Advances in Global Oyster Reef Restoration: Innovations and Sustainable Ecological Approaches

Abstract

Oysters have been recognized as ecological engineers for aquatic ecosystems, as oyster reefs provide critical habitats and foraging locations for other marine species. In the past few decades, anthropogenic activities have negatively impacted oyster reef ecosystems across the globe, resulting in a significant decline in their population. This review critically examines the causes and extent of oyster reef degradation, as well as the effectiveness of restoration initiatives employed to reverse this decline. Furthermore, this review evaluates the effectiveness of restoration strategies employed to rehabilitate oyster reefs. Different approaches, such as genetic improvement, suitable site selection, and oyster seeding to enhance oyster reef restorations, are critically reviewed in this paper. Furthermore, some advanced restoration approaches such as 3D printing, shell recycling, and acoustics technologies are also discussed in this paper, which opens the new doors for researchers in the field of restoration ecology. Challenges and barriers hindering successful restoration are also addressed, including financial constraints, regulatory complexities, and public engagement. The findings and insights presented herein contribute to the growing body of knowledge on oyster reef ecology and serve as a valuable resource for policymakers, scientists, and conservation practitioners seeking effective strategies for restoring these vital coastal ecosystems.

1. Introduction

The health and sustainability of marine ecosystems are of utmost importance for the well-being of our planet. These ecosystems play a crucial role in maintaining a balanced and thriving environment and provide indispensable ecological services that are imperative for the survival of both marine and terrestrial species [1,2]. However, due to human activities such as coastal development, overfishing, and natural processes like climate change, the marine ecosystem is undergoing continuous degradation [3]. The loss of habitats is undeniably a notable threat to biodiversity and ecological functioning of global ecosystems. For example, habitat destruction has profound implications, resulting in reductions in biodiversity, disruptions in ecosystem services, and alterations of marine food webs [4]. Approximately 50% of terrestrial and marine habitats have been destroyed or altered worldwide, resulting in a decline in species diversity and increased risk of extinction [5]. Therefore, extensive habitat loss poses a serious risk to humanity by endangering ecosystem productivity and vital ecosystem services. Consequently, scientists and natural resource managers have devoted significant time and efforts to the field of restoration ecology, with the goal of restoring degraded habitats and ecosystems to a more favorable state [3].

Oyster reefs are widely recognized as ecological engineers, forming dense aggregations that result in the creation of three-dimensional biogenic structures [6]. These reefs are a prevalent feature of the estuarine ecosystem and offer crucial habitats for benthic invertebrates, fish, and mobile crustaceans [7]. Oyster reefs are intricate and dynamic ecosystems that form through the accumulation of oyster shells. These shells interweave to create a complex network of structures, which serve as critical habitats for diverse marine organisms [7]. The presence of oyster reefs is essential for the health of coastal ecosystems, as they provide a multitude of ecological services that are fundamental for maintaining the balance and productivity of marine environments. For example, oysters are filter-feeding shellfish that filter plankton, algae, and other particulate matter as part of their feeding mechanism to purify water. In addition, the oysters provide other services including shoreline protection, nutrient cycling, and provision of vital habitats for fish and other invertebrates (Figure 1).

However, over the past 200 years, natural oyster reefs worldwide have experienced a staggering decline, with over 85% of oyster reefs disappearing [8]. The oyster populations in several bays and estuaries across North America, Europe, and Oceania have now reached a state of functional extinction [9,10]. A geographical map representing the decline in oyster population on a global scale is shown in Figure 2. This decline can be attributed to various reasons, such as their sensitive nature, mismanagement, and human overhunting [11,12]. The major factors responsible for the degradation of oyster reefs are related to human activities, such as nutrient pollution, disease, climate change, invasive species, and rising sea levels [13,14].

With oyster populations reaching historic lows and the recognition of the numerous ecosystem services provided by oyster reefs, such as essential fish habitats, global efforts for oyster reef restoration are increasing. The United Nations (UN) has designated the years from 2021 to 2030 as the decade of restoration, with the restoration of oceans and coastal environments being one of their primary Sustainable Development Goals [16]. Initially, oyster reef restoration efforts were focused on the eastern oyster (Crassostera virginica), Ostrea lurida, and Olympia oyster in the USA. However, these efforts have now extended to European nations as well as Australia, China, and New Zealand [17]. There is a growing interest in the potential use of oyster reef restoration and oyster farming to mitigate the impacts of eutrophication. The launch of the United States Environmental Protection Agency’s nutrient reduction program for Chesapeake Bay [18] has brought attention to the potential water quality benefits of oyster reef restoration. The main objectives of these restoration programs include enhancing biodiversity, increasing fish productivity, establishing a natural coastal defense system, and improving water quality. Furthermore, oyster reef restoration, by providing moisture and shade, may assist in biodiversity management strategies aimed at mitigating climate change and reducing temperature stress on various marine species [19]. The ecological significance of oyster reefs and the wide range of ecosystem services they provide have propelled global efforts to rehabilitate these reefs.

The objectives of this literature review are to shed light on the intricate realm of oyster reef restoration, with a focus on their ecological process. In this study, we will examine the ecological mechanisms that underpin successful restoration endeavors, as well as the strategies and innovations employed. In addition, we will explore key aspects of restoration efforts, including site selection, hybridization, population breeding, selective breeding, and the introduction of oyster nurseries. Additionally, we have taken a forward-looking approach to identify emerging trends and future directions in oyster reef restoration, considering the dynamic interplay between research, policy, and public engagement.

2. Literature Analysis

The data for this study were comprehensively searched from the Web of Science Core Collection from 1 January 1998 to 26 July 2024. The string used for the literature retrieval was (TS = (Oyster reefs)) AND TS = (Restoration). This search yielded 713 documents (articles and review articles). Only the documents written in English were included in this study. The data were extracted in the form of .txt files, containing the full records and the cited references. The data for the current study were analyzed using Citespace (version 6.2.R7), Arc GIS (ArcMap version 10.8), and the Origin Pro (version 2024b) software. The number of documents published since 1998–2024* has been summarized in Figure 3A. The highest number of documents, 45, which accounts for 6.3% of the total, were published in 2023. A significant surge in the number of publications can be seen in the figure, representing the thrust of the scientific community to invest more effort in the restoration processes. In Figure 3B, we have summarized the collaboration between different countries and institutions working in the field of oyster reef restoration. A total of 53 countries globally are actively participating in the field of oyster reef restoration. Notably, the United States of America has published the highest number of documents, accounting for 74.19% of the total number of publications, and poses the strongest collaborations with other countries like Australia, China, the Netherlands, and England. Australia ranks 2nd with 109 documents, which accounts for 15.28% of total publications, while China ranks 3rd with 46 publications, which accounts for 6.03% of total publications. The social network of co-occurrence keywords has been presented in Figure 3C. The analysis of keyword co-occurrence resulted in the identification of seven distinct clusters. Each cluster in the figure is depicted by a unique color. For example, the 1st cluster is represented in green and its main keywords are ecological restoration, marine conservation, and shellfish reefs. The 2nd cluster is represented in blue, and the main keywords in this cluster are oyster reefs restoration, artificial reefs, biogenic reefs, and water quality. The 3rd cluster, in orange, consists of keywords like sustainability, landscape ecology, and monitoring. The 4th cluster in purple consists of keywords such as larval recruitment and settlement. The 5th cluster is represented in brown, and the principal keywords are settlement, marine ecology, and larval recruitment, while the 6th cluster in pink contains only one keyword, sedimentation, and the 7th cluster in yellow also contains only the keyword “sediments.” Figure 3D can help in identifying the most pertinent topics within the realm of oyster reef restoration. The red line on the heat bar represents the period with the strongest citation bursts. The Chesapeake Bay, initially identified as a keyword in the year 2000, subsequently led to the emergence of other significant topics such as the Eastern oyster, reefs, and ecosystem services, which gained prominence between 2000 and 2019. From 2020 to 2022, the focus shifted towards oyster reefs, biodiversity, and the restoration of these crucial ecosystems. Figure 3E represents the number of documents published by various countries in the realm of oyster reef restoration. The United States of America is the major contributor in publications on the oyster reef restoration with a document frequency of 1549, which shows their great interest in this field of research.

3. Factors Affecting Oyster Populations

Various factors that can influence the populations of oysters in the aquatic environment include human activities, physical factors, and biological factors (Figure 4). Oysters are ectothermic organisms, which means that their body temperature depends on their surroundings [20]. Hence, fluctuations in temperature can have a direct impact on the reproduction, growth, and overall health [21]. Due to human activities in coastal areas, the global ocean temperature has increased by 0.11 °C, which can have a notable effect on the growth of oyster reefs [22,23]. Warmer temperatures can induce higher metabolic rates, resulting in increased growth and reproductive capacity, ultimately leading to a larger population [24]. However, excessive heat can have negative effects, which can lower survival rates and make oysters more susceptible to disease. For example, at higher latitudes, the population of oysters has increased due to the rising ocean temperature; however, at lower latitudes, rising temperatures have increased the mortality rates of oysters [25,26,27]. Cold temperatures can have negative impacts on metabolism and the reproductive activities of oysters, which may result in a decline in their populations [28]. In addition, a decline in temperature can also enhance the chances of disease incidence and mortality. Furthermore, this increment in temperature, in combination with other stressors such as salinity, heavy metals, and acidification, more profoundly influences oyster development [29].

Numerous other environmental changes brought about by global climate change are modifying the suitability of sites for oyster reefs [16]. For instance, oysters are highly vulnerable to salinity, and extreme changes in salinity levels can cause significant damage to their populations [30]. Oysters may experience osmotic stress when faced with higher salinity levels, as they struggle to regulate the concentrations of salts in their bodies. Consequently, this can lead to reduced growth rates, decreased reproduction, and enhance the chances of parasitic attachments and mortality of the oysters. For instance, in Northeastern United States estuaries, due to high precipitation, the salinity level is continuously decreasing beyond the threshold level required for oyster survival [31,32]. Hence, even low salinity levels can have adverse effects on oyster populations. Therefore, oysters depend on a certain level of salinity to carry out their physiological processes, and insufficient salinity can disrupt their ability to filter feed and obtain vital nutrients from the water. Additionally, low salinity levels can render oysters more susceptible to predation and expose them to harmful pollutants. Hence, we can conclude that ocean acidification can impact oyster populations; however, these effects could differ for various ecological regions.

The uncontrolled urbanization and industrial growth along the coastal belts release toxic organic and inorganic pollutants directly into the oceans, which enhances the rate of eutrophication (enrichment of phosphates and nitrates) [33]. Eutrophication enhances the growth of algae and decreases oxygen levels in water, which negatively affects oyster health. Likewise, some types of algae release toxic substances causing perturbation in the growth of oysters [34,35]. For example, several species of dinoflagellates are capable of producing toxins that pose significant risks to marine organisms. Under optimal conditions, these organisms experience rapid population growth, leading to harmful algal blooms. Such blooms can produce neurotoxins that accumulate in oysters and induce poisoning [36]. In addition, human alterations of flow for flood control, water security, or the expansion of metropolitan areas into the ocean can alter salinity, bottom-water oxygenation, and the availability of food and larvae, all of which affect the appropriateness of a site for oyster reefs [16]. However, consideration of the above-mentioned critical situations indicates that these are adversely affecting oyster settlement and recruitment to a significant extent. Hence, there is a need to regulate urbanization and development in estuaries and coastal areas through the implementation of strict regulations and management strategies.

4. Restoration Efforts for Oyster Reefs

The restoration of marine biogenic habitats is a rapidly emerging conservation priority aimed at reintroducing ecological, economic, and cultural benefits to communities. A schematic representation of methods that can be used in oyster reef restoration including genetic improvement, oyster seeding, specific site selection, shell recycling, artificial substrates, and 3D-printed substrates, is shown in Figure 5.

The primary objective of oyster reef restoration is to reinstate the lost services and populations of shellfish that have historically been overharvested, particularly during the colonization periods in the USA and Australia. The map of typical ongoing oyster reef restoration projects around the globe has been shown in Figure 6A. Since 1990, the United States, Australia, China, and the United Kingdom have emerged as leading countries in oyster reef restoration projects. Restoration work in mangrove and salt marsh environments has demonstrated the significance of the species and the imperative for diverse species assemblages. Similarly, seagrass restoration operations have highlighted the significance of genetic variety in transplants [37]. The restoration of oyster reefs may involve the replenishment of the hard substrate to facilitate spat settlement or the introduction of new living oysters. However, the success of these methods is largely contingent upon the successful settlement of oyster larvae [38,39]. However, the successful restoration of oyster reefs requires not only an understanding of the local climate, but also global political support and collaboration [1]. Despite advancements in restoration technology, many oyster habitat restoration efforts lack clearly defined goals and often neglect post-construction monitoring, which is crucial for adaptive management to assess goal achievement and compare plans.

4.1. Genetic Improvement of Oysters

4.1.1. Population Breeding

In oyster reef restoration projects, it is crucial to consider genetic factors, as they determine the success or failure of the restoration efforts. When selecting species for restoration purposes, it is imperative to consider not only the species itself but also the source population and its genetic diversity. In the field of restoration ecology, it has long been believed that transplanting individuals from local areas to restoration sites increases the likelihood of survival, as they have already adapted to the local climatic conditions [39,40]. However, the sole utilization of indigenous resources may impede swift adaptation to populations characterized by restricted dispersal and limited gene flow, or those that have undergone a decrease in effective population size or substantial alterations in genetic makeup due to factors such as harvest. This is particularly pertinent in the context of adjusting to the emerging stressors of anthropogenic and climatic change [41,42]. In such scenarios, genetic diversity and genetic enhancement can be achieved by augmenting transplants with aquaculture stock or stock acquired from alternative locations [43].

Furthermore, in the field of terrestrial ecosystem restoration, two methodologies such as predictive provenancing and admixture provenancing are currently gaining attention in scientific communities [44]. Predictive provenancing involves analyzing the genetic diversity and adaptation of different populations of a specific marine species to identify the best genetic matches for a particular restoration project [45]. It is an emerging conservation and restoration technique that comprehends the predictions about forthcoming environmental conditions such as climate change to determine source populations for restoration projects. This approach builds upon the principles of traditional provenancing by taking into account not only existing environmental factors but also anticipated modifications. The core objective of this approach is to select populations possessing attributes that will prove advantageous in the future [46]. On the other hand, admixture provenancing uses seeds sourced from multiple populations across the species’ distribution. This approach entails utilizing an amalgamation of genetic materials from diverse source populations to mend and enhance debilitated oyster reefs [44]. By harnessing the genetic diversity present in distinct regions and populations, the rehabilitated reefs can become more resilient and better equipped to endure and adapt to fluctuations in their surrounding environment [47]. Both methods aim to increase gene flow and genetic variation [46]. However, the advantages and disadvantages of using these methodologies in oyster reef restoration are not yet fully understood, so further investigations are needed. By analyzing the quantitative genetic variation within existing oyster populations at a specific site, we can determine the most suitable genetic approach to use.

Figure 6. (A) A map of ongoing projects on oyster reef restoration at the global scale (the map is modified from [8]; (B–E) Various artificial substrates including bagged oyster shell (B), mixed oyster substrates (C), concrete structures (D) mixed concrete substrates (E) used for the attachment of oysters [48].

Figure 6. (A) A map of ongoing projects on oyster reef restoration at the global scale (the map is modified from [8]; (B–E) Various artificial substrates including bagged oyster shell (B), mixed oyster substrates (C), concrete structures (D) mixed concrete substrates (E) used for the attachment of oysters [48].

4.1.2. Selective Breeding

Selective breeding can be a powerful tool in oyster reef restoration projects, as it enhances the resilience and recovery capacity of oyster populations. A summary of various studies involving selection breeding to enhance the resistance of various oyster species against disease and other abiotic factors has been presented in Table 1. This approach involves deliberately breeding oysters with desirable characteristics, thereby augmenting the efficacy of restoration efforts [49]. For example, disease incidence is a major cause of reduction in oyster populations around the world. The most common diseases that can influence oyster populations are “Dermo (Perkinsus marinus)” and “MSX”, which have chronic effects on oyster populations [50]. Restoration efforts can enhance the survival ability of oysters in the wild by selectively breeding individuals that demonstrate resistance to the disease [51]. This process can facilitate the establishment of populations that are more robust and capable of withstanding challenges, thus leading to the development of more stable and resilient reefs.

Rapid changes in climatic conditions have adversely affected oyster populations at a global scale. For example, low salinities and rapid temperature enhancement have reduced oyster growth and increased mortality rates [52]. Selective breeding can enhance desirable characteristics, such as accelerated growth rates, to help restore oyster reefs. Oysters that grow at a faster pace reach reproductive age within a shorter period, thereby significantly contributing to the rapid expansion of reef populations. Oysters face various environmental challenges, including temperature fluctuations, salinity levels, and water contamination. Therefore, selective breeding initiatives can prioritize enhancing oysters’ abilities to withstand these challenges, thus ensuring their resilience in diverse environments [53]. Furthermore, breeding oysters with higher fertility rates has the potential to enhance the reproductive success of the population, consequently augmenting the probability of effectively establishing and expanding reefs, particularly in regions with restricted natural recruitment [54]. Oysters are widely recognized for their proficiency in constructing reefs, which serve as critical habitats for other marine species. Through the strategic selection of traits that promote shell production and overall reef-building capacity, we can expedite the restoration of oysters as ecosystem engineers.

Table 1. A summary of the studies conducted to enhance the oyster’s resistance to diseases using selective breeding.

Oyster Species	Disease	Country	Results	Reference
Eastern oyster	Dermo	USA	A significant genetic variation in resistance to among different families of eastern oysters, with family 286 showing the highest resistance and family 242 the lowest.	[55]
Crassostrea virginica	MSX	USA	Selected strains demonstrated a discernible enhancement in their capacity to survive against disease. The cumulative mortality rate declined significantly from 92% in the unselected strains to 32% in the fifth-generation selected strains.	[56]
Crassostrea virginica	MSX and Dermo	USA	The F3-DEBY oysters demonstrated a significantly higher survival rate of 79% and showed better growth compared to the F3-JR and F1-LA strains. Additionally, the F4-DEBY strain had lower mortality and disease prevalence when compared to the control strains.	[57]
Crassostrea virginica	Ostreid herpesvirus 1 (OsHV-1)	France	Selected groups showed significant survival improvements over four generations. For example, G1 (34.5%), G4 (69.0%) vs. controls (12.3%, 7.3%).	[51]
Crassostrea gigas	ostreid herpesvirus 1 (OsHV-1)	USA	Survival rates improved by 10.3% and 21.2% after each selection cycle.	[58]
Crassostrea gigas	Vibrio aestuarianus and OsHV-1	France	Stock B showed improved resistance at the adult stage with a 14% reduction in death rates.	[59]
Crassostrea gigas	Summer mortality	China	Heritability values ranged from 0.12 to 0.28, indicating potential for genetic improvement.	[60]
Crassostrea gigas	Summer mortality	France	The high narrow-sense heritability range of 0.47 to 1.08 suggests a significant genetic influence on survival.	[61]

Table 1. A summary of the studies conducted to enhance the oyster’s resistance to diseases using selective breeding.

Oyster Species	Disease	Country	Results	Reference
Eastern oyster	Dermo	USA	A significant genetic variation in resistance to among different families of eastern oysters, with family 286 showing the highest resistance and family 242 the lowest.	[55]
Crassostrea virginica	MSX	USA	Selected strains demonstrated a discernible enhancement in their capacity to survive against disease. The cumulative mortality rate declined significantly from 92% in the unselected strains to 32% in the fifth-generation selected strains.	[56]
Crassostrea virginica	MSX and Dermo	USA	The F3-DEBY oysters demonstrated a significantly higher survival rate of 79% and showed better growth compared to the F3-JR and F1-LA strains. Additionally, the F4-DEBY strain had lower mortality and disease prevalence when compared to the control strains.	[57]
Crassostrea virginica	Ostreid herpesvirus 1 (OsHV-1)	France	Selected groups showed significant survival improvements over four generations. For example, G1 (34.5%), G4 (69.0%) vs. controls (12.3%, 7.3%).	[51]
Crassostrea gigas	ostreid herpesvirus 1 (OsHV-1)	USA	Survival rates improved by 10.3% and 21.2% after each selection cycle.	[58]
Crassostrea gigas	Vibrio aestuarianus and OsHV-1	France	Stock B showed improved resistance at the adult stage with a 14% reduction in death rates.	[59]
Crassostrea gigas	Summer mortality	China	Heritability values ranged from 0.12 to 0.28, indicating potential for genetic improvement.	[60]
Crassostrea gigas	Summer mortality	France	The high narrow-sense heritability range of 0.47 to 1.08 suggests a significant genetic influence on survival.	[61]

4.1.3. Hybridization

Hybridization has the potential to enhance the adaptability of oysters through increased heterozygosity and the creation of new genetic combinations. Hybridization can be of two types based on species selection, including interspecific hybridization and intraspecific hybridization. In interspecific hybridization, the genetic materials from two different species are combined to create a new species. On the other hand, intraspecific hybridization involves the breeding of individuals within the same species that have the potential to harness both the additive genetic variations present within a single linkage, as well as the non-additive genetic variations between the different linkages. The initial occurrence of interspecific hybridization in shellfish was observed within the oyster species Crassostrea angulata and Ostrea edulis [62].

This process serves a dual purpose: reducing the risk of extinction by enhancing adaptive potential and masking harmful alleles. Furthermore, hybridization can lead to the development of new adaptive traits, enabling oyster species to expand their distribution range and successfully colonize new ecological niches [63]. Specifically, hybridization can be applied in the context of genetic rescue or evolutionary rescue [64]. Genetic rescue involves the restoration of populations through hybridization. This approach is particularly relevant for small and isolated populations that often suffer from low genetic diversity and inbreeding depression. By introducing new genetic material through hybridization, these populations can be revitalized, preventing further genetic deterioration [65]. In a similar way, hybridization can contribute to evolutionary rescue by facilitating a shift towards the optimal phenotype. This occurs through selection acting on newly introduced or recombinant hybrid genotypes in the subsequent generations. Furthermore, it is worth noting that the term “evolutionary rescue” in some studies is strictly used to describe the adaptation to changing environments based on existing genetic variations.

4.2. Introduction of Oyster Nurseries

Oyster seeding, also called oyster spat seeding or oyster farming, is a key part of the aquaculture industry, especially for cultivating oysters. This practice is carried out in the sites where the population of oysters has declined below the threshold levels [11], and the process involves intentionally placing young oysters, known as spat, onto a substrate called a clutch [66]. There, they can grow and mature until they reach full development. Oyster seeding is a complex and important practice that plays a crucial role in sustainable environmental restoration and coastal protection [67]. Adult oysters are forced to mate under artificially regulated environments in specialized hatcheries, where spat production normally takes place. After this spawning process, the resultant larvae are fed and watched over closely until they grow to a specific size, at which point they can be linked to a clutch. Old oyster shells are a common place for the spat to settle since they offer an ideal growing habitat. However, the success of oyster seeding is contingent upon effectively addressing various challenges that can impede oyster growth and survival. These challenges encompass a range of factors, including environmental conditions, disease, and human activities.

4.3. Specific Site Selection

The careful selection of specific sites for oyster reef restoration is a crucial determinant of project success [68]. The chosen restoration site has a significant impact on the survival, growth, and reproduction of oysters, as well as the overall ecological benefits provided by the reefs [69]. In the planning of oyster reef restoration initiatives, it is essential to consider the ecological advantages in conjunction with the potential impacts on human activities. The sharp shells of oysters can pose hazards to swimmers, boaters, and the hulls of watercraft. Therefore, the careful selection of restoration sites is essential to mitigate conflicts with recreational and commercial water uses. A comprehensive site assessment should encompass factors such as water depth, proximity to popular swimming and sailing areas, and potential interference with navigation channels. Engaging local communities, stakeholders, and marine experts can facilitate the identification of locations for oyster reefs that optimize ecological benefits while minimizing human and economic impacts. This discussion highlights several important parameters that should be considered when selecting sites for oyster reef restoration projects.

4.3.1. Water Quality and Hydrodynamics

Oysters require a specific water salinity level to grow rapidly, typically ranging from 14 to 28 parts per thousand (ppt) [70]. Thus, it is critical to find a site with salinity levels that align with the requirements of specific oyster species to ensure their growth and survival. Deviations from optimal salinity levels can induce stress in oysters, rendering them more susceptible to disease and impairing their reproductive capacity [71]. Adequate levels of dissolved oxygen are also vital to the health of the oysters. Thus, the selection of sites with strong water circulation is essential to ensure optimal oxygenation and minimize the risk of hypoxia, a condition characterized by low oxygen levels that can result in mass oyster mortality [72]. Sites with higher tidal flow can enhance the oysters’ settlement and post-settlement survival. For instance, a study revealed that higher flow rates had a positive effect on larval settlement and post-larval settlement. Specifically, locations characterized by heightened flow exhibited an average survivorship rate of 72%, whereas areas with normal flow recorded a rate of 56%, and those with diminished flow registered a mere 22% [73]. Moreover, sites with appropriate tidal flow patterns can enhance the feeding efficiency of oysters [74]. For example, oysters filter plankton and other particulates from the water, and favorable tidal flow helps maintain a healthy supply of food while preventing sediment accumulation, which can suffocate oysters [75]. Consequently, by thoughtfully selecting sites with moderate currents, we can ensure that oysters have access to an ample food supply and minimize the risk of sediment buildup.

4.3.2. Substrate Suitability

The selection of substrate is an important factor to be considered in oyster reef restoration projects. Oysters require a hard substrate for their attachment and optimum growth. Hard substrates such as rocky bottoms, shells derived from previous oyster beds, or human-constructed structures, such as limestone or concrete, serve as a stable foundation for oyster larvae, commonly referred to as spat, to establish themselves and grow [76]. In contrast, soft, muddy bottoms are less ideal due to the potential for oysters to become buried or suffocated by sedimentation. For example, the populations of Crussostrea virginicu oyster significantly declined when grown under muddy conditions [77]. In another study, it was reported that the bottom cages had lower survival rates compared to floating cages [78]. This is likely due to issues such as sedimentation, fouling, and being stuck in the sediment, which can decrease survival and feeding efficiency. Furthermore, in the muddy bottoms, the chance of disease incidence can also be increased, which can affect the survival of the oyster species.

4.3.3. Protection from Predators and Human Disturbances

Oyster populations can be preyed upon by many marine predators, such as crabs, sea stars, drills, and even other species of oysters [79,80]. Therefore, cultivating oyster species away from predators can enhance the success of a restoration project. To safeguard oyster beds against predation, it is advisable to cultivate them in areas that are challenging for predators to access, such as protected coastal regions or artificially constructed reefs. The installation of predator deterrent apparatuses, such as nets and cages around the beds, physically prevents predators from reaching the oysters. Furthermore, the introduction of natural predators that prey on oyster predators, such as starfish and snails, can aid in controlling predator populations. Additionally, employing chemical or biological repellents, as well as implementing sound or light deterrents, can dissuade predators from approaching the oyster beds. Moreover, when selecting a site for an oyster reef restoration project, it is crucial to avoid areas with heavy boat traffic, dredging activities, or potential sources of pollution, such as industrial discharge or agricultural runoff. These disturbances have the potential to cause physical damage and introduce contaminants that can harm oyster populations.

4.4. Habitat Restoration

Without a doubt, preventing the loss of natural oyster habitat is the most important step in reducing oyster reef degradation, as it may take centuries for restored habitat to provide the same levels of biodiversity, functions, and services as original habitat. However, simply reducing or halting habitat loss is not enough. Habitat restoration is a powerful tool to reduce the impacts of oyster reef degradation. Scientists and coastal resource managers have employed oyster habitat restoration to recover essential ecosystem services and functions of oyster reefs. In this section, we will discuss how diverse technologies have been used in oyster habitat restoration, and how modern technologies are highlighted.

4.4.1. Artificial Substrates

Bivalve shells, particularly oyster shells, have been widely used as settlement substrates due to their high surface complexity and the release of chemical cues that attract and promote oyster settlement [81]. Oyster shells provide a surface for spat attachment and growth. However, the availability of natural shells for restoration projects is limited due to their high demand for other purposes [82]. Furthermore, the use of shells for restoration may pose security risks, as the transportation of shells from one region to another can increase the spread of diseases [83]. Additionally, ocean acidification can cause the decalcification of shells, and the placement of shells in plastic bags may introduce microplastics into the environment [84]. Therefore, considering the limitations associated with oyster shells, alternative natural and artificial substrates are being utilized for oyster reef restoration.

In order to address the issues surrounding oyster shells, various artificial substrates have been developed and utilized in reef restoration projects. A representation of artificial substrates used in oyster reef restoration has been shown in Figure 6B–E. These artificial substrates are deployed in ocean environments, serving as attachment points on which the oyster larvae can grow. Concrete, natural tone, canvas, plastic, and anchor blocks are among the most commonly employed materials in the synthesis of the substrates. Recently, biodegradable substrates like coir have been incorporated in the construction of artificial substrates, offering a protective habitat for oyster growth, settlement, and development [85,86]. Each of these substrates possesses unique structural and compositional characteristics that enable them to withstand diverse environmental conditions, thereby contributing to the survival of oyster reefs and the ecosystems they support. Furthermore, these substrates vary in terms of their economic cost and the specific habitats they create for oyster reef settlement, ultimately providing valuable ecosystem services.

Substrates that are used for oyster restoration also vary in their chemistry, porosity, color, surface texture, and durability [87,88]). These are the characteristics of substrates which interact with different environmental factors that determine to what extent oysters can settle on them. The chemistry of a substrate is significant due to the gregarious nature of oysters, which utilize chemical signals to communicate with members of their own species as well as with other organisms inhabiting alkaline surfaces, such as the bivalve shells of surf clams and concrete. This behavior is mediated through peptides [88,89]. The color composition of the substrate also affects the settlement of oysters. Most oyster larvae prefer to attach to brighter substrates as compared to darker substrates [90]. Moreover, absorbance and reflection of sunlight are also dependent upon the darkness and brightness of a substrate [25]. Darker substrate becomes especially unfavorable for oyster accretion due to climate change.

It is noteworthy that, for oyster settlement, substrate surface and texture can be more important than chemistry [90,91]. In continuously changing environmental conditions, the density and durability of a substrate determine its stability and suitability for oyster reef recruitment [92,93]. Less dense substrates disseminate during high-wave storm conditions, thus reducing the suitability of the substrate for oyster restoration and coastal protection as compared with denser substrate. A more rapidly biodegradable substrate is recommendable in areas with high larval supply and rapid reef deposition. However, a more durable substrate is suitable in areas with a slow reef deposition process and limited larval supply. Moreover, highly dense substrates are more beneficial, considering changing environmental conditions and wave surges.

4.4.2. Shell Recycling

Shell recycling is a crucial element of initiatives aimed at restoring oyster reefs. Shell recycling programs can be established with the goal of collecting discarded oyster shells from restaurants, seafood wholesalers, and individuals, and reusing them to construct new oyster reefs [94]. These shells undergo thorough cleaning and processing before being strategically placed to aid in the restoration of oyster populations. By engaging in the recycling of oyster shells, these programs not only prevent the wasteful use of valuable natural resources but also contribute to the restoration of crucial habitats [95]. Besides the environmental benefits, shell recycling programs also promote awareness regarding the importance of conserving oyster reefs and create opportunities for community engagement and participation in restoration endeavors. Ultimately, shell recycling plays a pivotal role in the restoration of oyster reefs and the preservation of coastal ecosystems.

4.4.3. Artificial Reefs Construction for Restoration

Artificial reefs are human-made structures placed in the marine ecosystem that provide a habitat for oysters to grow. These structures have shown comparable performances to natural shells. Deploying artificial reefs in areas with depleted oyster populations can assist in the restoration of these valuable ecosystems [76]. In addition to serving as a foundation for oyster growth, artificial reefs also provide a habitat for a variety of marine species, thereby promoting biodiversity in the region [96]. This, in turn, contributes to the overall well-being of the ecosystem and offers supplementary benefits for fishing and recreational activities. Overall, artificial reefs play a critical role in the restoration of oyster reefs, facilitating the reconstruction of these essential ecosystems and enhancing the marine biodiversity that relies on them. Through careful planning and strategic implementation, artificial reefs have the potential to mitigate the decline in oyster populations and improve the well-being of coastal ecosystems.

In artificial reef construction, various factors such as height, interstitial gaps, and reef structure are the key factors to be considered. The height of the reef plays a crucial role in determining the long-term sustainability and adaptability of its oyster populations [8,97,98]. It is imperative to establish a minimum reef height that ensures the survival of these populations, as a higher supply of larvae allows for lower initial reef heights. On the other hand, insufficient reef height can result in rapid sediment accumulation and subsequent reef degradation, which poses significant challenges to the success of restoration endeavors [99]. The presence of optimal interstitial spaces within the oyster reefs confers significant advantages to oyster recruitment and survival [52,100]. These spaces function as sanctuaries for juvenile oysters, affording them protection against predators and offering unhindered growth opportunities [100]. The ensuing heightened survival rates contribute to the expansion of larger oyster populations, thereby exerting a favorable influence on marine ecosystems, water quality, and biodiversity. Hence, the incorporation of interstitial space into artificial substrates utilized for oyster restoration is important in bolstering coastal habitat conditions. The third important factor that needs to be considered is the shape and structure of the substrate. For example, the longer the substrate is battered, the fewer artificial materials are needed to sustain and improve the reefs [101,102]. These factors are essential for the stability of diverse substrates where oysters can settle and grow, thus enabling them to effectively compete with environmental stressors and make valuable contributions to the ecosystem [92]. Complex habitats provide high protection from different environmental stressors to oysters; therefore, habitat complexity is highly important. Naturally complex habitats such as concentrate blocks, limestone rocks, and oyster shells provide high protection to oysters from different environmental factors, such as temperature, anoxic and hypoxic conditions, salinity, and predators [16]. Complex habitats also provide dense attachment sites for other associated biodiversity, that can be preyed on by other ocean animals, which favors or enables the oysters to still recruit and settle to make their habitat more complex and biogenic. Some physiological and biological processes such as predation, filtration, and wave attenuation are dependent on the shape, size, and pattern of the reef arrangement [103]. In addition, reef designs with large surface areas such as frozen and linear reefs provide refuge, food, and crabs. The ability of fissured circumferential reefs to facilitate a habitat is completed by the harboring of a large population. Similarly, substrate patterns that increase inside to outside rugose populations are beneficial for aquatic organisms that prey on reef eggs [104].

4.4.4. Three-Dimensional Printing Technology in Oyster Reefs Restoration

Recently, the use of engineering principles with ecological processes in ecological restoration projects has attracted significant attention. These eco-engineered methods also have the potential to improve regional biodiversity and enhance fisheries’ production [105]. To be more precise, ecological engineering aims to optimize the advantages of morphological, ecological, and socio-economic methods for protecting coastlines, all of which can contribute to the overall improvement of coastal resilience [106]. Three-dimensional printing or additive manufacturing are two technologies that allow the printing of 3D objects via the deposition of successive layers of material in a layer-by-layer arrangement, and this technology has been extensively used in oceanography [107,108]. The utilization of 3D printing technology has been proposed as a potential solution for the restoration of oyster reefs. This concept entails the application of 3D printers to fabricate artificial structures resembling oyster reefs, which can be strategically deployed in areas where natural oyster reefs have experienced depletion [109,110]. These synthetic structures are meticulously designed to replicate the intricate and irregular shapes characteristic of natural oyster reefs, thus providing optimal substrates for oyster colonization and growth.

Furthermore, several types of biopolymers obtained from natural sources, such as algae, seaweed, or marine organisms, can be used in the field of 3D printing for the purpose of fabricating artificial reefs. For example, the artificial reefs made from 3D printed biopolymers such as celluloses, polylactic acid (PLA), and polyhydroxybutyrate (PHB) have shown notable results in enhancing the establishment of coral species [109,111]. These innovative structures aim to restore marine habitats. The intricate composition of these biopolymers closely mimics the complex habitats of oyster reefs. Hence, these structures provide a stable substrate for the attachment and proliferation of oysters and other marine organisms, thereby facilitating the rejuvenation of depleted reef systems [112]. One of the primary advantages of utilizing 3D printing technology in the restoration of oyster reefs is the ability to tailor the structures according to specific environmental conditions [110]. By incorporating data on local environmental factors, such as water flow and sediment composition, scientists can design 3D-printed reef structures that are finely optimized for oyster survival and growth in a particular area. This customization significantly enhances the success rate of oyster reef restoration projects, as the structures are better suited to the local ecosystem.

Additionally, 3D printing technology enables the rapid and cost-effective production of artificial reef structures, which facilitates the efficient execution of large-scale restoration projects [113]. Consequently, this has the potential to expedite the recovery of oyster populations in degraded areas. Moreover, 3D printing technology allows for the use of sustainable and environment-friendly materials, such as biodegradable plastics, in the construction of artificial reef structures. However, the utilization of 3D printing technology for oyster reef restoration also poses challenges and limitations. For instance, the long-term durability and stability of 3D-printed reef structures in marine environments must be meticulously evaluated. Furthermore, the ecological impacts of introducing artificial reef structures into natural ecosystems should be extensively researched to ensure that they do not disrupt existing ecological processes. Overall, 3D printing technology holds the potential to revolutionize oyster reef restoration efforts by providing customized, cost-effective, and sustainable solutions for the recovery of these valuable ecosystems.

4.4.5. Use of Acoustics Technology in Oyster Reef Restoration

The use of sound technology is another effective strategy in oyster reef restoration. It is a cost-effective method that enhances spat recruitment [114]. This technology entails the utilization of submerged acoustic equipment, including hydrophones and sound recorders, to capture and analyze the acoustic composition of the reef habitat. Marine soundscapes offer crucial navigational cues when larvae are scattering in search of suitable habitat. These soundscapes provide information on habitat location and quality at spatial scales that significantly outweigh the impacts of other cues [115]. Consequently, soundscapes are hardly used in conservation or restoration projects, although they might be extremely important for ecological recruitment. This is concerning because, in areas where ecosystems have suffered, soundscapes have also suffered, endangering the supply of new recruits that are essential to the restoration of habitat and the maintenance of biological processes [116]. When it comes to restoring marine ecosystems (which usually happens in areas where soundscapes have been damaged) soundscape ecology may be an especially useful tool. This type of restoration depends on natural recruitment to seed recovery [117]. For example, in the presence of soundscapes, larval recruitment was increased by 300% as compared to control in a laboratory experiment [118]. In addition, spat can detect sound and move to the source so that settlement increases along horizontal gradients of increasing sound. However, anthropogenic noise can affect the process of recruitment [119].

In addition, acoustics technology can be used in monitoring the population dynamics of oysters and other marine organisms. By listening to the sounds that these organisms produce, researchers can gain valuable insights into behavior, distribution, and abundance. For instance, the sounds of oysters opening and closing their shells, as well as the calls of fish and invertebrates, provide important information about the overall health of reef communities [120]. Additionally, acoustic technology can be used to assess the physical structures of the reef itself [121]. By analyzing the pattern of sound propagation and reflection with the reef environment, researchers can better understand its architecture and composition. This knowledge is crucial for determining the suitability of the habitat for oysters and other organisms, as well as for designing effective restoration methods. Moreover, acoustics technology enables researchers to monitor environmental parameters that are vital for the growth and survival of the oysters [122]. Continuous monitoring of their parameters using acoustic sensors allows researchers to identify potential stressors that may impact reef health and take protective measures for its mitigation. More comprehensive long-term experiments are required to assess the use of sound technology in oyster reef restoration.

5. Challenges to Oyster Reef Restoration

Oyster reef restoration provides numerous benefits to mankind and aquatic biodiversity. However, these projects may face some issues that could be hurdles to their success.

(1)

Oyster reefs are complex ecosystems that are vulnerable to both environmental stressors and anthropogenic activities. The complex ecosystem dynamics can vary significantly between different habitats and regions. Understanding the complex interactions within the ecosystem can be challenging. In addition, natural variability in environmental conditions can affect the outcomes of restoration efforts, making it difficult to draw broad conclusions from specific studies.

(2)

There is a shortage of long-term monitoring and data collection. Oyster reef restoration often requires long-term studies to assess success. Short-term studies may not capture the full ecological impacts of restoration efforts. Furthermore, limited historical data on baseline conditions of oyster reefs can hinder the ability to evaluate changes and set restoration goals.

(3)

There are still many technical and methodological limitations in the field of oyster reef restoration. Globally, oyster reef restoration technology is still in its infancy. Determining the best methods for substrate placement, oyster culturing, and reef design often requires extensive experimentation and may not yield quick results. There is also a lack of standardized methods for evaluating restoration success, making it difficult to compare results across different studies and regions.

(4)

Understanding the genetic diversity of oyster populations and how oysters can adapt to changing environmental conditions is crucial for successful restoration, but research in these fields can be complex and resource-intensive. The impacts of climate change (e.g., rising sea levels and ocean acidification) can complicate research efforts, as these changes may alter the conditions under which restoration takes place and affect the survival of oysters.

(5)

Navigating environmental regulations and permitting processes can be time-consuming and may slow down research and restoration projects. In addition, integrating research findings into policy and management practices can be challenging due to differing priorities among agencies and stakeholders.

Addressing all the above challenges requires a coordinated effort among researchers, policymakers, and stakeholders to enhance the understanding of oyster reef dynamics and improve restoration practices. Collaborative, interdisciplinary approaches that integrate ecological, social, and economic considerations are vital for advancing restoration research.

6. Conclusions and Outlooks

There exists significant potential for both ecological and financial benefits arising from oyster reef restoration. Current evidence indicates that oyster reefs play a critical role in enhancing biodiversity, improving water quality, and providing habitats for a diverse range of marine organisms. In certain regions, efforts to restore these ecosystems have yielded promising outcomes, suggesting the feasibility of successful recovery initiatives. Conversely, in some locales, oyster reef restoration projects have not met their intended objectives. The utilization of artificial substrates in oyster reef restoration projects is a promising approach; however, further field studies are necessary to substantiate this method. Integrating ecological principles with technological advancements may prove beneficial in the restoration of oyster reefs. In order to effectively address challenges such as habitat degradation, disease vulnerability, and the impacts of climate change, sustained research and innovative restoration strategies are essential for moving forward. Collaboration among ecologists, policymakers, and local communities will be critical in developing effective strategies for the restoration of oyster reefs.