Benthic-based contributions to climate change mitigation and adaptation

1. Introduction

The effects of anthropogenic activity and climate change are becoming so pervasive that there is wide recognition that human intervention is needed to both mitigate climate change and to promote adaptation [1]. In response, many countries are contemplating, or beginning to implement, ambitious adaptation plans [2] that include a portfolio of natural and nature-based solutions, an umbrella concept [3–5] that builds on approaches that collectively use the features and complex system processes of ecosystems to achieve multiple benefits for nature, the economy and society [6–8]. Although the concept of nature-based solutions is gaining momentum, and is undergoing a process of maturation [9–11], emphasis has largely been placed on context-specific actions aimed at improving broad, and often unspecified [12], aspects of urban regeneration [13], energy demand [14] or well-being [15], disaster management and resilience [16], carbon storage [17] or physical coastal protection [18–22]. While these actions have merit because they can lead to beneficial outcomes, substantial scientific evidence for the interconnectivity of ecosystems [23–25], and an awareness that the provision of ecosystem services is not restricted to areas within arbitrarily defined boundaries [26], means that efforts to improve resilience to climatic-related phenomena fall short of their potential as the default is to assume that ecosystem services are spatio-temporally constrained. Contributions from natural systems located beyond the immediate vicinity of highly populated areas tend to be overlooked [27]. In these instances, what is often forgotten is that the social and economic spatial scale at which positive outcomes are realized can extend beyond the physical spatial scale of ecosystem processes or habitats. Storm protection by saltmarshes and mangroves, for example, can provide protection from inclement conditions in the immediate vicinity, but can also benefit populations situated further inland by preventing storm surges, salination or inland flooding [28], thereby minimizing follow-on social and governance challenges that tend to accumulate in the wake of a storm. Failure to recognize the contribution of ecosystems beyond the focal area, at least in part, stems from a predisposition to consider familiar habitats that people routinely interact with as being key to the solution, while disregarding habitats that are more inconspicuous, seldom or indirectly accessed, or otherwise catalogued as unconnected. It is easier to comprehend, and therefore to effectively manage, interactions between ecosystems, or between social and ecological systems that are proximally located, and considerably more difficult to understand the multiple steps that may link distant systems. Yet the effects of climate change are global, and systems are linked across time and space, which together demand a comprehensive response. As public scrutiny of the extent and effectiveness of political action increases [29] and the need to meet adaptation targets intensifies [30], the appetite to accelerate and scale-up instances of transformative change is growing [31] and provides impetus to explore the potential of underutilized or previously untapped natural resources.

Oceans exert a major control on global climate [32] and they connect disparate ecosystems in ways that can shape how climatic forcing is expressed across entire terrestrial and marine regions [33]. They are also vast and, therefore, offer great potential to contribute to safeguarding the resilience of humanity [34], already absorbing greater than 90% of the excess energy in the climate system [35] and greater than 30% of anthropogenic CO₂ emissions [32], as well as contributing negative feedbacks to counteract the effects of warming at higher latitudes [36]. Yet, with the exception of the use of habitat-forming assemblages to counter coastal wave and wind action (e.g. sand dunes, coral reefs, reef-forming bivalves, seaweed and seagrasses, salt marsh vegetation, mangroves; reviewed in [37–39]), the broader role of marine habitats in mitigating or avoiding other climate change impacts has received much less attention. Offshore soft-sediment ecosystems, in particular, are not a prominent feature of the nature-based solutions narrative, despite the fact that much of the prima facie evidence for the effectiveness of eco-engineering to support mitigation measures emanates from, an albeit small proportion of, benthic habitats [40]. This oversight is surprising, as marine sediments cover an area greater than all other habitats on Earth combined [41] and can host impressive levels of biodiversity (coast, 803 species in 10 m² [42]; deep sea, 798 species in 21 m² [43]) that regulate biogeochemical cycling [44], climate active gases [45], ocean chemistry [46] and the long-term removal of carbon from the ocean–atmosphere system [47,48]. Indeed, the effects of warming [49], acidification [50], deoxygenation [51], sea-level rise [52] and their interactions [53], can be appreciably modified by the particle reworking and ventilatory behaviour of sediment-dwelling invertebrates and, depending upon the seasonal timing of extreme climatic events, their activities can either exacerbate, buffer or alleviate the long-term directional effects of forcing [54]. However, the capacity of benthic environments to continue to moderate change in this way is being challenged on an industrial scale by a multitude of human pressures [55] that can frustrate biodiversity-function relations [56,57]. This immediately raises the question of whether coastal and offshore benthic environments could be better managed to temper the effects of climatic associated events and minimize CO₂ emissions at particular times of the year, or for a specific set of circumstances, and, if so, encourage processes of innovation that could usefully contribute to mitigation and adaptation pathways? To initiate this conversation, here we briefly review the potential for benthic systems to prevent, mitigate or enhance the impacts of climatic forcing, highlighting theory and practice that show most promise given the long-term effects anticipated prior to, and beyond, climate stabilization [58]. As the major responses of benthic systems to climate change have been extensively covered elsewhere [59], we restrict our review to the consideration of species-climatic forcing interactions that are amenable to management and most likely to make a difference to mitigation obligations.

2. Harnessing the benthos

Adaptation to climate risks that can no longer be avoided is fundamental to the global response to climate change, but it is clear that the articulation of adaptive measures is more exercised in safeguarding the continuity and economic viability of certain sectors through changes in practice (e.g. farming and fishing [60]), than it is in widening the adaptation search space to incorporate the influence of environment and ecology that can alter overall levels of resilience [61,62]. In the marine benthos, the latter might include the conservation, restoration or management of functionally important species and ecosystem processes [63], improving the growth and phenotypic/genotypic potential of commercial species (algae, crustaceans, molluscs and fish) under climate change [64], or the repositioning of aquaculture or fishing activity to regions that offer buffering capacity from warming or acidification [65,66]. There is also scope for using benthic environments to contribute to terrestrial-based problems, such as supplementing cattle food with algal derivatives to lower methane production [67]. Most of these strategies are in their infancy, or not yet established, and, while the frameworks and principles of adaptation planning are routinely presented in the scientific literature, there are a limited number of examples where adaptation actions have been physically implemented and formally evaluated [68,69]. Moreover, the current repertoire of species, habitats and intervention possibilities considered is limited. Nonetheless, the literature base necessary to support the development of adaptation measures exists and is building for many species and habitats; for example, we have a good idea of the pace [70] and spatio-temporal expression [71] of climate change, which species are most vulnerable to ocean acidification and warming [72,73], what engineering materials [74] and habitat configurations [20,75] are most eco-beneficial, and the location of benthic communities likely to contribute most to nutrient and carbon dynamics [76]. We also have some understanding of the feedbacks associated with changes in species behaviour and species interactions in naturally assembled communities under future climate scenarios [57], and how context-specific system attributes and local management can moderate impact [54,77]. Despite the availability of the evidence, it has seldom been collated and expressed in this way for a benthic setting. It is our view that the assembly of such information, and other similar narratives, will be scientifically instructive and form an invaluable resource for decision-makers tasked with relocating people or business, establishing or diversifying sources of food or income, or when performing cost-benefit analyses prior to changing practice to improve sustainability.

While exemplars of adaptation are in short supply for offshore marine systems, interventions to mitigate against the effects of climate-related change are more common, but conclusions are mixed and lack consensus [78]. In the marine benthos, most work has involved the management of nutrients to control the export and sequestration of carbon (reviewed in [79]) and has focused around the use of saltmarsh, macroalgae, mangroves, seagrass and shellfish. Notably, these include the dominant primary producers in coastal habitats which, following detachment, can be sequestered in offshore sediments, including the deep sea [80], a fraction that is often missed from global budgets. However, the provenance and fate of vegetated ecosystems are largely unknown because the contribution of different primary producers to organic carbon and nutrient pools in depositional marine environments has not been distinguished [81]. In coastal and shelf regions, longline mussel farming is emerging as a tool to remove nutrients and counteract the negative effects of eutrophication, while also providing food, local employment and other environmental and economic benefits [82]. Early indications are that full-scale mitigation cultures can achieve a higher impact on basin-scale water quality parameters than equivalent land-based measures [83], but mussel farms are not necessarily a cost-effective option relative to other abatement measures [84]. They also generate additional environmental impacts, such as excessive enrichment of the seafloor through faecal pellet production, that require supplementary remedial solutions which, ironically, could be tackled by introducing bioturbating fauna to enhance organic matter decomposition [85]. An alternative mitigation mechanism is restoration of mussel, oyster or other bivalve populations, as shellfish reefs contain significant pools of carbon, facilitate atmospheric CO₂ drawdown via filtration and biodeposition [86,87], and also seem to reduce coastal flood risk cost relative to complementary grey (structural) or policy measures [88]. The success or otherwise of such ventures is, however, often viewed through the lens of a small subset of response variables. Should a more holistic view of farmed or restored shellfish reefs be quantified and monetized, expenditure on such mitigation options may promote public subsidy and hasten investment and trading mechanisms that will lead to their growth [89]. Indeed, concepts such as living shorelines, where multiple habitats are engineered together to provide multiple benefits, are rapidly emerging (e.g. the coastal CO₂ removal belt in Korea [69]), but maximizing habitat structure does not necessarily result in higher levels of function or enhanced multiple benefits as is so often assumed [90].

Interventions to mitigate the consequences of climate change hold much promise in offshore sediment systems, as concepts of ecological succession, habitat recovery [91–93] and ecosystem engineering [94,95] are particularly well developed (figure 1), and the functional role of fauna are well known and can be applied generically [96]. This presents the possibility of controlling bioturbation to prevent carbon loss or enhance carbon sequestration, modify sediment erosion thresholds, or generate hotspots of climatically beneficial activity through the introduction or removal of specific species from targeted functional groups [85]. Emissions of carbon dioxide, nitrous oxide and methane linked to the formation of biogenic mounds have been resolved at a local level by modifying tidal flushing regimes to deter mound-building species and by direct control of specific populations [97,98]. Manipulations such as these tend to focus on positive species interactions that reinforce ecosystem processes [38,99], but there are also examples of using negative species interactions to improve restoration outcomes. For example, the antagonistic relationship between the sediment-destabilizing lugworm Arenicola marina and the sediment-stabilizing seagrass Zostera noltii can be moderated by adding a shell layer below seagrass transplants to reduce lugworm density and restore sediment stability to preferentially support the proliferation of seagrass, thereby reducing ocean acidification through growth-related CO₂ removal [100]. Indeed, there are numerous examples in the literature that are reinterpreting species interactions within a climate solutions framework but, while most offer intuitive and credible actions, they lack ambition in terms of being of sufficient scale to make meaningful contributions to climate mitigation. Larger scale interventions will require different approaches that move beyond individual species. It is known that sediment-dwelling invertebrates are important in modulating carbon mineralization pathways [101], and that they promote the turnover and influence the fate of carbon [102] at large scales and in response to climate fluctuations [103]. It follows, therefore, that as ocean warming is set to increase stratification and decrease nutrient availability of mid-ocean surface waters, decreases in carbon sequestration linked to reduced particulate organic carbon export from the euphotic zone to the deep ocean could be moderated through the adjustment of deposit-feeding communities [104] or via iron fertilization [105]. The latter exploits the persistence of high-nitrate, low-chlorophyll conditions in the surface waters of several large regions of the world, where various micronutrients required for photosynthesis are in low concentration. Release of limiting nutrients, such as iron, results in phytoplankton blooms that quiesce and then fall to the seafloor. While high levels of carbon drawdown have been documented over the short term (reviewed in [106]), iron fertilization may only be worthwhile if sustained over millennial timescales [107]. It is already clear, however, that the process can generate other negative climate and ecosystem consequences, including the production of additional greenhouse gases, increased oxygen consumption leading to hypoxia, toxic algal blooms and fundamental changes to benthic ecosystem structure [106,108,109]. Indeed, evaluations of other large-scale climate engineering methods, such as artificial ocean upwelling, alkalinization and solar radiation management, yield similar lists of secondary effects that have not been fully appraised [110]. Furthermore, as has been shown for the renewable energy and energy extraction sectors, both positive and negative effects can extend for hundreds of kilometres from the point of origin [111] and are likely to go undetected in the absence of appropriate monitoring programmes [112,113].

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Much of the effort diverted to establishing mitigation opportunity has so far been directed at long-term sustainability, but with the advent of more intense and more frequent extreme climatic events, it is equally important to develop short-term coping strategies. Evidence is emerging that the protection of designated areas of marine habitat can form a significant component of local and global adaptation strategies [114] by increasing the resilience of species to extreme events. Unexploited invertebrate species within a protected area grow larger and are more resistant to deviations in temperature, and they can provide larval spillover across the edges of the reserves to expedite recovery in areas that have been affected [115]. Reserves free from bottom fishing activity also tend to establish habitat-forming assemblages, which can be important in forming refugia for stress susceptible species by altering the surrounding microclimate [77]. For instance, macrophyte photosynthetic activity buffers calcifying organisms from ocean acidification [116], while the canopy of dense stands attenuate flow, shade light and reduce temperature for the associated community. Analogous phenomena occur within soft-sediment communities, where tube building polychaetes attenuate flow and stabilize the sediment [117] and infaunal bioirrigation behaviour alleviates oxygen, biogeochemical and temperature variation within the sediment profile [49,57]. However, the relief that facilitative activities can exert under times of stress are recognized and generally accepted, but have seldom been interrogated within an extreme event context [118]. Post-event interventions, such as transplanting species or building corridors to connect populations, lack examples of application, but form plausible temporary solutions for benthic environments that should be further explored and investigated.

3. Bright spots in the benthos

The pace of climate change demands the rapid adoption of pathways to transformative change, best achieved by drawing on existing experiences from a diversity of practices, worldviews, values, and regions. Examples of good practice that are positive, sustainable and scalable exist and are well documented [31], but examples from marine systems are scarce, constrained in scope, and are often viewed independently from other systems. Moreover, the vast majority of exemplar studies stem from coastal protection projects that follow a ‘rebuild by design’ philosophy, where the risk of wave and flood exposure is minimized by establishing a wide area or buffer zone that consists of multiple habitat types (e.g. low versus high salt marsh habitat, shrubland, mudflat, beach, dune, reefs, barrier islands) designed and configured to provide multi-layered protection while enhancing environmental, economic and social benefits [20]. Reliance on this limited set of marine examples, however, may mean that we are missing out on the capacity to fully harness the potential for change in the way benthic systems are governed to help with rapid adaptation to, and mitigation of, climate change. Some efforts can be quite elaborate and consider multiple components of the ecosystem or involve multiple ecosystems [20,69,119], but success or otherwise often relates to the directional change in a limited number of parameters and does not involve the necessary follow up to fully assess the wider consequences of action [112,113]. Nevertheless, there are a number of scalable benthic-based solutions that are subsidiary to these larger projects, but have merit as they have characteristics that may reduce ecological footprints, improve resource management and biodiversity conservation, increase the sustainability of food production or improve equitable access to resources [31]. For example, suspension-feeding bivalves optimized to mitigate eutrophication and nutrient loading are cost-efficient relative to land-based measures while providing local employment and, in some cases, a harvestable product [82,120]. Shrimp and fish are being farmed in closed recirculation systems on land with no discharge, achieved using biodegradable biopolymers to absorb waste products [121]. Such systems provide food security as well as economic and social benefits, such as social cohesion, educational value and livelihood enrichment [122]. Similarly, bioengineered breakwaters and living shorelines are emerging with multiple benefits, such as reducing flood risks and mitigating the loss of intertidal and shallow water biodiversity while offering recreational value [20].

4. Getting it right

We have argued that benthic communities offer a variety of social, economic and environmental opportunities as society adapts to climate change. Yet, realizing these benefits requires management to, firstly, establish the most likely consequences of climate-related change, and secondly, to do so across a broad range of spatial and temporal scales. To date, the role of sediment communities in climate mitigation has largely been considered as part of a wider debate about the negative consequences of human activities, such as bottom fishing, where it has been convenient to include discussion about using marine protected areas (MPAs) as climate refugia [114,123]. Such an approach does not put climate change at the heart of the design and, while implementation of an MPA may be practical at large scales (greater than hundreds of kilometres), plans will need to be sympathetic to needs of multiple users if they are to be accepted and effective in the long term. This problem is illustrated by the findings of a recent model concerning the adaptation of benthic species to climate change, which found that locating MPAs in cool refugia was a relatively unsuccessful strategy [124]. Rather, establishing MPAs that allow sufficient larval dispersal between warmer and cooler areas is more likely to facilitate natural adaptation. Current regional conservation plans typically protect areas that exhibit low levels of vulnerability to climate change and disregard how species may redistribute as climate change advances [125].

Climate change adaptation is, of course, a major rationale for the surge of interest in benthic habitat restoration [4]. Yet theory over how such restoration should be planned remains in its infancy. There are two key siting considerations, which may prove to be incompatible and involve strong trade-offs. The first is simply where should restoration be placed to maximize its sustainability? Answering this question is not entirely straightforward because it depends on the outcome of the interactions of multiple components of the system [126], as well as the effect of habitat configuration [75,127] and environmental setting [128,129]. The second asks where restoration can have the greatest spillover benefits to connected ecosystems [130]. Such benefits include the spillover of larvae to replenish damaged habitats elsewhere, but the extent to which this occurs has not been widely determined [131], especially in the deep ocean [132]. Lagrangian models of connectivity have been combined with network theory to identify local populations that play an exceptionally important role in resupplying other locations. For example, it is estimated that 3% of reefs comprising Australia's Great Barrier Reef can resupply corals to almost half of the entire ecosystem within a single summer spawning event [133]. Identifying such population sources and the networks of dispersal provides an entry point to tailoring restoration where it can be most effective, but a priori assumptions about dispersion capability and habitat suitability are not always verified and can lead to surprises that require restoration plan adjustments [134]. In both cases, the majority of the research has focused on biological and ecological considerations; there has been much less focus on social-ecological or governance considerations.

An important point about ‘getting it right’ is that increased investment in management, both to support practical application of interventions and to maintain appropriate post-intervention monitoring and evaluation [112,113], is likely to be critical as climate impacts strengthen. Yet, there are a variety of reasons why governments might be tempted to reduce investments into the management of benthic ecosystems [135]. These include a lack of clarity about appropriate solutions, perceived futility of local interventions, short-termism in extracting a declining resource, the perception that management is unsuccessful because ecosystem state continues to decline (which can be addressed by using appropriate counterfactuals for the system state with less management), and difficulties with suitability of legislation that is not always formulated adequately to protect the benefits most valued by people [136]. The out-of-sight and data deficient [137] nature of much of the marine environment, coupled with differences in perspectives between terrestrial and marine ecologists [138], compounds these problems. Our focus on benthic ecosystem functions can be translated into ecosystem services by focusing on the benefits that benthic restoration would provide for people [139]. However, we should also be careful not to oversell the utility of taking an ‘ecosystem services’ approach to the selection and management of benthic ecosystem functions. In many cases, alternative ecosystem service values are so disparate that they can only be reconciled through somewhat arbitrary rescaling of values. For example, an insightful analysis of the value of benthic habitat for fisheries versus wave energy generation required fisheries values to be multiplied by a factor of 50 in order to create a ‘level playing field’ [140].

5. Thinking big

While many of the examples of nature-based solutions concern proof of concept studies over relatively small spatial scales, it is clear that for the potential of these interventions to be fully realized, they must be implemented over the range of interacting scales within which marine social-ecological systems function (figure 2). The process of scaling up may be fiscally or politically challenging but, more fundamentally, the survey and monitoring required to formulate a nature-based solution can be highly intensive and time-consuming [144]. Remote sensing techniques (including satellite, airborne, boat and autonomous vehicle-based sensors; figure 2a) have been shown to be highly effective for large-scale monitoring of benthic communities and habitats, including coral reefs [145] and large expanses of the deep ocean [146]. These techniques also provide the opportunity to link across scales, for example from individual to community to regional and beyond, recognizing that one scale of monitoring will unlikely be able to capture all data required to assess the changing nature of our benthic habitats. Many of the factors (e.g. physical process, infrastructure, climate and weather) that influence the decision of what type of intervention to make and where to site it can be remotely sensed [147] and we argue that, in doing so, we are able to better map onto the physical impacts and socio-economic scales related to climate change (figure 2b). As an example, remote sensing has been used in conjunction with ground-truthing surveys, to design marine protected areas [148]. The large spatial coverage and high temporal frequency of collection (figure 2a) make remote sensing techniques an ideal tool for the routine survey and identification of benthic communities and habitats, including ongoing monitoring of nature-based solutions at management and policy-relevant scales.

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6. Research priorities

Opportunities for enhanced socio-ecological resilience and planning and more informed decision-making within the benthic arena seem rife, but there is a need to (i) formulate basic science in support of best practice, including the interrogation of realized levels of risk reduction and routine follow-up checks that can identify maladaptive outcomes, and (ii) establish effective participatory processes with implicated stakeholders that maximize engagement and lead to the co-design of solutions [149]. Realization of a coherent plan is embryonic, in part because of compartmentalized funding streams and the interdisciplinary nature of the problems society now faces, but also because the case for the benthos has not been strongly articulated. It can be especially hard, for example, to identify relevant stakeholders when systems are distantly located and the links required to connect from the system to the stakeholders are multiple. While we acknowledge the challenges that lie ahead, decision-makers nevertheless need credible and relevant information to inform regional and national responses to climate change. Hence, for the benthos, we see an immediate and urgent need to:

In order to accomplish this research agenda, a consortium enterprise and a change of culture is needed to find meaningful solutions to the climate crisis, requiring interdisciplinary and international collaboration to seek measures that can be tested and applied. Practical applications need to be embraced and investigators need to work with institutions and agencies in order to identify research priorities and move solution-orientated debate forward in a positive manner [151,152].

7. Conclusion

Adapting to climate change is contingent on being able to respond to the effects of climate change impacts with meaningful countermeasures. Natural and nature-based solutions have been presented as a multifunctional, solution-oriented approach to increasing sustainability and have rapidly become the de facto means to alleviate or avoid the consequences of climate change. Marine benthic systems have been instrumental in many of the mitigation and adaptation plans already proposed, but our analysis suggests that significant further benefit can be derived from consideration of shelf and deep ocean environments. Progression in this area, however, will demand a shift in attention to the role of benthic species and habitats that are presently unrepresented, especially on the shelf, in the deep ocean and at higher latitudes. It also will require an emphasis on using technology and new ways of processing data to address questions at climatic- and societal-relevant scales. The importance of temporal and spatial scale, both in terms of the application of an intervention and in relation to any unforeseen negative outcomes, cannot be emphasized enough. We conclude, however, that within this space many of the tools required are already present, theory and mechanistic understanding is well developed, and that there are the appropriate foundations to deliver a rich and fruitful research agenda capable of contributing to the development of a structured and holistic plan of enactment.

Data accessibility

This article has no additional data.

Authors' contributions

M.S., E.M.B. and P.J.M. designed the study. M.S. wrote the first draft of the manuscript, and all co-authors contributed to subsequent iterations.

Competing interests

We declare we have no competing interests.

Funding

This work was supported by the Raymond and Beverly Sackler USA-UK Scientific Forum, jointly administered by The Royal Society UK and the National Academy of Sciences USA. M.S., J.L. and J.A.G. also acknowledge time allocated under the ‘Physical and biological dynamics of coastal processes and their role in coastal recovery (BLUE-coast)’ project (NE/N015703/1, 2016–2021), funded by the Natural Environment Research Council (NERC).