Achieving conservation and restoration outcomes through ecologically beneficial aquaculture
Article impact statement: Twelve ecologically beneficial outcomes are achievable via aquaculture.
Abstract
enA range of conservation and restoration tools are needed to safeguard the structure and function of aquatic ecosystems. Aquaculture, the culturing of aquatic organisms, often contributes to the numerous stressors that aquatic ecosystems face, yet some aquaculture activities can also deliver ecological benefits. We reviewed the literature on aquaculture activities that may contribute to conservation and restoration outcomes, either by enhancing the persistence or recovery of one or more target species or by moving aquatic ecosystems toward a target state. We identified 12 ecologically beneficial outcomes achievable via aquaculture: species recovery, habitat restoration, habitat rehabilitation, habitat protection, bioremediation, assisted evolution, climate change mitigation, wild harvest replacement, coastal defense, removal of overabundant species, biological control, and ex situ conservation. This list may be expanded as new applications are discovered. Positive intentions do not guarantee positive ecological outcomes, so it is critical that potentially ecologically beneficial aquaculture activities be evaluated via clear and measurable indicators of success to reduce potential abuse by greenwashing. Unanimity on outcomes, indicators, and related terminology will bring the field of aquaculture–environment interactions into line with consensus standards in conservation and restoration ecology. Broad consensus will also aid the development of future certification schemes for ecologically beneficial aquaculture.
Resumen
esSe necesita una gama de herramientas de conservación y restauración para salvaguardar la estructura y función de los ecosistemas acuáticos. La acuacultura (el cultivo de organismos acuáticos) generalmente contribuye a los numerosos estresantes que soportan los ecosistemas acuáticos, aunque algunas actividades de la acuacultura también pueden proporcionar beneficios ecológicos. Revisamos la literatura sobre las actividades de acuacultura que pueden contribuir a los resultados de conservación y restauración, ya sea al incrementar la persistencia o recuperación de una o más especies objetivo o al llevar a los ecosistemas acuáticos hacia un estado objetivo. Identificamos doce resultados con beneficios ecológicos que pueden lograrse con la acuacultura: recuperación de la especie, recuperación del hábitat, restauración del hábitat, rehabilitación del hábitat, protección del hábitat, bioreparación, evolución asistida, mitigación del cambio climático, sustitución de la captura silvestre, defensa costera, eliminación de las especies sobreabundantes, control biológico y conservación ex situ. Esta lista puede expandirse conforme se descubren nuevas aplicaciones. Las intenciones positivas no garantizan resultados ecológicos positivos, así que es importante que se evalúen las actividades de acuacultura con un posible beneficio ecológico por medio de indicadores del éxito claros y medibles para reducir el abuso potencial por ecoblanqueo o greenwashing. La unanimidad en los resultados, indicadores y terminología relacionada armonizará las interacciones entre la acuacultura y el ambiente con los estándares de la conservación y la ecología de la restauración. Un consenso generalizado también ayudará con el desarrollo de futuros esquemas de certificación para la acuacultura con beneficios ecológicos.
Obtención de resultados de conservación y restauración a través de la acuacultura con beneficios ecológicos
【摘要】
zh水生生态系统结构和功能的保护需要一系列保护和恢复工具。水产养殖, 即水生生物的养殖, 通常会导致水生生态系统面临许多压力, 但一些水产养殖活动也能带来生态效益。本文综述了水产养殖活动可能有助于保护和恢复目标的文献, 这些活动或是促进了一个或多个目标物种的续存或恢复, 或是促进了水生生态系统向目标状态转变。我们确定了 12 项可通过水产养殖实现的生态效益成果, 包括物种恢复、栖息地恢复、栖息地修复、栖息地保护、生物修复、辅助演化、减缓气候变化、替代野生采收、海岸防御、清除过剩物种、生物控制, 以及就地保护。这个列表可能会随着新应用的发现而继续扩充。然而, 积极的意图并不能保证获得积极的生态结果, 因此, 还应通过明确和可衡量的成功指标来评估有潜在生态效益的水产养殖活动, 以减少可能的虚假环保宣传的滥用情况。结果、指标和相关术语的一致性有助于水产养殖-环境的交叉学科与保护和恢复生态学的共识标准保持一致。广泛的共识也将有助于未来发展有生态效益的水产养殖认证计划。【翻译: 胡怡思; 审校: 聂永刚】
INTRODUCTION
Anthropogenic stressors are intensifying in aquatic ecosystems (Geist & Hawkins, 2016), including habitat loss, overfishing, eutrophication, pollution, climate change, and species invasions (Bayraktarov et al., 2016; de Silva, 2012; Geist & Hawkins, 2016; Halpern et al., 2008). The need to slow or reverse ecosystem degradation and the associated loss of biodiversity has resulted in a push for active and passive approaches to conserve and restore aquatic ecosystems (Geist & Hawkins, 2016).
The culture of organisms for conservation and restoration is a cornerstone of many management programs. Aquaculture, the culturing of aquatic organisms, plays a crucial role in food production and security, with an estimated 122.6 million t of global production in 2020 (FAO, 2022). Aquaculture can also have a range of positive and negative social, cultural, and economic effects (Campbell et al., 2021; de Silva, 2012; Edwards, 2000; Krause et al., 2015; Ottinger et al., 2016). However, the direct and indirect environmental impacts of aquaculture can contribute to the degradation and destruction of habitats, including coastline modification, pollution, and negative effects on wild populations (de Silva, 2012; Primavera, 2006). Despite potential negative impacts, there are accumulating examples of how aquaculture can create environmental benefits, both within and beyond food production. Ecosystem services, the benefits people obtain from nature (Hassan et al., 2005), that can be provided through aquaculture include regulating services (e.g., nutrient uptake, wave attenuation, and shoreline stabilization) and habitat or supporting services (e.g., provision of habitat structure that increases population growth of wild organisms with value to society) (Alleway et al., 2019; Barrett et al., 2022; Gentry et al., 2020; Theuerkauf et al., 2022; van der Schatte Olivier et al., 2020).
The concept of environmental benefits resulting from aquaculture is not novel. However, there is little consensus among researchers, practitioners, and decision makers about how to define and delineate aquaculture activities that deliver, or aim to deliver, conservation and restoration outcomes (Mizuta et al., 2023). Further, there are significant crossovers in the terminology used to describe analogous concepts and corresponding aquaculture activities (Anders, 1998; Froehlich et al., 2017; Mizuta et al., 2023; Patterson, 2019; The Nature Conservancy, 2021). As aquaculture applications progress beyond food production, the field will benefit from clear terminology and definitions.
We reviewed the ways in which aquaculture can benefit ecosystems and developed a framework of 12 distinct ecologically beneficial outcomes generated by aquaculture or aquaculture techniques.
EXISTING CLASSIFICATIONS
There are currently several (nonmutually exclusive) classification schemes commonly applied in the context of aquaculture–environment interactions, including concepts of environmental sustainability and provision of environmental or ecological benefits.
Use of the term sustainable aquaculture is growing in popularity, likely reflecting public demands for more sustainable practices (Boyd et al., 2020). We accept the sustainable aquaculture definition proposed by Boyd et al. (2020), whereby aquatic resources for human sustenance are cultured “without harming existing ecosystems or exceeding the ability of the planet to renew the natural resources required for production.” The efficient use of natural resources, traceability, transparency, and the preservation of intact habitat must all be met for an activity to be regarded as sustainable aquaculture (Boyd et al., 2020). Integrated multitrophic aquaculture (IMTA), whereby multiple trophic levels are cultured in series to minimize production waste (Chopin et al., 2012; Troell et al., 2009), is typically aimed at improving the environmental sustainability of aquaculture. Importantly, aquaculture does not have to deliver environmental benefits to be considered sustainable.
Several terms are used to describe aquaculture activities that have beneficial effects on the surrounding environment via restoration or conservation (Table 1). There are 4 existing definitions of restorative aquaculture (Table 1) with a substantial focus on increasing provisioning of ecosystem services and the importance of measurable positive outcomes (Mizuta et al., 2023; The Nature Conservancy, 2021; Theuerkauf et al., 2019, 2022). In a narrower context, restorative shellfish mariculture, proposed by Carranza and zu Ermgassen (2020) (Table 1), divides aquaculture into hatchery-dependent and nonhatchery-dependent strategies. The first relies on hatcheries to generate stock for outplanting, whereas the second uses a range of passive and active approaches that may not involve aquaculture, including establishing no-take areas, substrate provision, and wild brood stock translocation. Conservation aquaculture was first defined in the context of conservation and recovery of endangered fish populations (Anders, 1998) (Table 1). More recently, Froehlich et al. (2017) broadened the definition to include all aquatic organisms that may be cultured for conservation purposes, such as aquatic plants, marine invertebrates, and other aquatic vertebrates (Table 1). In addition, Froehlich et al. (2017) specify that conservation aquaculture encompasses planned management activities, such as stock enhancement by off-site rearing or transplantation.
| Term | Definition | Reference |
|---|---|---|
| Restorative aquaculture | “The intentional use of aquaculture to positively affect (ecosystem) services” | Theuerkauf et al., 2019 |
| “Commercial aquaculture with ecological benefits” | Theuerkauf et al., 2022 | |
| “Commercial or subsistence aquaculture that provides direct ecological benefits to the environment with the potential to generate net positive environmental outcomes” | The Nature Conservancy, 2021 | |
| “Commercial or subsistence aquaculture that supports initiatives to provide/or directly provides ecological benefits to the environment, leading to improved environmental sustainability and ecosystem services in addition to the supply of seafood or other commercial products and opportunities for livelihood” | Mizuta et al., 2023 | |
| Restorative shellfish mariculture | “A multi- and/or interdisciplinary approach involving some form of human intervention during the species life cycle, aiming to address negative socioecological impacts derived from the unsustainable use of marine shellfish” | Carranza & zu Ermgassen, 2020 |
| Conservation aquaculture | “The use of aquaculture for conservation and recovery of endangered fish populations along with their locally adapted gene pools, characteristic phenotypes, and behaviors” | Anders, 1998 |
| “The use of human cultivation of an aquatic organism for the planned management and protection of a natural resource” | Froehlich et al., 2017 |
WHAT WE CONSIDER TO BE AQUACULTURE
Throughout this review, we apply the most literal definition of aquaculture as the culturing of aquatic organisms, regardless of its purpose, duration of culture, or life stages that are cultured. For instance, we consider the application of these techniques at any life cycle stage (e.g., culturing larvae in a hatchery, planting propagules in a nursery) of an organism aquaculture, even if the organism is subsequently released or outplanted into a target ecosystem and has no further human intervention. Similarly, culturing a species for economic motivations (e.g., finfish aquaculture for commercial food production) and culturing a species for conservation purposes (e.g., culturing coral in nurseries to be outplanted onto denuded reefs) are both considered forms of aquaculture.
WHY A FRAMEWORK FOR AQUACULTURE THAT DELIVERS ECOLOGICAL BENEFITS IS NEEDED
The fields of restoration ecology and conservation science have become increasingly integrated (Hobbs et al., 2009; Wiens & Hobbs, 2015), driven by a realization that few habitats are genuinely pristine and that projects that combine preservation with other values are more likely to gain support. This is especially relevant to marine environments, where populations are highly connected and impacts such as eutrophication, sedimentation, fishing pressure, and introduced species are ubiquitous (Halpern et al., 2008). Accordingly, we believe it would be useful for putative ecological benefits from aquaculture to be assessed within a single framework that encapsulates the breadth of aquaculture–environment interactions.
Although recent literature on conservation and restorative aquaculture refers to environmental or economic motivations, direct or indirect mechanisms, or the ecological levels targeted (Froehlich et al., 2017; Mizuta et al., 2023; The Nature Conservancy, 2021), we argue that delineations should be made purely based on demonstrated outcomes. This is because commercial enterprises can deliver ecological benefits as a positive externality (a side effect of doing business), whereas aquaculture projects established to deliver ecological benefits can fail to do so. Similar cases in conservation and restoration ecology led those fields to develop consensus principles and standards used to assess progress toward goals via measurable indicators (Gann et al., 2019; Stewart et al., 2020). We believe the same evidence-based principles can be applied to the ecological effects of aquaculture.
ECOLOGICALLY BENEFICIAL AQUACULTURE
To deliver ecologically beneficial outcomes, aquaculture should enhance the persistence or recovery of one or more target species such that the existence of aquaculture causes the affected ecosystem to be closer to a target or reference state than it would have been without it. This can be achieved by directly modulating the abundance of species that are either more or less abundant than they should be according to the target ecosystem state or by improving environmental conditions to support passive recovery and resilience. We are not prescriptive about the target ecosystem state but intend it in the same sense as used by Gann et al. (2019). Often, this increases the total availability of ecosystem services, although this is not integral.
Outcomes of aquaculture activities are often context dependent, such that a positive impact in one setting may be a neutral or negative impact in another. Further, terms such as overall or net impact are unfortunately more applicable in theory than in practice because a given aquaculture activity will often have numerous effects, many of which will trade off against each other and vary through space and time. Net ecological benefits and costs can be difficult to calculate, even when extensive ecological monitoring has taken place because aquaculture–environment interactions are complex and there is not always full agreement among stakeholders on the target ecosystem state or the prioritization of various outcomes. Because of this, there is considerable scope for greenwashing, fig leaf, or Trojan Horse tactics by commercial aquaculture industries (Firth et al., 2020), particularly where specific ecologically beneficial outcomes are promoted to distract from wider environmental impacts and maintain social license. The best defense may be to require that claimed ecological benefits are supported by an evidence base that is appropriate for the local context and reflects the breadth of the claim as one ecologically beneficial outcome does not imply a net positive ecological impact. A certification process conducted by an external organization or entity, based on a standardized set of measurements or variables, would be beneficial.
OUTCOMES ACHIEVED THROUGH ECOLOGICALLY BENEFICIAL AQUACULTURE
We identified 12 distinct ecologically beneficial outcomes that can be achieved through aquaculture (Figure 1; Table 2). This is only a starting point, and as ecological knowledge evolves and new applications arise, we expect that new outcomes will be added. The outcomes below are also not mutually exclusive; a single aquaculture activity may deliver several. For example, a native shellfish farm operating in an area where wild counterparts have undergone historical declines may deliver positive outcomes for species recovery and habitat restoration, especially if the farmed shellfish carry locally adapted wild-type genes (e.g., Norrie et al., 2020). Further, if the area is eutrophic or turbid, filtering and nutrient assimilation by farmed shellfish can also provide a bioremediation outcome (e.g., Petersen et al., 2014). Finally, if the shellfish is farmed in an area facing habitat loss due to coastal erosion (e.g., due to boat wakes or storm surges), wave attenuation or sediment stabilization is likely to deliver habitat protection and coastal defense (e.g., Plew et al., 2005). Although this example shows how multiple positive outcomes can be achieved, ecologically detrimental outcomes are also possible; therefore, evaluation of the net benefit of an aquaculture activity is required.
| Ecologically beneficial outcome | Outcome description | Measurable indicators of outcome achievement examples | Aquaculture activities that can deliver the outcome | Aquaculture activities that are not aligned and do not deliver the outcome |
|---|---|---|---|---|
| Species recovery | Targeted release of a cultivated aquatic organism of conservation concern to recover a lost or depleted local population |
Quantified survival or persistence of reintroduced population Increase in species abundance through time Increase in recruits or offspring through time |
Captive breeding program to maximize genetic diversity Collecting individuals from wild populations with the intention to change a phenotypic trait between collection and release or introduction Use of commercial or conservation hatcheries or nurseries to produce or raise biomass or stock to be released or reintroduced to a target area, which can include management programs such as genetic rescue and stock enhancement |
Direct transplantation or translocation of biomass or stock from one location to another, including genetic rescue programs that directly translocates individuals Escapees from commercial aquaculture that interact and breed with wild conspecifics and compromise fitness by introducing deleterious alleles, phenotypes, or disease |
| Habitat restoration | Use of cultivated aquatic species to substantially or fully restore structure and function of a degraded, damaged, or destroyed habitat |
Quantified survival or persistence of reintroduced population Quantified self-sufficiency of restored habitat Increase in biodiversity Demonstrated resilience toward disturbances and stressors Quantified return of habitat structure, function, or both |
Reintroduction of a native cultivated species (hatchery-, nursery-, or research facility-produced stock) to an area where habitat is degraded, damaged, or previously lost Habitat restoration with cultivated species theoretically restores ecosystem function to some extent, improves habitat quality, and increases biodiversity if successful Use of cultured aquatic organism to facilitate recovery of an ecosystem engineer of conservation concern (positive species interactions) |
Introduction of a non-native cultured species to perform an ecosystem function similar to a native lost species Provision of substrate for settlement in substrate limited systems that facilitates recruitment and recovery Direct transplantation or translocation of biomass or stock from one location to another Fallowing periods in areas where intensive sea-cage-based commercial aquaculture has been undertaken Formation of a hybrid or novel ecosystem |
| Habitat rehabilitation | Use of native or non-native cultured organisms to reinstate structure or function of an ecosystem to achieve partial recovery, rather than attempting to recreate the biodiversity and integrity of the native reference ecosystem |
Increase in biodiversity Return of ecosystem structure, function, or both |
Establish a cultured native or non-native species that performs the same ecosystem function as the lost species Reconciliation ecology techniques, such as introducing cultured species on existing artificial structures, that provide partial recovery of ecosystem structure or function |
deployment of an artificial structure to reinstate ecosystem structure (e.g., artificial reef) without outplanting cultured organisms |
| Habitat protection | Use or culture of an aquatic organism that results in direct or indirect protection of a species or the structure or function of an existing habitat of conservation concern |
increase in native species biodiversity Return of structure, function, or structure and function of habitat Reduced impact or effect of an abiotic stressor |
Aquaculture and associated structures that prevent degradation or protect an existing habitat or species of conservation concern Restoration of a habitat with flow-on benefits or interactions with another existing habitat or species of conservation concern (i.e., long-distance facilitation) |
Lack of fishery exclusion zone around commercial farm sites Aquaculture activity itself degrades, displaces, or destroys habitat |
| Bioremediation | Use of cultivated aquatic organisms to improve or restore the quality of a degraded, damaged, or destroyed ecosystem |
Volume of water filtered Mass of excess organic material in sediments reduced Mass of excess organic and inorganic nutrients or matter removed Decrease in concentration of contaminants or pollutants Increase in water clarity |
Use of cultured plant or algae (phytoremediation), fungi (mycoremediation), or bivalves to remove excess nutrients, nitrogen, heavy metal contamination, or hydrocarbon or oil spills from the environment Dependent on scale at which bioremediation benefits are realized |
Crop or culture rotations to mitigate environmental impacts and break pest and disease cycles Nutrient uptake in an oligotrophic estuary by a cultured species Farming at an intensity that exceeds carrying capacity Sustainable aquaculture (e.g., integrated multitrophic aquaculture) that aims to mitigate or reduce impacts rather than providing bioremediation benefits beyond the context of the site |
|
Assisted evolution |
Use of a selectively bred aquatic organism of conservation concern with a phenotypic trait that has been selectively bred to reduce susceptibility or improve the ability to adapt to a specified stressor at an accelerated rate |
Reduced susceptibility (hence increased survival and persistence) of species to specified stressor Increase in species abundance through time Increase in recruits and offspring through time |
Selective breeding programs that can include intraspecific or interspecific hybridization between different populations to increase tolerance or resistance to a pathogen or changing environmental conditions | Genetically modifying commercial species to reduce susceptibility to pests or diseases |
| Biological control | Release of cultivated aquatic organism into a habitat or ecosystem to control an undesirable (pest) species that has degraded or damaged an ecosystem |
Reduction in selected (pest) species Return or increase in native species abundance or biodiversity |
Release of cultured predator or natural enemy to control a target pest that has cascading trophic effects (biomanipulation) Release of a cultured vector to enhance virus or pathogen spread to an invasive or target species |
Mass release of commercial biological control agent in commercial farms to control a commercially important pest Direct translocation of a predator to control a target species |
| Removal of overabundant species | Direct removal of an overabundant species from an ecosystem where it is then cultured and subsequently harvested that alleviates or removes pressure on a degraded, damaged, or previously lost ecosystem and provides capacity to recover or reestablish |
Increase in abundance of ecosystem engineer Return of ecosystem structure, function, or both structure and function Return or increase in native species abundance or biodiversity Reduction in target species |
Removal of an overabundant species to a level that facilitates return to a previous state as the system demonstrates hysteresis |
Ranching a species as part of fisheries enhancement Direct harvest of an overabundant species without aquaculture interventions |
| Ex situ conservation | Culturing of an aquatic organism outside of its natural range or habitat where biotic stressors, abiotic stressors, or both are reduced or eliminated |
High survival of ex situ cultured population Maintenance or increase in genetic diversity |
Captive breeding programs in predator-free environments Insurance populations Zoos, botanical gardens, and aquariums |
Commercial aquaculture Culturing a species for illegal black-market trade Compensation (creation of new habitat) |
| Coastal defense | Use or culture of an aquatic organism that directly or indirectly protects coastal habitats of conservation concern by reducing abiotic stressors |
Increase in sedimentation rates or reduction in coastal erosion rates Reduction in wave energy Reduction in inundation extent |
Aquaculture activity (including associated structures; e.g., shellfish cultured on longlines or in baskets) that reduces abiotic stressors (e.g., wave attenuation) and reduces or prevents coastal erosion |
Large-scale aquaculture that displaces vulnerable habitat of conservation concern Incorporation of integrated greening of gray infrastructure to justify ocean sprawl (proliferation of artificial or engineered structures in coastal and marine environments) |
| Climate change mitigation | Use of cultivated aquatic organisms in an ecosystem that can contribute to local, regional, or global mitigation of climate change impacts |
Mass of CO2 and N sequestered Reduction in ocean acidity (increase in pH) |
Use of aquacultured biomass to restore aquatic vegetative habitats (e.g., mangrove forests, saltmarshes, seagrass meadows) that function as carbon sinks and enable subsequent carbon storage Carbon sequestration through use of cultured organisms via carbon storage enterprises (e.g., carbon tax, blue carbon enterprises) |
Carbon sequestration of enterprises that do not account for the full carbon cycle or fate of harvested materials Carbon emissions on site and throughout supply chain that negate sequestration or storage |
| Wild harvest replacement | Culture of an aquatic organism that entirely replaces wild harvest and does not rely on wild stock for continued culture | All 5 of Biggs et al. (2013) and Tensen (2016) criteria met | Wild harvest replaced by culturing an aquatic species |
Continued unsustainable harvest of a species (typically ornamental aquarium species) despite an established aquaculture program Continued reliance on wild individuals for spat or seed or as brood stock to sustain aquaculture program |
In Table 2, we present the ecologically beneficial outcomes that can be achieved through aquaculture; describe each outcome, measurable parameter, or metric that can be used to quantify the achievement of each outcome; and list activities that can or cannot deliver the outcome. We discuss these in turn below.
Species recovery
Species recovery or reestablishment can be achieved through the targeted release of a cultivated aquatic organism of conservation concern to recover a lost or depleted local population (Table 2). The history of conservation aquaculture is closely tied to species recovery, with the white sturgeon (Acipenser transmontanus) in the Kootenai River cited as an archetypal conservation aquaculture case (Anders, 1998; Paragamian, 2012). Similarly, genetic rescue can aid species recovery; individuals from a small and imperiled (and hence low fitness) population are outbred with individuals from another population to increase genetic diversity and vigor (Ingram & De Silva, 2015; McClelland & Naish, 2007; Whiteley et al., 2015). However, in the context of this framework, this must entail an aquaculture component. For example, genetic rescue efforts through the release of hatchery-reared Snake River sockeye salmon (Oncorhynchus nerka) in Idaho and Washington (USA) have been considerably successful (Kline & Flagg, 2014). Species recovery can also be achieved through headstarting or conservation interventions by collecting individuals from the wild and rearing them to improve survival (Bell et al., 2005; Heppell et al., 1996). Although there is disagreement about the effectiveness of these activities and their conservation value (Bennett et al., 2017; Pullin & Knight, 2009), several cases in aquatic ecosystems have demonstrated their conservation value. For example, a headstarting program for the endangered green turtle (Chelonia mydas) in the Cayman Islands via the collection of eggs and subsequent release of captive-raised hatchlings and yearlings had some success; survival to adulthood was recorded (Bell et al., 2005).
Restocking native species for fisheries management can deliver species recovery benefits if the wild population has declined through overfishing or other impacts (Bell et al., 2008; Blount et al., 2017; Carranza & zu Ermgassen, 2020; Munro & Bell, 1997). However, ecological benefits are lost if the fish are quickly recaptured by fishers. For example, Murray cod (Maccullochella peelii) fingerlings are frequently stocked in freshwater bodies throughout southeastern Australia to maintain wild populations under continued recreational fishing pressure (Lintermans, 2013). In this case, the aquaculture component achieves species recovery when viewed in isolation, despite future events neutralizing that benefit. However, our framework does not incorporate the direct translocation of individuals, stock, seed, or spat from one location to another to recover a species because despite being potentially beneficial, it would not entail a sufficient aquaculture component.
Habitat restoration
Habitat restoration can be achieved with cultivated organisms to substantially or fully restore the structure and function of a degraded, damaged, or destroyed habitat (Table 2). The cultivated species is typically an ecosystem engineer (habitat forming) and hence is usually a plant or invertebrate. It should be native to the area being restored, rather than a non-native species that performs the same ecosystem function (habitat rehabilitation [Table 2]). This outcome can be achieved by actively stocking individuals cultivated in a hatchery, nursery, or research facility to the target area. For example, coral gardening is commonly used to culture coral in situ and restore degraded reefs (Rinkevich, 1995, 2014). Additionally, field-collected propagules of mangroves can be cultured in nurseries and planted for habitat restoration (e.g., black mangrove [Avicennia germinans] [Patterson et al., 1993; Toledo et al., 2001]). Cultured organisms can also be harnessed to achieve ecologically beneficial outcomes through positive species interactions. For example, in North Carolina (USA), hatchery-produced quahog (Mercenaria mercenaria) planted alongside eelgrass (Zostera marina) seeds facilitated greater patch productivity and expansion through increased nitrogen availability via pseudofeces deposits (Zhang et al., 2021). Habitat restoration is not achieved by adding habitat structure where it would not naturally occur, although doing so could still provide rehabilitation outcomes (see below).
Habitat rehabilitation
In the context of this framework, we define habitat rehabilitation as the use of native or non-native cultured organisms to improve the function of a degraded ecosystem without necessarily restoring the lost original structure (Bayraktarov et al., 2016; Elliott et al., 2007; Gann et al., 2019; Table 2). The stocked cultured organisms function as analogues of what was lost. For example, aquaculture gear, such as cages or ropes associated with seaweed and bivalve aquaculture, can provide settlement substrates for recruitment of native sessile invertebrate communities and provide refuge for fish and invertebrates, with cultured organisms contributing to food subsidies and breeding habitats for native biota (Tallman & Forrester, 2007; Theuerkauf et al., 2022).
A related activity, ecological reconciliation, attempts to modify and diversify existing anthropogenic habitats to allow them to harbor a wider variety of species without compromising human uses of the habitat (Rosenzweig, 2003). Although reconciliation is generally considered distinct from habitat rehabilitation, reconciliation can still achieve aspects of rehabilitation if the stocked organism can provide structure or function that was previously lost. For example, although considered reconciliation, the addition of ropes seeded with hatchery-produced blue mussels (Mytilus galloprovincialis) to artificial structures in marinas reduced invasive taxa and improved native taxa biomass and biodiversity and therefore provided rehabilitation benefits given enhanced ecosystem structure and biodiversity outcomes (Adams et al., 2021).
Habitat protection
Habitat protection can be achieved through the use or culture of an aquatic organism that results in the direct or indirect protection of a species, or the structure, function, or both of an existing habitat (Table 2). For example, the Mediterranean long-snouted seahorse (Hippocampus guttulatus) is abundant at some mussel farms because the farms provide substrate for prey species and excludes trawling (Gristina et al., 2015). Farms can also partially function like marine protected areas if there is a fishery exclusion zone around the farm site that protects aggregating fishes (Alleway et al., 2019; Clavelle et al., 2019; Dempster et al., 2002, 2006), although farming can also displace or threaten certain species and habitats (McKindsey et al., 2011; Primavera, 2006). Finally, habitat restoration via a cultured species can improve ecosystems beyond the farm footprint (Barrett et al., 2022; Callier et al., 2018; Costa-Pierce & Bridger, 2002). For example, the restoration of an oyster reef with hatchery-reared spat can result in far-field positive interactions through the amelioration of biological stressors, physical stressors, or both (Reeves et al., 2020; van de Koppel et al., 2015). Aquaculture activities that do not deliver habitat protection may include commercial farms that allow fishing at the farm site. Further, potential negative impacts on habitats should be considered, such as shading by farm structures, accumulation of sediment, and benthic organic loading (Barrett et al., 2022; Deslous-Paoli et al., 1998; Heery et al., 2017; McKindsey et al., 2011). Accordingly, habitat protection will not be achieved if the aquaculture activity itself degrades existing habitat (Ferriss et al., 2019; Tallis et al., 2009).
Bioremediation
Cultured organisms can be used to bioremediate a degraded, damaged, or destroyed environment (Table 2). For example, cultured plant or algae (phytoremediation; Huesemann et al., 2009; Yamamoto et al., 2008), marine-derived fungi (mycoremediation; Cecchi et al.,., 2020; Vala & Dave, 2017), or bivalves (e.g., mussels, oysters; Lindahl et al., 2005; van der Schatte Olivier et al., 2020) can remove excess nutrients, heavy metal contaminants, or hydrocarbon spills in the aquatic environment. Blue mussel (Mytilus edulis) mitigation farms in Denmark can cost-effectively remove excess nutrients in eutrophic coastal waters (Petersen et al., 2014). Similarly, large-scale seaweed aquaculture in China is projected to remove 100% of terrestrial phosphorus inputs in Chinese coastal waters by 2026 (Xiao et al., 2017). The underlying environmental conditions (i.e., whether a system is eutrophic or oligotrophic) will determine whether the removal of nutrients is ecologically beneficial; aquaculture should not exceed the ecological carrying capacity of an ecosystem (Byron et al., 2011; McKindsey et al., 2006). Finally, there is an important distinction between bioremediation and biomitigation. For example, sustainable aquaculture practices, such as IMTA, typically aim to mitigate the immediate impact of a farm by improving waste management (Granada et al., 2016). Biomitigation is better described as a sustainable activity rather than an ecologically beneficial activity because it mitigates the farm's own impact without necessarily delivering net positive effects (Sanz-Lazaro & Sanchez-Jerez, 2017, 2020). Other biomitigation activities include culturing algae to remove metal contaminants in waste streams from coal-fired power stations (Ellison et al., 2014) and assimilating nutrients in wastewater (Valero-Rodriguez et al., 2020).
Assisted evolution
Current rates of evolution and adaptation for numerous organisms in aquatic ecosystems are being outpaced by anthropogenic stressors such as climate change. Assisted evolution through the genetic manipulation of wild organisms can enhance the capacity to tolerate stress or promote recovery (Aitken & Whitlock, 2013; Filbee-Dexter & Smajdor, 2019; van Oppen et al., 2015). Assisted evolution can be achieved by selectively breeding aquatic organisms of conservation concern for a phenotypic trait that improves survival (Table 2). Examples include breeding for resistance against parasites (e.g., bonamiosis in the flat oyster [Ostrea edulis] [Lallias et al., 2010]) and increased tolerance to environmental conditions (e.g., thermal tolerance in corals; Howells et al., 2021; van Oppen et al., 2015). Assisted evolution techniques used to improve or safeguard production of cultured organisms (e.g., increased tolerance to ocean acidification and rising sea temperatures in commercial bivalves; Tan et al., 2020) may achieve an ecologically beneficial outcome depending on the species and local ecological context.
Biological control
Releasing cultured organisms into a habitat or ecosystem for biological control of pests or other selected species can achieve ecologically beneficial outcomes (Table 2). This can occur by consumption of the selected species (e.g., stocking of weevils to control water hyacinth; van Driesche & Bellows, 1996) or release of a cultured vector that enhances pathogen spread to a selected species, although this can present significant risks to nontarget organisms (Secord, 2003). Further, biological control through biomanipulation can also be achieved by releasing a cultured predator to trigger cascading trophic effects and allow elements of a previously degraded ecosystem function to return (i.e., bioremediation) (Shapiro & Wright, 1984). For example, stocking cultured piscivorous fish to control planktivorous fish released zooplankton from predation pressure and benefitted water quality (Ha et al., 2013), and stocking cultured sea urchins onto coral reefs can reduce benthic algae and facilitate the recovery of coral reef ecosystems (Williams, 2022). However, biological control is not always ecologically beneficial (e.g., the stocking of various cleaner fish species in Atlantic salmon [Salmo salar] farms to consume ectoparasitic sea lice [Overton et al., 2020]) and may not involve aquaculture (e.g., translocation of a predator to control local outbreaks of an invasive species [Atalah et al., 2013]). Such cases are outside the scope of the ecologically beneficial aquaculture framework.
Removal of overabundant species
The direct removal of an overabundant, but not commercially viable, species from an ecosystem where it is then cultured and subsequently harvested can achieve ecologically beneficial outcomes (Table 2). For example, overabundant sea urchins in many countries lead to significant loss of kelp cover and associated biodiversity, and the formation of urchin barrens (Filbee-Dexter & Scheibling, 2014; Ling et al., 2015). Several capture-based aquaculture operations harvest these wild urchins from barrens, then transfer them to aquaculture facilities where they undergo months of intensive feeding with specialized diets to increase their roe content to become marketable (Angwin et al., 2022; Pert et al., 2018; Zupo et al., 2019). The direct harvest, removal, or destruction of an overabundant species does not fit within our framework because there is no aquaculture component.
Ex situ conservation
In the context of the ecologically beneficial aquaculture framework, ex situ conservation can be achieved by culturing an aquatic organism of conservation concern outside its natural range or habitat and reducing or eliminating biotic or abiotic stressors (Table 2). For example, the establishment of a refuge population of the endangered delta smelt (Hypomesus transpacificus) and a variety of coral species to safeguard against species extinction can achieve ex situ conservation benefits (Leal et al., 2016; Lindberg et al., 2013; Petersen et al., 2006). Ex situ conservation will mostly provide benefits at a species level, without substantial wider ecological benefits. Culturing a species for the purpose of future commercial harvest or for illegal black-market trade is typically not aligned with ex situ conservation, although it is conceivable that captive populations maintained for commercial aquaculture could provide an ex situ conservation service if wild populations were lost. Finally, ex situ conservation is distinct from compensation through biodiversity offsets, which aims to recreate biodiversity value that is destroyed elsewhere and, in practice, typically does not prevent a net loss of biodiversity (Curran et al., 2014; Quétier & Lavorel, 2011).
Coastal defense
Aquaculture activities can contribute to climate change adaptation by providing direct or indirect protection from coastal hazards (Table 2). Aquaculture infrastructure in the coastal zone can result in wave attenuation and shoreline stabilization (Duarte et al., 2017; Zhu et al., 2020). Cultured organisms can be used to restore or create ecosystems for the purpose of coastal defense, which are known as living shorelines or nature-based coastal defense (Morris et al., 2021; Zhu et al., 2020). In these projects, aquaculture can be used to generate a large biomass of organisms that reduces or eliminates reliance on transplantation (Patterson, 2019). Target ecosystems that can provide coastal defense or protection include seagrasses, mangroves, saltmarshes, coral reefs, kelp beds, and shellfish reefs (Morris et al., 2018). Coastal defense should not be used to justify ocean sprawl that results from a proliferation of artificial structures, as well as aquaculture and its associated infrastructure (Duarte et al., 2013; Heery et al., 2017), particularly if habitats of conservation concern are being displaced. As discussed above (“Habitat protection”), negative impacts of structure or habitat that provide coastal defense should be quantified.
Climate change mitigation
Strategies to mitigate the impacts of anthropogenic climate change can be achieved by using cultured aquatic organisms within an ecosystem that contribute to local, regional, or global mitigation of climate change or specific related impacts (Table 2). The restoration of a range of aquatic plant species produced via aquaculture, such as mangroves (Tri et al., 1998), seagrasses (Greiner et al., 2013), and wetlands (Burden et al., 2013), can enhance blue carbon sequestration (but see Komada et al., 2022). Blue carbon trading schemes and enterprises are emerging industries (Steven et al., 2019). Opportunities for cultured algae to capture and absorb large amounts of carbon dioxide and act as carbon sinks are arising (Chung et al., 2011; Duarte et al., 2017; Wan et al., 2021), albeit with questionable feasibility (Costa-Pierce & Chopin, 2021) because their culture will only contribute as meaningful carbon sinks if they are exported to the deep sea or buried in coastal sediments (Hill et al., 2015; Krause-Jensen & Duarte, 2016). Finally, seaweed aquaculture can elevate pH and generate oxygen, allowing reductions to the effects of coastal acidification and deoxygenation at a local scale (Duarte et al., 2017). Assessment of climate change mitigation requires carbon accounting that considers the full carbon cycle, the fate of harvested materials, and emissions both on-site and throughout the supply chain.
Wild harvest replacement
The culture of an organism to replace wild harvest and hence alleviate pressure on wild populations may achieve conservation outcomes. In practice, there have been both successes and controversies (e.g., wildlife or conservation farming [Bulte & Damania, 2005]). Tensen (2016) and Biggs et al. (2013) propose strict criteria under which wildlife farming can have a conservation outcome if 5 criteria are met: legal products form a substitute for wild products; demand is met and hence does not increase; legal products are more cost-efficient to produce than black-market prices; wild populations are not relied on; and laundering from wild populations into commercial trade is absent. In terrestrial ecosystems, few wildlife farming practices have met all 5 criteria (table 2 in Tensen [2016]). These criteria are equally applicable within this framework. Culturing freshwater ornamental species to achieve this outcome has been more successful than for marine species; over 90% of freshwater aquarium species are farmed (Froehlich et al., 2017; Olivotto et al., 2011; Wabnitz et al., 2003). In contrast, most marine aquaria are stocked with wild-caught specimens (Wabnitz et al., 2003), with limited culture tied to several critical bottlenecks (Olivotto et al., 2017). Although emerging technologies may overcome these hurdles, the financial viability of aquaculture operations will limit their feasibility and uptake. For example, although sea cucumbers and sea urchins can be cultured, it remains cheaper for the aquarium industry to source individuals from the wild (Calado, 2009; Olivotto et al., 2011). However, there is still significant promise for a range of marine species of conservation concern (Gentry et al., 2019; Tlusty, 2002).
CONCLUSIONS
Historically, there has been a disconnect between the fields of aquaculture and conservation and restoration, with only partial attempts to identify where and how they might align. Here, we took an outcome-focused approach to delineate 12 distinct ecological benefits that are achievable through aquaculture and used terminology that is largely consistent with terminology in the fields of restoration ecology and conservation science. We hope this framework assists researchers and practitioners to clearly identify aquaculture activities that can achieve ecologically beneficial outcomes. The next step is to develop an internationally recognized accreditation scheme for ecologically beneficial aquaculture to incentivize commercial aquaculture industries to increase the delivery of ecological benefits and, importantly, to document and evaluate those benefits. Clear terminology and standardization of key indicators and assessment protocols will allow for a greater understanding and mobilization of aquaculture for ecological benefit.
ACKNOWLEDGMENTS
We thank members of the SALTT Lab and D. Angel for providing valuable feedback on the manuscript. We respectfully acknowledge the Wurundjeri and Boon Wurrung people of the Kulin Nation as the traditional owners of the land and water on which our research was conducted and pay our respects to their elders past, present, and emerging.
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