proliferation of harmful algal blooms (Richard et al., 2022).
Krishna et al. 10.3389/fmars.2024.1481734Nutritional composition and thus the commercial value of oysters
and mussels decrease under combined acidi?cation and warming
stress (Tate et al., 2017).
4.4 Research gaps
Effects of different stressor levels on populations in orthogonal
experimental designs are dif?cult to examine, particularly when many
stressors are involved Griffen et al. (2016). It is costly in terms of time
and resources and the inclusion of different stressor intensities may
complicate the experimental design (King et al., 2022).
We identi?ed only a few studies (only 8%) which investigated the
interactive effects of multiple stressors on ecosystem-level dynamics in
coastal waters. This has been also noted by Crain et al. (2008) in their
review of non-additive effects of human stressors in marine systems,
pointing out the existing bias towards studying single species in ex-situ
setups. Experimental determination of complex interactions in coastal
environments is challenging (Carrier-Belleau et al., 2021), and it is
dif?cult to measure stressor effects at the community or ecosystem level
in natural settings (Adams, 2003; Elliott and Quintino, 2007; Borja,
2014; Wake, 2019).
As the interactive effects at every trophic level vary, depending on
factors such as stressor magnitude and exposure duration,
measurements of multiple endpoints have to be considered while
designing the experiments on an ecosystem scale (King et al., 2022). A
?rst step would start with individual stressor studies across a wide
range of intensities to understand responses and then examine
combinations of multiple stressors across a smaller range of stressor
levels to explore interactions between them. This approach would helpVihtakari et al. (2013) suggested that warming affects larval
development, whereas acidi?cation affects the reproductive
capacity of adults.
A moderate increase in water temperature can counteract the
growth effects of reduced pH in M. galloprovincialis by allowing more
active feeding time Kroeker et al. (2014), and thus constituting an
antagonistic interaction. Mostly, however, the combined effect of OA
and warming in bivalves has been observed as negatively synergistic:
Thomsen et al. (2013), e.g., showed that heat shock proteins are
downregulated under elevated pCO2, amplifying heat stress
experienced by Mytilus edulis. Many traits may be affected by the
combination of warming and acidi?cation: for both M. edulis and
Mytilus galloprovincialis growth rate, shell size, and acid-base buffering
capacity were found to decrease (Gazeau et al., 2014; Fitzer et al., 2015).
The occurrence of further stressors along with warming and
acidi?cation exacerbates the negative synergistic effects. Adding
hypoxia impairs the ?tness of marine mussels by reducing the
activity of digestive enzymes (Khan et al., 2020). Likewise, an
increased frequency of extreme climatic events has been reported
to impact bivalve species at 12 coastal regions around the
Mediterranean (Rodrigues et al., 2015).
Multi-stressor effects on bivalve species propagate to the entire
coastal ecosystem via the ecosystem services provided, foremost the
habitat creation and water quality improving ?ltration services, but
also food provisioning. The presence of bivalves prevents theFrontiers in Marine Science 09to identify critical stressors for multiple stressor experiments. Another
dif?culty in studying interactive effects across ecosystems is the
variable response time of different taxa to a variety of stressors
(Griffen et al., 2016; Turschwell et al., 2022). Furthermore, the time
at which stressor response is measured can also affect the classi?cation
of the interaction type (Garnier et al., 2017). While studying and
quantifying the direct cumulative effects of multiple stressors
themselves is challenging, their indirect effects further complicate
the problem. This has implications for coastal management, as they
do not follow typical cause-and-effect pathways but signi?cant modify
ecosystem responses (Adams, 2005; Gladstone-Gallagher et al., 2023).
Thus, it has been suggested to focus on both the direct and indirect
effects of stressor interactions for effective stressor management
(Gladstone-Gallagher et al., 2023).
Despite the complications in measuring ecosystem responses to
multiple stressors, some efforts have been made in this direction. With
the advent of mesocosm experiments, it has become possible to study
ecosystem-level responses and effects of climatic and anthropogenic
stressors in quasi-natural habitats (Stewart et al., 2013). For example,
the mesocosm experiments of Pansch and Hiebenthal (2019) facilitated
assessment for a whole range of effects of multiple stressors
(temperature, salinity, pH, light) on benthic ecosystems and
communities. Given the large number of stressor combinations and
species in coastal ecosystems, it will remain unfeasible to fully
understand multi-factorial stressor effects by means of observational
experiments. Therefore, other approaches such as modelling and expert
opinions have been proposed by Halpern et al. (2007); Griffen et al.
(2016); Stelzenmüller et al. (2024). For modelling, a 3-tiered approach
has been proposed. First, understandmechanistically the stressor effects
at the individual level Griffen et al. (2016), and then scale these to
population-level responses and, ?nally, assess the risks for communities
across ecosystems. This practice has been adopted by some modelling
studies (Pörtner, 2012; Cornwall and Eddy, 2015; Queiro?s et al., 2015).
Other researchers propose that combining methods can improve
understanding such as aligning experiments from the beginning with
the models they aim to inform (Hodgson and Halpern, 2019).
Although we found that the majority of multi-stressor studies
focus on species-level effects, these are largely restricted to
phytoplankton and bivalves. Other taxonomic groups, such as
zooplankton, ?sh and benthic organisms, which constitute
important trophic linkages in the coastal food webs, are
underrepresented (Figure 8). It is dif?cult to manage physiologically
complex and larger organisms in manipulative experiments and to
track variable responses to the same stressors by different species of
the same group, e.g. in ?sh. Most of the multi-stressor studies
performed on seagrass are in-situ experiments where co-variations
in environmental boundary conditions make it hard to unravel non-
additive interactions (Stockbridge et al., 2020). As a consequence, we
could not identify a trend in reported interactive effects for seagrass or
?sh. Intra-speci?c responses in higher organisms (such as ?sh) vary
depending on stressor magnitude and duration (Barton, 2002).
Stressor-driven changes at higher trophic levels trigger cascading
effects that impact the food web dynamics in coastal ecosystems
(Pinnegar et al., 2000; Scheffer et al., 2005; Murphy et al., 2020). The
same applies to the coupling of pelagic and benthic ecosystems. In
our analysis, we found that only a few studies focused on benthicfrontiersin.org