetia canopies by early successional species,
which are generally robust to abiotic stressors (Table S12, Sousa 1979,
Farell 1991). The mature assemblage of Understory Full plots, however,
had diverged between Silvetia treatments and the effect ofSilvetia canopies on these assemblages had similarities to the
mesocosm experiment (Table 2). For example, in this survey and the
winter mesocosm trial, Corallina declined in the absence of a
canopy while Centroceras increased. When resurveyed two months
later in winter, the mature assemblages had homogenized, perhaps due to
the recovery of species sensitive to Silvetia loss following
cooler conditions (Cheung-Wong et al. 2022). The assemblages within
Understory Cleared plots, however, had now shifted betweenSilvetia treatments, possibly because late-successional stage
species, such as Gelidium and Gigartina , which are better
competitors for space but are also reliant on canopies at higher
elevations, had developed (Sousa 1979). However, because bare rock was
the primary contributor of dissimilarity, this shift may have also
resulted from unrelated factors (e.g., stochastic scouring during winter
storms). Regardless, if Silvetia cover declines under future
climate conditions as seen in our mesocosm experiment, shifts in natural
assemblages, such as those observed in our field experiment, will likely
occur.
Climate change-mediated shifts in the Silvetia assemblage will
ultimately reduce or restructure intertidal communities, altering
individual fitness, species interactions, and ecosystem services
(Kroeker et al. 2020). Declines of Silvetia alone will lead to
loss of nursery habitats for subtidal species during periods of
submergence (Schmidt et al. 2011, Vercaemer et al. 2018) and a lack of
refuge for mobile and sessile intertidal species during periods of
emergence (Sapper & Murray 2003). Loss of canopy-forming seaweeds can
also result in reduced primary production (Edwards et al. 2020, Sullaway
& Edwards 2020, Spector & Edwards 2020), especially in the upper-mid
intertidal zone (Vadas et al. 2004). Indirect effects of canopy loss
will include reduction of available habitat for understory species
facilitated by canopies as well as the ecosystem services they provide
(Fales & Smith 2022). For example, future climate scenarios in our
mesocosms led to decreases in Corallina . Because Corallinaprovides settlement cues and substrate for invertebrate larvae (Morse &
Morse 1984, Seabra et al. 2019), climate change may reduce invertebrate
recruitment via changes to Silvetia and Corallina .
Additionally, if the understory also facilitates a canopy-forming
species (e.g., by providing a hospitable surface for the settlement of
canopy-forming recruits), then climate-mediated canopy loss may lead to
feedback loops, causing further canopy declines and exacerbating
disruption at the community level.