REVIEW   Open Access    

Colorful and nutritious abundance: potential of natural pigment application in aquatic products

  • Authors contributed equally: Ning Ding, Yongjie Zhou

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  • The promising future of natural colors in the food industry aligns with the shift in consumer preference toward healthier food options. These naturally derived ingredients gradually replace their artificial counterparts and find applications in a wide range of food categories, and aquatic products have emerged as one of them. In this work, we introduced the characteristics and extraction of several main types of natural pigments and also explored the positive outcomes of integrating the pigments, such as carotenoids, curcumin, anthocyanins, and betalains, in aquatic product processing and preservation. Their outstanding antioxidant and dyeing properties contribute to the production and storage of various aquatic products. This review aims to provide a comprehensive understanding of the current state of natural pigment applications in aquatic products and to provide inspiration for future research and industry practices.
  • In the modern era, humans have not often attempted to intentionally design a food system at any scale much beyond a local farm or limited region. In 2021, however, it is increasingly clear that profound transformation across multiple levels is required in how we produce and consume food if we are to stay within safe planetary boundaries on Earth[1, 2, 3]. This is evident from the scientific literature as well as recent reports on achieving sustainable food systems from major international organizations[4, 5, 6].

    The common catch phrase in this literature is that fundamental, or transformative change is needed within our food systems, where ‘transformative’ means 'system-wide reorganization across technological, economic, and social factors, making sustainability the norm rather than the altruistic exception'[7]. In this sense, food systems include all elements (nature, people, institutions, governance) and actions (from production through consumption) along with their environmental, economic, and social outcomes[8, 9]. This expansive definition is rooted in a social-ecological systems perspective on nature and people in which both environmental and human factors are considered in relation as they are mutually shaped by key drivers, interact across many scales, exhibit complex dynamics, respond to multiple feedbacks, and are subject to uncertainty and change over time[10].

    If the goal of a sustainable food system is the delivery of food and nutritional security for all people over the long-term with limited environmental degradation, then the biophysical basis for transformative change is obvious. Croplands cover about one third of terrestrial land on Earth[11] and agricultural activities contribute about 26% of total global greenhouse gas emissions[12]. Food systems are the primary driver of biodiversity loss and ecological degradation[11], the largest contributor to freshwater consumption[1], and are major sources of multiple pollutants including nitrogen[13], phosphorus[14], heavy metals[15], antibiotics[16], and microplastics[17]. If all non-food greenhouse gas emissions ended immediately, food systems emissions alone would likely carry us beyond a 1.5C rise in global temperature soon after 2050[18].

    Staying within safe planetary boundaries, however, is not just about the biophysical elements of food systems; the social aspects are equally important within a social-ecological framework. And, since 2014, in spite of six years of implementation of the food-oriented targets of the United Nations (UN) Sustainable Development Goals (SDGs), global food insecurity has been growing, with the number of hungry people reaching 690 million, about 9% of the human population[19].

    The above data portray elements of food security before COVID-19. The number of additional undernourished people resulting from impacts from COVID-19 is modelled to increase 83-150 million by the end of 2021[20], and projections show that there may be up to 840 million hungry people by 2030[19]. Therefore, the virus is seen by many as a wake-up call that has brought social vulnerabilities into focus across multiple elements of food systems, including farmer and laborer vulnerability, global supply chains, import/export trade policy, and more[21, 22]. Yet, as of the beginning of 2021, individual country responses to strengthen food systems have been minimal, despite multiple calls from international agencies and researchers to link food security measures with expanded support for public health.

    As COVID-19 spotlights weaknesses in food systems, other trends continue to put inexorable pressure on conventional agricultural activities. Total greenhouse gas emissions are projected to increase at an annual average rate of 2−6% out to 2030 with major contributions from rising carbon-intensive livestock production, growing beef and dairy consumption, and continuing cropland expansion into natural ecosystems[23, 24]. Longer-term trends appear to offer little relief. Out to 2050, the medium range projection for human population growth is 9.7 billion people, an increase of about 2 billion over 2020[25]. Over this period, some two billion people are expected to enter the global middle class with projections that they will use their increased wealth for more resource-intensive consumption, including eating many more animal products[26]. These two trends underlie projections for a 25−70% rise in global food production to meet demand to 2050[27].

    Transformative change in food systems is uniquely challenging given the links between food as a source of physical and cultural sustenance and its commodification through heterogeneous systems of private and public economics, institutions, and governance. Fostering change in food systems requires more than technical innovation; it is about how culture and identity shape individual attitudes about food. And food systems transformation is also about political decisions that influence policy, institutions, and governance[28].

    In response to these challenges, current food systems research is expanding to address links within and beyond how crops are grown in fields to the full range of agriculture practices within tele-coupled food systems in the 21st century[29]. However, even as concomitant understanding of the ecological and social sides of food systems is growing, coordinated research and international policy remains missing.

    In this broad overview paper, we briefly outline and explore critical problems and promising prospects for circular agriculture’s contributions to transitions to sustainable food systems in the Anthropocene. We define circular agriculture (CA) and provide historical context on its development. We then consider how CA may contribute to food system transformations in four key areas: multi-functional landscapes; sustainable intensification (focusing on nitrogen/crop-livestock management and digital agriculture); small holder farmers; and dietary change. We selected multi-functional landscapes, sustainable intensification, and dietary change following recent research that has identified specific sectors of food systems that, if prioritized, can deliver large co-benefits for climate change mitigation and adaptation, biodiversity protection, and degraded lands restoration[30, 31, 32]. We focus on smallholder farmers since their productivity and livelihoods are a major target of SDG2. For each of these areas, we offer suggestions for CA research that can stimulate new advances toward sustainability.

    The idea of minimizing harmful inputs and outputs in any production system through creating closed loops that recycle valuable end products back into a circular economy has been discussed for decades[33]. Several countries have pioneered versions of a circular economy as state policy (Germany in 1996, Japan in 2000), yet circularity in agriculture is a much older idea following the principles of ‘grow, make, use, restore’[34]. Circular agricultural systems involve 1) system thinking to design closed cycles of nitrogen, phosphorus, carbon, energy and water along ecological cycles and waste treatment re-use along social value chains; 2) consideration of multiple organisms including microbes (bacteria and fungi), plants, animals, and insects as they form food webs from producers to decomposers; 3) innovations using smart design, digital technology, artificial intelligence, and big data; 4) and efficient and effective design and decision making across multiple scales throughout the entire value chain, often using life cycle assessment (LCA) on a farm, within a company or a country, or at the global scale[35, 36]. CA is but one of several sets of practices that are aimed at implementing food system transitions; others include agroecology[37] and climate-smart regenerative agriculture[38]. There is considerable overlap among these collections of practices, even as they seek somewhat divergent goals.

    Today, CA in various forms is being implemented around the world from small farm fields to large countries. There is a tremendous diversity of projects, for example, in Europe[39], Africa[40], Asia[41], North America[42], Australia[43], and South America[44]. China and the European Union (EU) are leading CA proponents. China has had a national strategy for a circular economy since 2013, making much progress in increasing resource use efficiencies, and the country has been implementing a national sustainable agriculture plan since 2015[45]. In 2018, the EU issued a farm-to-fork agricultural policy including a comprehensive set of CA practices, though it has yet to be approved by member nations[46].

    One of the challenges of designing CA at any scale in any place is capturing the elements of complex food systems. These challenges are related to debates about whether to narrowly frame food systems as only about technological, supply-side issues (increase crop yields, close nutrient loops, re-couple crop-livestock links, etc.) to produce more food efficiently, or whether to include social and demand-side issues (improve smallholder livelihoods, create sustainable supply chains, promote dietary shifts, etc.) to produce more food security[47]. CA has a history of being technically framed; on these grounds, it has been critiqued for placing agricultural efficiency above social outcomes[48, 49]. But including all elements of food systems in CA is not a win/lose proposition; using a social-ecological framework in a world where food systems are often inefficient and inequitable requires that the social aspects of food systems be accounted for. Certainly, the international discussion about food system goals is no longer confined to maximizing productivity, recapturing wastes, and lowering environmental costs; it now includes optimizing outcomes across the full range of environmental and social concerns in complex systems of production and consumption[50, 51].

    Given the impacts of agriculture on natural ecosystems, it is clear that food systems transitions must include eliminating new cropland expansion into natural ecosystems while increasing on-farm protection of biodiversity, ecological functions and ecosystem services[11]. The latter can be accomplished through creating multifunctional landscapes on lands where crops are grown, thereby increasing biodiversity and ecosystem services values[52]. A host of practices are already being employed on farms to do this including: diversifying vegetation on field edges; incorporating agroforestry into fields; protecting semi-natural patches of vegetation in and around farms; creating ravine and riparian buffers; managing to increase pollinators; enhancing soil biodiversity; and more[53, 54, 55]. Understanding how much of the area of agricultural lands should be managed for biodiversity and ecosystem services is evolving. Currently, few countries have any minimum area requirements for conservation of natural habitats within working lands, though there is some research that shows protecting as little as 5% of within-field natural habitat yields benefits[56]. New work suggests a minimum goal of 20%, though the authors recognize that some places may need more or less land area protected[57].

    In addition to these practices, innovative CA projects are moving to increase connectivity across watersheds and regional landscapes to support plant and animal dispersal[58, 59]. Restoration of both on-farm and surrounding degraded lands is another practice that can link working lands with protected areas[60]. Connecting farms with larger landscapes requires a commitment from CA workers to gather science-based evidence about landscape links from field locations where they work and then sharing it with other actors at multiple scales. This is beginning to occur in China, where agricultural lands are being incorporated into spatial planning for the national system of Ecological Conservation Red Line areas[61]. At the global scale, linking food system and biodiversity goals will be especially important in 2021 since the UN Convention on Biological Diversity is convening, and the draft Global Biodiversity Framework that will set policy out to 2030 as yet contains no specific strategy for agricultural lands[62].

    Given the tremendous diversity of food systems from smallholder to large corporate farms, there is much room for CA to make contributions to learning about best practices to integrate agricultural lands into multifunctional landscapes. A general strategy of testing mixes of the practices mentioned here depends on the establishment of multiple pilot projects, monitoring research results to help define what works and what does not work at scale, and identifying costs and trade-offs to optimize implementation. Three critical actions can help support successful implementation. The first is working with local farmers to discover and implement place-specific, field-level practices that have co-benefits for crop production and biodiversity[63]. The second is developing regional landscape-scale spatial planning that can explore connecting food systems with biodiversity, ecosystem services, climate, and other outcomes[64]. The third action lies with looking for opportunities to convey research outcomes to local and regional/national decision makers. These links can serve to build support for project outcomes with institutions and decision makers, and may spark initiatives that support new multifunctional landscape policies.

    Sustainable intensification, where agricultural outputs are increased while environmental impacts are reduced, is an essential component of transforming food systems[47]. There is much overlap here with CA. Sustainable intensification has focused on reducing external inputs (fertilizers, pesticides,) and decreasing environmental impacts in service of growing more food on less land. CA has emphasized closing nutrient loops and creative recycling of wastes. Both approaches begin at the field level and share a broad mix of technical practices; we focus here on two: nitrogen/crop-livestock management, and digital agriculture.

    Nitrogen cycles on most agricultural lands are open, highly inefficient, and unsustainable due to the overuse of synthetic fertilizers, poor animal waste management, and the de-coupling of animal/crop production loops[65]. Together, these inefficient practices have resulted in dramatic increases of various forms of nitrogen pollution in air, water, and soils[13,66, 67]. Growing global livestock production resulting from increasing demand for consumption of animal products, especially meat and dairy, accounts for the vast majority of these pollutants, and there are large global disparities in all forms of nitrogen pollution between regions, countries, and subnational areas[68]. For example, fertilizer application rates in China are four times greater than in the EU, while application rates in Africa are minimal[69].

    Yet the economic and social value of livestock production add complexity to finding solutions for better nitrogen management. Globally, 34% of all farm market value comes from animal products[70]. Some one billion people, mostly local smallholders often living on lands less suitable for growing crops, depend on stock for their nutrition, livelihoods, and many cultural values[71].

    Ongoing research is helping to identify what places and practices must be prioritized so that CA and sustainable intensification solutions for livestock production can be better targeted and implemented. The general use of LCA is widely advocated[72, 73]. Many studies also recommend particular focus on three areas: local fertilizer use efficiencies, changes in animal feed production, and manure management[66, 74, 75].

    Numerous changes in fertilizer use efficiency are being pursued within CA. These include reducing urea-based fertilizer application rates, deep placement of fertilizers, and changes in crop straw use[76]. Much innovative work is being done with improving animal feeds including using a variety of new supplements in animal foods (food wastes, tannin-rich plants, fungi, algae, insect proteins)[77, 78, 79]. For improved manure management, there is active experimentation using anaerobic digesters, biogas production, membrane filtration systems, worm composting, algal cultivation, and fungal digestion[77, 80, 81, 82].

    Efforts to reconnect crop-livestock loops are focused on getting animal wastes back onto fields to replace synthetic fertilizers[83, 84]. In addition, researchers are pursuing innovations using algal and fungal-based waste treatments[77]. Zhang and colleagues[85] in China have gone farther than many researchers by looking at county-level nitrogen management practices to discover and showcase where the most efficient management is being done. This kind of fine-scale research provides a model that other countries can pursue to optimize livestock management.

    Nitrogen inefficiencies are not limited to agricultural practices; they occur across food systems from fertilizer production and processing to retail and trade[86]. Further, global trade in animal feedstocks (soy and corn) and meat allows importing countries to avoid the embodied LCA costs of nitrogen pollution. Embodied costs also extend to ground water depletion[87], ecosystems services[88], and carbon emissions[89]. We know of no country accounting for embodied flows in their agricultural policy or national food systems planning; this is an area where CA research using LCA and other modelling at the global scale can make important contributions.

    At all scales, for nitrogen management to meet the sustainability standards of safe planetary boundaries, major transformation of conventional practices will be needed. These include more mainstream use of cost/benefit and trade-off analyses across national agricultural sectors and international trade, redesign of research programs, local extension services, agricultural credit and insurance systems, and food safety regulations[90, 91]. It is also clear that increasing supply-side efficiencies without also addressing demand-side dietary change (and food loss and waste) will not solve nitrogen cycle problems[92]. The expectation is that the positive co-benefits from reduced water and air pollution and greenhouse gas emissions along with increases in benefits to public health and food security will drive increasing nitrogen cycle efficiencies throughout food systems.

    Innovative use of digital technologies is expanding across food systems at all scales, providing producers with more targeted information and tools to assist with growing crops efficiently and linking them into supply chains[93, 94]. Digital agriculture refers to the integrated use of digital and geospatial information technologies to assess, manage, and monitor conditions in the field so that optimal agricultural outcomes may occur. Mehrabi[95] outlines three key areas: data generation (for example, mobile devices, drones, field sensors, satellites), data processing and predictive analytics (big data, machine learning), and human–computer interactions (ways to blend voice, text and images to improve understanding and communication of results). These technologies are assisting farmers to optimize amounts, timing, and placement of fertilizers, nutrients, and water, while also enabling better monitoring and communication of environmental conditions in fields and across landscapes. Digital technologies can also help to create supply-side links to financial services for farmers and foster demand-side environmental traceability along supply chains.

    Digital agriculture is evolving, but it is not a panacea to solve food system problems. While digital methodologies have been hailed as a breakthrough to provide smallholders with useful data and market links primarily through mobile phones, such use remains limited. Only 24−37% of global smallholders are connected to the Internet, and there are wide country and regional disparities in access and use[95]. In less wealthy countries, there are technological barriers due to poor internet infrastructure, data access costs, and private sector control of software and security[96]. Social barriers include disparities in adoption readiness, concerns about data ownership, and unequal gender access; these issues highlight the fact that adoption of digital agriculture has political as well as technological sides. Even where digital agriculture methods are in relative wide use, research has yet to determine their many tradeoffs[97], and economic and environmental costs/benefits[98]. CA researchers can make contributions here by using LCA studies that analyze trade-offs that extend beyond individual farms/farmers throughout supply chains to determine the comparative costs and benefits of using smart farming tools.

    Overall, the future is bright for the continued expansion of multiple sustainable intensification practices. Farmers working on 9% of global agricultural lands are already implementing at least one sustainable intensification measure[47]. CA researchers can focus on how to speed up adoption of the broad range of sustainable intensification practices, especially in regions where farmer needs are great and progress has been slow.

    Smallholder farmers are important actors in the transition toward sustainable food systems; they are the focus of SDG2 with its goal of doubling smallholder productivity and income by 2030. Of all farms in the world, about 83% are less than 2 h in size[99]. These farms provide 50% of global food calories and over 70% of food calories to people living in Latin America, sub-Sahara Africa, and South and East Asia[100]. At the same time, smallholders are often poor and subject to food insecurity.

    Despite relatively limited research, we do know something about what smallholder farmers need to be better served in sustainable food systems. These include enhancing extension services while respecting local agricultural knowledge, building farmer cooperatives, offering education and training, securing market access, and increasing targeted forms of private sector and government support[28]. With a focus on meeting SDG2, CA researchers and practitioners can play important roles by working with smallholders to experiment with, understand, and implement these actions.

    Extension services need to scale up provision of: forward-looking information about crop varieties suitable to regional changing climates[101]; methods for smallholders to re-couple crop/livestock links, including managing crop biomass[69]; and assistance with producing crops (legumes, nuts, etc.) that can replace animal products as dietary shifts occur[32]. Respect for farmers’ local knowledge must be part of enhanced extension services given that smallholders have not often been consulted about their needs[102].

    Farmer cooperatives and other forms of self-organized groups have been shown to support collective action around growing new crops, and gaining access to markets[103]. Co-ops often build mutual trust among farmers which is often necessary to support innovative behavior during times of change in food systems. Creating more co-ops, however, does not automatically lead to better outcomes for smallholders; group efforts often show a positive effect on farmer income and a mixed influence on crop yields and crop quality[104]. Working with farmer co-ops can help CA researchers to better evaluate costs and benefits of this form of social organization and how it may contribute to greater on-farm efficiencies and off-farm market links.

    Two large studies of smallholder needs found that education and training provide important ingredients for making progress in food system transitions[101, 28]. These actions can be integrated into extension services and cooperatives with particular attention paid to women, who make up about 50% of the rural agriculture labor force[105]. Women are commonly overlooked by local officials and academic researchers, but recent work is beginning to change this[106]. Chanana and colleagues[105] use a multi-factor model that maps locations where female farmers are most vulnerable to climate change and food insecurity so that decisions about where to provide services can be prioritized. This model can be adopted by CA researchers and other investigators to provide details that are specific to local research sites.

    CA researchers are beginning to work to establish better links between smallholders and new markets for their products. This work often begins on a farm assisting a smallholder to connect with nearby markets (often urban consumers) to purchase her new, sustainably-grown product[107]. But it does not end there. Supply chains with their multi-faceted environmental and social footprints often extend beyond local and regional levels since one-third of all food is globally traded and crosses two or more international boundaries[70]. For globally important products like soy and beef, the embedded impacts of production and consumption have serious environmental consequences; for example, the greenhouse gas emissions footprint of beef exported to the EU from Brazil comes close to cancelling out all EU carbon mitigation goals[108]. Food systems policy research suggests building transparent and traceable supply chains from smallholder farms to global networks using digital means to close loops in tracking environmental and social costs and benefits[109, 110]. This work faces complex challenges across multiple sectors of tele-coupled food systems[29]. For CA researchers working with smallholders, a critical decision is deciding how far up supply chains and away from small farm study sites one should go to account for these impacts[111, 112]. Eco-certifications, improved product labelling, and LCA are tools to help do this, but transformative change in global food systems will eventually require reevaluation of national and international supply chains.

    To better address the needs of smallholders far removed from global trade, local and national governments have roles to play in three main areas—infrastructure, incentives, and financial support. For infrastructure, governments should prioritize provision of irrigation for the 37% of smallholders in water-stressed regions around the globe who likely lack any means to irrigate their fields[113]. Digital network connections for smallholders and facilities for food storage and transport to reduce post-harvest food losses (and bolster farmer profits) are two additional areas where more government attention is needed. Creating positive incentives that influence smallholder behavior is another area where governments can act. These range from relatively straightforward actions like providing greater access to credit and crop insurance[107] to revising regulations for digital access and data privacy[114]. More challenging changes are the need to address long-standing land tenure problems that confer high levels of risk to farmers and reduce agricultural innovation[115].

    Dietary shifts toward more nutritious, plant-based foods will also be challenging as we learn how to construct a more sustainable food system. In fact, of all strategies out to 2050, plant-based diets (56% reduction) and diets following improved nutrition guidelines (29% reduction) yield the largest modelled decreases in greenhouse gas emissions from global food systems[18,116 ]. This means that animal products, especially meats, must play a reduced role in many human diets going forward. This is a demand-side area of food systems analysis that has been so far been little addressed by CA researchers.

    Dietary shifts away from animal foods at the speed and scale that appear to be required will be difficult to encourage. Though animal products are the single largest source of greenhouse gas emissions from food systems, global production and consumption of these products are rising[5]. And there are pronounced dietary differences between countries that must be accounted for in crafting strategies to encourage shifts away from animal foods. For example, beef consumption in the US has declined almost 36% since the 1970s, but overall consumption of all meats remains very high[23]. In China, per capita meat consumption is much less than in many countries, but it is steadily rising[117].

    There are multiple strategies that are essential to promoting global dietary transformative change. The question is, if dietary change is a priority, then what do we know that would facilitate the rapid adoption of new ways of eating? Given the diversity of global diets, there is no single answer to this question; dietary shifts must be attuned to every country and cultural context. However, scientific information does not much influence peoples’ decision making when it comes to what they choose to eat; taste, tradition, and values about foods are more important. The main drivers of dietary change are social norms among peer groups and individuals’ beliefs that what they choose to eat can contribute to group dietary shifts[118]. Lack of knowledge about the environmental impacts of food choices is widespread. Even in a relatively well-educated country such as the US, only 43% of people know about the climate impacts of eating meat[119]. This suggests that government-led programs that employ relatively strong dietary incentives will likely be needed[120]. Past government efforts to spur national dietary shifts have occurred in several countries over spans of 2−4 decades, however, most of these programs only focused on supply-side growth in crop yield and income from products with scant attention to overall food systems sustainability[121].

    The Lancet Commissions’ work[3] has established a global model to encourage transitions toward healthy eating. Yet, less than half of all countries have established national dietary guidelines[122], and costs of dietary change for poor people in less wealthy nations may be prohibitive without some form of subsidy[123]. An important knowledge gap that CA researchers could address here is evaluation of what cost-effective, protein-rich crops might help to replace animal products as the transition toward consuming less meat and dairy proceeds. Other steps would be for countries to solidify national dietary standards followed by efforts to reach international consensus on global guidelines and monitoring to track progress. These actions will certainly demand some form of international cooperative mechanism; it is here that trade-offs between food systems and climate, biodiversity, public health, and sustainable development goals may lead to co-benefits that compel action.

    At the beginning of this paper, we observed that humans have little historical experience with intentionally designing food systems much beyond local levels. The task humanity faces today is considerably greater; from tiny subsistence farms in sub-Sahara Africa to the more than US100 billion dollars of international trade in beef, corn, and soy, food systems require a 'major shift in mindsets'[2]; engagement with 'a massive scientific challenge'[124]; and 'radical and coordinated action'[125].

    How may we accomplish these things? There is some general work that describes how social transformations unfold over 10−30 years[126, 127], and reviewing the history of progress on meeting international goals for climate mitigation and biodiversity protection confirms that 2−3 decades (or more) are likely required. Studies at national[75] and global scales[32] suggest that significant progress can be made in food system transitions by 2030 and out to 2050, but none of this research comes close to projecting net zero greenhouse gas emissions from food systems. Given these timelines and projections, it is imperative that CA and all food system researchers be more cognizant of how their work addresses implementation of transformative actions as described in this paper. To encourage such efforts, we offer four observations.

    First, food system researchers can benefit from what has already been discovered about how societal transformations are shaped and stimulated[128, 129]. Are there actions that may accelerate change in food systems in a preferred direction? Research suggests that societal transitions may be encouraged by: supporting transdisciplinary knowledge co-production so that the science, social issues, and the politics of change are equally addressed[130, 131]; identifying and then working with actors, institutions, and decision makers who are willing to support innovative projects[132]; setting strategic priorities for action since resources (funding, workers) will likely be insufficient to accomplish every task[133]; and experimenting with multiple pilot projects to learn what works best before scaling up initiatives[134]. These actions, by themselves, may not yield much momentum for change; however, used in combination, they may spark shifts that lead to deeper transformations. Researchers investigating climate change and energy transitions are already using these lessons to design projects and recommend implementation measures; CA researchers may also benefit from experimenting with these methods.

    Second, it is important to emphasize how the employment of innovative tools can stimulate food systems transitions. These tools include: More frequent use of LCA to help define cost/benefits of CA projects; incorporating the full range of food system actors and institutions into CA analyses so that trade-offs throughout the system are routinely revealed; and greater use of multi-actor, multi-sector spatial assessments that build links between land, water, food, and social systems[97]. If sufficient use of these tools can be sustained across multiple sectors of a countries’ food system, then the scientific basis for national planning may be strengthened. Science-based national planning may, in turn, contribute key ingredients to the negotiation of a platform for international food systems cooperation.

    Third, on the matter of governance, general lessons from transformative change research along with specific observations from food systems analysts show that transitions are often slowed down by established institutions and decision-makers[135, 136, 137, 138]. This makes sense since, by definition, CA and other movements toward food systems sustainability offer alternatives to the existing norms, policies, and power relationships of conventional, linear agriculture. Conventional agriculture actors often believe that the price of food systems transformation is prohibitive due to redistribution of cost and benefits throughout social-ecological systems[4,139]. Despite these challenges, there are methods that CA scientists and practitioners can wield to more directly address the governance aspects of food systems. One way is for CA workers to strategically use the tools and techniques outlined in this paper while continuing to ask fundamental questions: ‘what does full cost accounting reveal about barriers and bridges to the true price of affecting change in food systems here?’; ‘how can we work collectively with local people, government, and other actors in this place to design and implement sustainable foods solutions?’; ‘who are the specific decision makers that could use my research to promote change and how do I best communicate with them?’ These practical questions demand active solutions to sort out the inevitable tradeoffs that are found throughout all food systems.

    Finally, it is important to remember that food systems evolve through peoples’ everyday behavior where seeds of change are planted that accumulate and are amplified over time. These incremental, 'small wins'[140], 'small stories of closing loops'[141], and 'bright seeds'[142] range from a farmer adopting a climate-smart crop, to a county-level decision maker funding more extension services, to a food systems researcher incorporating ecosystem services, food systems, and urban land-use into an improved, spatially-explicit model that can better serve government planners. CA researchers do not have to foment a revolution; however, they do have to think more strategically about which steps have a better chance than others to initiate and sustain food systems transformations.

    The Anthropocene will continue to offer many challenges and opportunities to effect transformative change in food, climate, and biodiversity protection so that human endeavors stay within safe planetary boundaries. In 2021, there will be additional opportunities to support secure food systems including the UN Food Systems Summit (https://www.un.org/en/food-systems-summit); the Nutrition for Growth Summit (https://nutritionforgrowth.org/events/); the Convention on Biodiversity Conference of the Parties 15 (https://www.cbd.int/convention/); and the United Nations Framework Convention on Climate Change Conference of the Parties 26 (https://www.ukcop26.org/). The time for planting transformative seeds of change is now.

    The field of sustainable agriculture is vast; there are 685,000 hits to the subject on Google Scholar since 2016, and over 12,000 papers referenced in Scopus (as of 12/21/20). For this review paper, we did not attempt to thoroughly summarize this literature; instead, we selectively searched for papers within this extensive field that focused on circular agriculture; multifunctional landscapes; sustainable intensification (including nitrogen management in agriculture, crop/ livestock management, and digital agriculture); smallholder farmers; and global and national-level dietary change. We emphasized work published since 2015 (reflecting the timeline of implementation of the SDGs), and scoping reviews and other syntheses of the above portions of the sustainable agricultural literature that offered results extending beyond a specific farm field setting. We filtered our search to highlight transdisciplinary processes and cross-links to multiple areas of food systems that suggested innovative areas of research. In all, we reviewed abstracts from 409 papers which led to the reading of 210 papers of which 142 are cited in this review.

    This work was generously supported by the Key Project from the Ministry of Sciences and Technology of China (No: 2017YFC0505101), and CGIAR Research Program on Forests, Trees and Agroforestry (FTA). REG was supported by the Chinese Academy of Sciences President's International Fellowship Initiative (PIFI) for visiting scientists. We thank three reviewers for comments that improved the manuscript.

  • The authors declare that they have no conflict of interest.

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  • Cite this article

    Ding N, Zhou Y, Dou P, Chang SKC, Feng R, et al. 2024. Colorful and nutritious abundance: potential of natural pigment application in aquatic products. Food Innovation and Advances 3(3): 232−243 doi: 10.48130/fia-0024-0023
    Ding N, Zhou Y, Dou P, Chang SKC, Feng R, et al. 2024. Colorful and nutritious abundance: potential of natural pigment application in aquatic products. Food Innovation and Advances 3(3): 232−243 doi: 10.48130/fia-0024-0023

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Colorful and nutritious abundance: potential of natural pigment application in aquatic products

Food Innovation and Advances  3 2024, 3(3): 232−243  |  Cite this article

Abstract: The promising future of natural colors in the food industry aligns with the shift in consumer preference toward healthier food options. These naturally derived ingredients gradually replace their artificial counterparts and find applications in a wide range of food categories, and aquatic products have emerged as one of them. In this work, we introduced the characteristics and extraction of several main types of natural pigments and also explored the positive outcomes of integrating the pigments, such as carotenoids, curcumin, anthocyanins, and betalains, in aquatic product processing and preservation. Their outstanding antioxidant and dyeing properties contribute to the production and storage of various aquatic products. This review aims to provide a comprehensive understanding of the current state of natural pigment applications in aquatic products and to provide inspiration for future research and industry practices.

    • The characteristic of color enables the differentiation of various food commodities types and qualities. The perception that color is linked to taste, freshness, shelf life, and nutritional value has driven the demand for coloring materials in food processing and storage[1]. The utilization of naturally derived colors in food is believed to have started long back in prehistoric times, then came the 19th century when chemically synthesized colorants were brought to the forefront and gained more popularity[2]. Despite their low production cost and good chemical stability, increasing dissatisfaction with synthetic colorants' detrimental and allergic effects gradually led to their limited use[3]. The public's awareness of safety and environmental conservation has rekindled enthusiasm for research on natural pigment sources. Advantageous characteristics such as the biodegradable nature and additional function of naturally derived pigments over their synthetic counterparts enhance their acceptability for utilization as additives not only in food systems but also in the cosmetics and pharmaceutical industries[4,5].

      Natural pigments ubiquitously exist in plant tissue, animal structure components, and microorganisms, including colorants and bioactive compounds. Fruits and vegetables constitute a significant part of our diet and serve as the primary source of chlorophyll, carotenoids, flavonoids, and betalains, the main types of edible pigments found in plants[6]. Pigments used for food coloration or nutraceutical purposes such as carminic acid (E120) and astaxanthin are derived from insects and microorganisms[7]. Besides the health benefits, natural pigments' antioxidant and antimicrobial efficacy have gained immense importance in recent years, demonstrating the potential to be a promising health-promotional ingredient and a food quality enhancer. As more and more attention is paid to their functional application in food preservation and quality improvement, the primary concern lies in maintaining the stability and biological properties[8]. These naturally derived pigments typically carry some limitations in food application when exposed to process stress (e.g., thermal processing, high-pressure, oxygen, or extreme pH values) and in-vivo environment (presence of enzymes and low-pH in the gastrointestinal tract). In this regard, various nanocarriers or stabilizers and encapsulation techniques are investigated as stabilizing methods to offer more options for utilizing natural pigments[9].

      Aquatic products are regarded as one of the important sources of dietary nutrients, providing nearly 20% of the global consumption of animal protein with high economic benefits[10]. The high nutritional value, palatability, and delicacy gained aquatic products increasing popularity. As a global food commodity, transporting and storing recently captured aquatic species for an extended time is necessary, followed by various processing methods to cater to the requirements of manufacturers, businesses, and customers. However, owing to the rich content of proteins, polyunsaturated fatty acids, and high water content, this type of product is more likely to undergo sensory and nutrition degradation than other muscle foods, which is induced by lipid and protein oxidation, enzymatic change, and bacterial spoilage[11]. Many antioxidants, cryoprotectants, and novel techniques have been used in aquatic food processing and storage[12,13]. The significant role of natural pigments in this context is emerging. For a while, pigments were applied in fish and shrimp products for color-protecting or coloration purposes. Now, they are more often used in quality enhancement, preservation, and packaging as their diverse functions have been widely perceived[14]. To our knowledge, a comprehensive overview of incorporating natural pigments into aquatic products has not been summarized. Here, recent research progress on natural pigments application with a specific emphasis on aquatic products is overviewed, in the hope of providing directions for further development of pigments in improving the quality of aquatic products.

    • Natural pigments' characteristics and chemical properties influence their applications and regulations in certain environments. Depending on the features of the resource, color, solubility, and chemical structure, pigments can be classified into different categories. Considering the molecular polarity and basic properties, they can be divided into water-soluble, lipid-soluble, and ethanol-soluble pigments. Generally, betalains and anthocyanins are soluble in water, while chlorophylls and carotenoids are soluble in lipids. From the perspective of diverse structures, these compounds contain categories such as carotenoids, iridoids, indoles, polyphenols, pyridines, pyrroles, etc. Based on natural occurrence, the classification of carotenoids, chlorophylls, betalains, and anthocyanins is currently adopted and investigated in most studies (Fig. 1).

      Figure 1. 

      Classification of the major natural pigments.

    • Showing colors include yellow, orange, red, and purple, carotenoids (E160) provide vibrant and attractive appearances for various vegetables, fruits, and flowers due to their chromophores consisting mainly of a chain of conjugated double bonds[15]. As a class of polyene terpenoids, there are two types of carotenoids: carotenes (α, β, γ-carotene and lycopene) and xanthophylls (lutein, zeaxanthin, astaxanthin, capsaicin, peridinin, etc.) distinguished by the existence of oxygen functional groups in the polyunsaturated hydrocarbon[7]. Up to now, with a wide distribution that includes algae, photosynthetic bacteria, insects, fish, and crustaceans, approximately 700 carotenoids have been identified, of which 40 can be consumed by the human body[16]. Astaxanthin, an extensively investigated carotenoid widely distributed in aquatic organisms, can be synthesized by shrimps and crabs from β-carotene, acting as an antioxidant and enhancing protection from lipid peroxidation[17]. Carotenoids have been employed as a coloring component in various foods, including butter, popcorn, fruit juice, ice cream, and fish products[4]. Especially in aquatic species, astaxanthin, and other biosynthesized carotenoids provide accurate color and higher consumer acceptance for fish fillets and surimi[18].

    • Chlorophyll (E141) is built of a symmetrical cyclic tetrapyrrole with a centralized magnesium atom. The two types of chlorophylls that are commonly used in industry and present in higher plants are chlorophyll a (with a methyl group) and chlorophyll b (with an aldehyde group). The structure variation leads to the appearance of a yellow-green color in chlorophyll a and a green-blue color in chlorophyll b. Another member of the porphyrin group of natural pigments is chlorophyllin, which is more stable than chlorophylls. Ester bond hydrolysis leads to the formation of chlorophyllin, resulting in a shift of the pigment from lipophilic to hydrophilic[4]. However, both types show low resistance to acid and heat and are easily degraded compared to other natural pigments. While treated with weak acid, the central magnesium ion would be displaced by hydrogen ions, forming the pigment called pheophytin with an olive-brown color[19]. Among the green colorants, sodium copper chlorophyllin (SCC) or copper chlorophyllin (E141) is the most used with qualifications worldwide[20]. This kind of semi-synthetic product derived from edible resources has been applied in vegetable and fruit preserves, fruit juice, alcoholic drinks, jelly, and candy dyeing.

    • Anthocyanins (E163) are accepted as the glycoside form of anthocyanidins in chemical terms, with enhanced stability due to glycosylation and acylation. As an important subclass of flavonoids, one of the common groups of phenolic compounds of plant origin, anthocyanins possess a basic structure of two benzene rings linked with different sugar residues, differing in degree of hydroxylation and methoxylation, glycosidic substitution, and possible acylation[21]. Found in all tissues of higher plants, they impart brilliant red or blue color to flowers and fruits, which is different from the range of colors (usually yellow) derived from other groups of flavonoids[22]. Purple grapes, berries, black carrots, and red cabbage are the primary sources for extracting anthocyanins. Due to the biological potential of elimination of superoxide free radicals, evidence from clinical trials and epidemiology studies has suggested the beneficial effects of anthocyanins on human health[23,24]. Furthermore, the capacity of anthocyanins to inhibit the growth of bacteria, such as E. coli, has received increased attention from researchers interested in improving stability for a broader application in the industry. Since there are some restrictions on the application potential under certain circumstances when exposed to heat, oxygen, enzymes, light, etc., co-pigmentation and encapsulation have emerged as increasingly prominent solutions to strengthen the color and stabilize the bioactivity.

    • Belongs to a class of N-heterocyclic compounds, betalains (E162) are ammonium derivatives of betalamic acid. Typically found in red beet, there are two major groups of betalains: red-violet betacyanins and yellow-orange betaxanthins. The categorization of the pigment is determined by the specific composition of the extra residues. Betaxanthins show high similarity in function with anthocyanins, yet these two pigment types have never been discovered in the same plant, indicating their mutually exclusive characteristic[25]. After the identifications of betacyanin from red beet[26] and betaxanthin from yellow-orange cactus pear[27], both types were addressed as betalains in the 1960s. Compared to anthocyanins, betalains possess an extended pH stability range of 3 to 7 and higher tinctorial strength. Its high hydrophilicity renders betalains more appropriate for incorporation into food. Depending on the pH, they change color from blue and violet to red in alkaline to acidic environments. However, it turns yellow when treated at temperatures over 70 °C, which is why betalains are exclusively suitable for coloration in non-thermal processing food.

    • Other prominent pigments commonly found in nature and employed in food processing involve polyphenolic pigments and pigments of microbial origin. The most representative pigment of polyphenols is curcumin (E100), which is widely used as a bioactive ingredient, functional additive, and herbal medicine. Strong antioxidants, anticancer, antibacterial activity, and dyeing properties with low toxicity are the advantages of its various utilization in the food industry[28]. For its lipophilic nature, curcumin utilized as a food coloring agent includes the following types: water-dispersible curcumin oils, oil-soluble purified curcumin, and curcumin powder. In the past few years, considerable attention has been paid to the fresh-keeping effects of curcumin on food, such as shelf-life extension and maintenance of nutrition and senses, especially the application of curcumin-loaded materials in preserving fruit, meat, and seafood. Nanocarriers and encapsulation technology have been used to increase curcumin's stability and solubility, thus ensuring its adaptability for practical uses[29].

      Monascus pigments are the secondary metabolites from Monascus species. They are widely used in China, Japan, and many other Asian countries, and they have a long history as edible colorants owing to their bright colors, excellent solubility, and high safety. These pigments are traditionally added as flavoring and coloring agents to Chinese food, such as fermented bean curd, fish cake, roast duck, and preserved dry meat and fish products. In Europe, they are considered a partial substitute for nitrate salt in meat and sausage preservation[30]. The pigments primarily present three colors: red, orange, and red, depending on the absorbance maxima at different wavelength ranges, and they can be converted into each other by reactions.

    • For commercial exploitation, it is imperative to avoid color fading and activity loss of natural pigments to ensure product quality and consumer satisfaction. Therefore, advanced approaches and progress are needed to stabilize natural pigments and increase their bioavailability. Numerous studies have been dedicated to devising strategies aimed at protecting pigments against degradation under various application conditions, such as the addition of stabilizing compounds, the use of metal ions, and encapsulation (Fig. 2).

      Figure 2. 

      Strategies for stabilization pretreatment of natural pigments.

    • Hydrocolloids are excellent candidates in the stabilization enhancement of pigments via non-covalent interactions. In contrast to the physical barrier of encapsulation, this interaction allows the formation of supramolecular assemblies of pigments and hydrocolloids. Pectin, an anionic polysaccharide, shows pH-dependent interaction and constant hydrogen bond, which is suggested to improve anthocyanins' stability and bioavailability[31]. Acacia gum and alginate are also used to form complexes with anthocyanins, betalains, and chlorophylls for stabilization, lowering color loss, and pigment degradation rat[32]. Supramolecular complexation with hydrocolloids is now attracting researchers' attention as a feasible method to increase pigment stability. Nevertheless, the addition of hydrocolloids in food products may lead to a change in textual properties and appearance, additional research is needed.

      Binding to protein or carbohydrates provides another strategy for stabilizing and applying pigments to the food system. Various proteins from aquatic species have been shown to bind astaxanthin in different binding ways, such as lipoprotein, muscle protein, and glycoprotein. Zhang et al.[33] demonstrated that the interaction of shrimp ferritin and astaxanthin provided defense against thermal conditions and oxidative damage induced by Fe2+. It is worth noting that one ferritin molecule is estimated to bind 48 astaxanthin molecules, and the improved water solubility facilitates its applications in the food industry. In microalgae, AstaP (astaxanthin-binding protein) is identified as an efficient carotenoid solubilizer, which provides potential carotenoid delivery approaches[34]. Moreover, catechin and β-cyclodextrin contribute to the deceleration of pigment degradation processes. Both of them were found to show promotive effects on the storage stability of betacyanin besides maintaining the visual color attributes in the model beverage[35].

    • Metal ions are essential for the structural integrity of certain natural pigments. According to the study by Cao & Dong[36], adding Na2CO3 salt could extend chlorophyll color retention time to 119 d while increasing recovery efficiency by up to 150% during extraction. Furthermore, some pigment molecules are capable of metal chelation and, in the presence of polysaccharides, achieve enhanced stability. The binding of metal cations are attributed to several hydroxyl groups present on the B-ring of anthocyanins[37]. In a comparison study, at the same concentration, more charged metal ions were suggested to have better protective effects on natural pigments, probably due to their increased capacity to bind free hydroxyl groups[38]. Although the metal cations cannot solely prevent pigments from degrading under heating conditions, they stabilize pigments in the presence of polysaccharides. Interaction with polysaccharides enables the formation of a more stable complex, thus preventing the dissociation of anthocyanin-metal chelates. Luna-Vital et al.[39] evaluated the color and chemical stability of colored corn anthocyanins in the beverage model with the addition of zinc ions and alginate. Alginate could protect anthocyanins from thermal degradation under lower temperatures, while the combination of these two additives showed higher efficacy in promoting chroma stability of the incubated beverage. Meanwhile, the combination of 0.02% zinc and alginate was capable of prolonging the half-life of anthocyanins during 12 weeks of 25 °C storage.

    • Encapsulation is a promising technology aimed to protect easily degradable compounds and control the release of natural bioactive components. It serves as an effective means to mitigate the impact of light, temperature, acidity, alkalinity, and other factors on natural pigments, thereby ensuring their stability. The functional barrier was achieved by a matrix or polymeric system, with carbohydrates, cellulose, gum, lipids, and proteins as the main types of materials. Depending on their size, encapsulated particles are classified as microparticles/microcapsules (1−1,000 μm) and nanoparticles/nanocapsules (< 100 nm). The encapsulation efficiency depends on the capsule material and the encapsulation method. Multiple techniques can be used for encapsulation, including freeze drying, spray drying, extrusion, ionic gelation, and emulsification. Spraying drying is the most widely studied method and is shown to efficiently encapsulate pigments in combination with polysaccharides such as maltodextrins[40]. To increase the stability of lutein, Álvarez-Henao et al.[41] obtained micro-particles with spray-drying, using maltodextrin, Arabic gum, and a modified starch as the encapsulating agent. Under the storage of 20 °C, the highest retention rate of lutein was achieved by the formulation of Arabic gum : maltodextrin : modified starch (33.3% : 33.3% : 33.3%), where Arabic gum is the key substance to improve the encapsulation efficiency. In comparison, freeze-drying is considered more suitable for sensitive pigment encapsulation under lower temperatures, which can offer an efficiency of up to 95%[42]. Ionic gelation is a novel technique that is appropriate for various component types. In a recent study by Tekin et al.[43], alginate/calcium-chloride ionic gelation was carried out to encapsulate red beet concentrate. It was found that betacyanins were more stable than betaxanthins after 6 weeks of storage at room temperature, and 79.48% of the betalain was preserved under the optimum encapsulation parameters. In addition to avoiding degradation, nanocarriers are also employed to incorporate lipophilic pigments in aqueous systems to extend their applicability in food products. Peng et al.[44] fabricated the curcumin nanoparticles by pH-shift method and evaluated the performance of different kinds of coating biopolymers (sodium caseinate, whey protein isolate, soy protein isolate, and Arabic gum). All four biopolymers could enhance aqueous dispersions of curcumin nanoparticles and showed high loading capacity, with casein showing the highest (27%). Among them, the best pH and salt stability were achieved by Arabic gum coatings, whereas the best heat stability was offered by sodium caseinate and soy protein isolate.

      In summary, the stability of the extracted pigment can be improved through appropriate treatment, with the selection of a pretreatment method depending on the type of pigment. Combining different approaches, such as metal ions and stabilizing compounds, can be performed to achieve better effects. Enhanced heat/light/pH stability will allow natural pigments to be more effectively applied in food processing.

    • Natural pigments find application in various seafood sectors, including preservation, packaging, production, and processing (Fig. 3), which are detailed in upcoming sections. Freshness and safety are among the most demand-driven challenges of aquatic products[45].

      Figure 3. 

      Applications of natural pigments in preservation, packaging, production and processing of aquatic products.

    • Despite the delicacy and palatability resulting from high protein content and accessibility of high-water activity, seafood products are exceptionally perishable after death and thus necessitate treatment and cold storage to enhance their quality and shelf life. Lipid oxidation, protein degradation, and formation of amine products under the effect of microorganisms and enzymes begin immediately after aquatic species die, compromising commercial products' nutritional quality and flavor profile[46].

      Many bioactive compounds preserve fish fillets or shrimp by being retained as nanoemulsions, aqueous solutions, or powders. They are summarized in Table 1. Currently, lycopene, curcumin, and theaflavin are the most common pigments employed for storing aquatic products, with relatively higher acceptance in sensory evaluation. Curcumin and rosemary oil nano-emulsion produced by sonication techniques have a pronounced effect in protecting rainbow trout fillets from contamination by bacteria such as P. aeruginosa, E. coli, and S. typhimurium[47], reducing peroxide value and prolonged shelf life after the storage. Meral and co-workers[48] fabricated nisin and curcumin-loaded nanomaterials to improve the acceptability of the fish fillets during the cold storage period. They observed the limited total mesophilic aerobic count growth and extended storage time of up to 10 d with acceptable sensory attributes of the fish fillet. To suppress protein and lipid oxidation, theaflavins are made into an aqueous solution for pre-soaking treatment on yellow croaker (Pseudosciaena crocea) fillets for 5 d at room-temperature and 40 d of chilled storage[49]. In addition to inhibiting myofibrillar protein and lipid oxidation, the theaflavins solution positively impacts the texture and color stability of the fillet samples.

      Table 1.  Utilization of natural pigments in aquatic products.

      Characterization Source Concentration Food product Method Application condition Metrics E number Ref.
      Curcumin / 1 g/L Rainbow trout Nanoemulsion 4 °C storage Specific pathogenic microorganism inhibition; delaying total mesophilic bacteria growth E100 [47]
      Curcumin / 0.1 g/L Rainbow trout Nanomats 4 ± 1 °C storage Extending shelf life of coated fillets to 12 d;
      high antimicrobial activity
      [48]
      Theaflavins / 0.5 g/L Yellow croakers Solution immersion for 30 min 4 ± 1 °C storage Protein and lipid oxidation degree reduction; myofibrillar protein stability improvement NA [49]
      Lycopene Tomato 360 ppm Rainbow trout Solution immersion for 30 min 4 ± 1 °C storage Shelf life extension; maintaining sensory attributes; delaying lipid oxidation E160d [50]
      Carotenoids/
      flavonoids/ anthocyanins
      Potato / sweet potato / red beet 0.1% Rainbow trout Powder Ice storage Sensory and chemical quality improvement;
      low cost
      E160/ NA/ E163 [53]
      Flavonoids/ betalains Red beetroot 1 g/L (crude extract) Tilapia fish Dipping solution (5 min) 5 °C storage Antioxidant activity; reducing TBA; high safety NA/ E162 [54]
      Astaxanthin Algae / Rainbow trout Dipping solution (30 s) 4 ± 1 °C storage Delaying microbial growth and lipid oxidation; maintaining meat color NA [55]
      Proanthocyanidins Grape seed / Salmon Film with microcapsules 5 °C storage Antimicrobial effect; maintaining the luminosity value; extend shelf-life to 4−7 d NA [58]
      Carotenoid Shrimp and tomato by-product 0.1 g/100 mg protein / Film 22 °C Edible; antioxidant; high stability; low carotenoid degradation E160 [60]
      Curcumin / 0.4 mg/mL Grass carp Emulsion 4 °C storage Shelf-life extension by 6 d; lipid oxidation suppression; reducing microbial coruption E100 [62]
      Anthocyanins Sweet potato 4% Bighead carp Film 4 °C storage Color change respond to pH; real-time monitoring of freshness; stability E163 [65]
      Anthocyanins Echium amoenum 19 mg/L Shrimp Film 4 °C storage Visually-distinguishable color change; TVC and TVB-N change indication; high sensitivity [66]
      Anthocyanins Purple corncob 0.8% Shrimp Film 4 °C storage Antimicrobial and UV-blocking properties;
      pH-responsive colorimetric indicator; biodegradability
      [67]
      Phycocyanin and anthocyanin Ipomoea nil and red cabbage 1 g/L Grass carp Film 4 °C storage High sensitivity to ammonia; fish freshness indication; non-destructively tracing [68]
      Betalains Cactus pears 3% Shrimp Film 20 °C, 48 h Antioxidant and ammonia-sensitive properties;
      high water vapor barrier property
      E162 [69]
      Betalains Red pitaya peel 1% Shrimp Film 20 °C, 48 h UV–vis light and water vapor barrier ability; antioxidant and antimicrobial properties;
      freshness indication
      [70]
      Carotenoid Shrimp waste 10 ppm Fish sausage Powder Frozen storage Color and flavor improvement; quality enhancement E160 [73]
      Astaxanthin Shrimp waste 1% Minced tilapia Oil soluble astaxanthin 4 ± 1 °C storage Extending shelf-life up to 20 d; antimicrobial activity; coloring ability; reducing lipid peroxidation; NA [74]
      Curcumin / 400 nmol/g surimi Shrimp surimi Solution 4 °C storage Bacterial growth inhibition; delaying quality deterioration E100 [78]
      Curcumin / 1 mg/mL Surimi Nanoparticle −3 °C storage Oxidation resistance and relative release efficiency; microbial growth inhibition; shelf-life extension [79]
      Lutein/ anthocyanin / 0.25%, / 3D-printing surimi Powder 4 °C storage Fresh-keeping effect; bacterial growth inhibition; freshness monitoring E161b/ E163 [80]
      Lutein / 0.5% 3D-printing surimi Nanoparticle 4 °C storage Prolonged lutein release; gel quality improvement; antioxidant function; E161b [82]

      Similarly, lycopene solution is demonstrated to be very effective in stabilizing the freshness of trout fillets during refrigeration[50]. Following immersion in various concentrations of lycopene (w/v) solutions, the rainbow trout fillets exhibited reduced PV, TBA, and FFA values compared to the control group. Fillet samples with extra lycopene, especially higher levels, remained acceptable throughout the test, suggesting lycopene's efficiency in extending the trout fillets' shelf-life. Nirmal & Benjakul[51] used a catechin solution to treat Pacific white shrimp (Litopenaeus vannamei) before 10-d ice storage. The retarded growth of microorganisms, lower increases in total volatile base (TVB) content, and delayed formation of melanosis that was observed in the results indicate a promising melanosis inhibitor as well as an antimicrobial and an antioxidant in ice-stored shrimp.

      Extracts derived from the peels, roots, and seeds of fruits and vegetables, which are abundant in polyphenolic pigments, effectively preserve shrimp and fish while increasing the value of the by-products[52]. Icing with sweet potato, sugar beet, and red beet peel extract as a source of antioxidants was employed to store rainbow trout fillets[53]. These peel extracts extended the shelf life by 4 d. It provided positive features on sensory, chemical, and microbiological quality, which can be used as an alternative technology for food preservation. Similar outcomes were obtained from investigating tilapia fish fillet preservation using red beetroot peel extract[54]. During the cold storage of the rainbow trout fillets, extract from Haematococcus pluvialis (Hp) among different algae extracts showed the most evident effect in delaying microbial growth and lipid oxidation processes. More importantly, the Hp extract contributed to the appearance of trout fillets by preventing a* values (redness) from decreasing throughout refrigeration[55].

    • Packaging is an essential safeguard against environmental threats during the transportation and storage of processed aquatic products. Addressing sustainable development and the health hazards of plastic products to living organisms, the current research topic in food packaging is the development of biodegradable packaging[12]. By integrating active ingredients/intelligent compounds into packaging or directly onto the surface of aquatic products, protection that contributes to the assured quality or timely information regarding the quality is provided (Fig. 4a). For monitoring the freshness of food products, additional functional substances such as natural pigments are embedded in films[56] to both preserve the food and indicate quality change (Fig. 4b).

      Figure 4. 

      Natural pigments as active coating and intelligent colorimetric film for freshness indicator of aquatic products.

    • Aiming for food preservation, edible coatings are made as a thin layer that wraps the food directly by submersion or spraying[57]. The coatings are initially formulated using a biopolymer matrix, with the option of including functional ingredients, and the resulting food-grade suspensions are then applied in a liquid form onto the surface of the food product, followed by drying. In terms of fishery product preservation, the coated film's strong antimicrobial and antioxidant capabilities are key factors in extending the shelf life on the premise of high quality. Chitosan is mostly employed in edible films among various biopolymers due to its superior performance, which is prepared with grape seed extract to preserve salmon fish[58]. Grape seed extract contains abundant phycocyanin and anthocyanins, commonly employed as natural antioxidants to strengthen coatings. Zhao et al.[59] introduced vacuum impregnation to fish gelatin-based coating containing grape seed extract for chilled seabass fillets storage. This coating effectively postponed the microbial spoilage and discoloration of the seabass fillets and its ability to impede the water migration sustained the fillet's water-holding capacity.

      Furthermore, pigments derived from aquatic waste are employed for preservation. Lipid-extracted astaxanthin from shrimp has been utilized to produce edible membranes with antioxidant properties that remain stable during refrigeration. Compared to lycopene and beta-carotene, astaxanthin exhibited the lowest degradation rate of 17% following a one-month storage period[60]. Arancibia et al.[61] developed a coating solution containing chitosan and enriched shrimp waste extract concentration and applied it to shrimp preservation during cold storage. The antioxidant activity of the extract delayed microbial growth and the onset of melanosis, resulting in a desirable color and taste on the shrimp. Sun et al.[62] reported an edible coating prepared by fish gelatin enriched with curcumin/β-cyclodextrin, which exhibited considerable potential in preserving grass carp fillets at 4 °C. With the addition of curcumin, the oxidation degree, microbial spoilage, and color change were suppressed in the fish fillet during storage. The curcumin/β-cyclodextrin emulsion coating treatment extended the shelf life of grass carp fillets for 6 d.

    • Unlike active films that contain natural compounds with bioactivities and physicochemical properties, it is not necessary for intelligent packaging to release specific elements. Intelligent packaging consists of three types: indicators (integrity, freshness, time, and temperature), data carriers, and sensors (gas sensors, chemical sensors, etc.)[63]. One of the main parts of the intelligent packaging system, freshness indicators based on pH sensing have found fast growth in the aquatic food industry due to their affordability, adaptable production, and easy visual observation detection of color changes[64]. The pH-sensitive films function by the released volatile amines from food products, which leads to an elevation in the pH of the package headspace.

      Recently, anthocyanins, betalains, curcumin, and phycocyanin from plant extracts have been primarily used solely or compositely as natural pH indicators. These pigments are typically immobilized into a solid-based platform, the natural or synthetic polymers including cellulose nanofibers, starch-chitosan, starch-polyvinyl alcohol gelatin, and alginate. Combined anthocyanins with curcumin, Chen et al.[65] produced starch and glycerol-based composite film that exhibited durability for no less than 180 d, which non-destructively indicated the different degrees of bighead carp fillet at 4 °C. It was found that films containing a 2:8 ratio of curcumin to anthocyanins exhibited a higher degree of precision in responding to pH variations. The bacteria cellulose film containing Echium amoenum extracted anthocyanins was fabricated and used to monitor packaged shrimp's freshness[66]. Three distinguishable colors were observed as the shrimp aged: violet (fresh stage), gray (use soon stage), and yellow (spoiled stage), indicating the suitability of anthocyanins from E. amoenum for quality indication of protein-rich food. Normally regarded as an agricultural waste product, purple corncob is a suitable raw material for preparing pH-sensitive packaging. Pigments and lignin-containing cellulose nanocrystals endowed the packaging film with a reversible color response and strong mechanical properties, which were proven to act well as a freshness indicator of shrimp and meat products[67]. Tavakoli et al.[68] immobilized anthocyanins and phycocyanin into composite gelatin/soybean polysaccharide matrices and obtained a highly sensitive colorimetric film. An obvious correlation was observed between the label color and the fish's pH, TVB-N, and bacterial growth, which can be used to trace the spoilage of grass carp refrigerated at 4 °C. Smart film formed by combining betalains from Cactus pears (Opuntia ficus-indica) with quaternary ammonium chitosan/polyvinyl alcohol blends exhibit favorable water vapor barrier properties and tensile strength, which also changes color in response to volatile nitrogen compounds, indicating shrimp freshness[69]. By adding betalains-riched red pitaya (Hylocereus polyrhizus) peel extract into starch/polyvinyl alcohol film matrix, the water vapor barrier, UV barrier, mechanical properties, antioxidant, and antimicrobial properties of the film can be effectively enhanced. The film is also sensitive to ammonia and can be used as a freshness test for shrimp[70]. In summary, natural pigments derived from plants are predominantly employed in smart and active packaging applications to assess the freshness of aquatic products. This utilization stems from the ability of natural pigments to undergo color changes due to pH variations caused by the release of volatile ammonia compounds during the storage of aquatic products.

    • Surimi products like fish balls, fish sausages, fish tofu, and shrimp surimi are becoming daily food with increasing popularity worldwide due to their high nutrition and elastic texture. Nevertheless, their quality is constrained by protein oxidation, fat oxidation, and contamination with foodborne bacteria during refrigeration because of their high protein content and perishable nature[71]. Regarding frozen surimi, measures have been taken to improve the quality and gel strength and reduce oxidation during extended freezing by employing several additives like cryoprotectants[72]. However, as for the prepared surimi-based products (ready to cook) mostly sold in hot-pot restaurants, attractive colors and designed shapes are the key sensory attributes that increase consumer preference and acceptance. Surimi products, including simulated crab sticks, shrimp cakes, and fish sausages, are often orange or red-colored. Typically, the desired color of the surface is achieved by adding colorants like carmine, monascus, paprika, caramel, and lycopene (Fig. 5).

      Figure 5. 

      Natural pigment application in surimi products.

      Carotenoids recovered from shrimp waste had been applied to the fish sausage, which had a positive impact on the color and flavor of fish sausage[73]. A previous study demonstrated the use of edible oil extraction to recover astaxanthin from shrimp processing waste[74]. In application, the recovered astaxanthin improved the storage quality and stabilized the color of minced tilapia fish. Suryaningrum et al.[75] reported the good performance of beetroot pigment extracts in improving catfish surimi's gel quality and appearance. Moreover, curcumin among the pigments extracted from colored plants is proven to be most effective in increasing microbial resistance and augmenting the sensory properties of tilapia fish surimi[76]. More vulnerable to deterioration under frozen conditions, shrimp surimi requires refrigerated storage between 0 and 4 °C[77]. Curcumin-mediated sono/photodynamic demonstrated superior bactericidal activity in preserving shrimp surimi quality, which can be used as a reliable non-thermal sterilization method[78]. Regarding the limited solubility in water and the poor chemical stability of curcumin, encapsulation with chitosan nanoparticles was incorporated into its application, providing improved oxidation resistance and maintaining the nutrient content of surimi[79]. Natural pigments also provide additional opportunities for the creation of colorful and diverse shapes, as well as the improvement of the quality of ready-to-eat snacks that are based on surimi.

      The antibacterial and antioxidant properties of these pigments exhibited the potential to extend the shelf life and monitor the freshness of printed food[80]. Because of its homogenous and suitable fluid properties, surimi is suitable for 3D printing technology as the 'ink' matrix, generating customized functional foods for the elderly, patients, and children[81]. Lutein is a potent addition for inhibiting oxidation and an effective quality enhancer, providing surimi with better structure and shapes. The addition of 0.5% lutein combined with nano starch imparted a visually appealing red hue to Pennahia argentata surimi, delaying the decrease of L* and increase of a* and b* caused by the addition of lutein separately[82]. The charged group of lutein contains electrons that could interact with radicals to exert antioxidant properties. Thus, controlled release becomes imperative when lutein is engaged in processing or digesting. With nanoparticles, pigments with antioxidant activity are released better for longer-lasting functions[83]. Comparable to the functional film, anthocyanins exert the role of pH indicator in the shell of 3D-printing surimi for non-destructive quality monitoring, turning green and yellow gradually during refrigeration to indicate that the freshness is getting worse. For ease of understanding, the utilization of different natural pigments are listed in Table 1.

      In summary, numerous studies have demonstrated the preservation value of natural colors in seafood products such as fish fillets and fresh shrimp, which provides possibilities for the development of ready-to-eat seafood. Commodities such as ready-to-eat cooked fish fillets, dried shrimp, and scallops are very popular and possess good economic benefits in China. Natural colors have good potential for their application in color enhancement and quality retention. At the same time, fat-soluble colors can be combined with fish oil and other nutrients rich in polyunsaturated fatty acids to develop nutritionally enhanced high-end aquatic products. This combination attracts consumers seeking minimally processed and natural products and ensures the benefits of the aquatic industry as well. These pigments' multifunction and nontoxic nature confirms their ubiquitous application range in the aquatic industry as natural additives and preservatives.

    • Natural pigments are always more favored by consumers than synthetic ones when applied in the food industry, which can be exemplified by the inclination of people to take pigments (anthocyanin, etc.)-rich foods to attain health advantages. Their ability to counter oxidants also attracted intensified interest from food researchers to find more approaches to unlock their application potential. Among numerous food product categories, aquatic products have relatively higher economic and nutritional value but are particularly sensitive to spoilage. Nevertheless, the stability, cost, color range, and safety are still the main concerns in the scale-up from lab to commercial application:

      (1) Regarding stability, susceptibility to some common conditions limits their incorporation efficiency, and the resulting color change may also affect the meat texture. More studies are needed to understand the degradation, color retention degree of pigment, and impact on the food matrix during storage and processing. Including encapsulation, advanced techniques need to be used to control the release of pigments. To solve the problem of low thermal resistance of pigments used for coloring purposes, potential integration approaches involve optimizing the food processing methods and incorporating the pigments directly into the final product.

      (2) As food additives, natural pigments generally require higher costs for extraction and larger amounts compared to synthetic alternatives due to the complexity of their extraction process. Further improvements in extraction techniques, such as supercritical fluid extraction and enzymatic extraction, and more sustainable pigment sources are also required to enhance their competitiveness in the marketplace. It is practicable to employ pigments derived from microorganisms, algae, and microalgae to preserve aquatic products, meet sustainable development needs and mitigating the seasonal influence on plant resources. The future may see the development of cost-effective biotechnological processes, such as fermentation and genetic engineering, and large-scale cultivation techniques that could drastically reduce production costs and ensure a steady supply of high-quality pigments.

      (3) The limited availability of natural pigments has led to a constrained color options for food products. While current natural colors continue to be extensively employed and favored by numerous consumers, the incorporation of a broader range of colors presents a promising opportunity for expanding the utilization of natural pigments in aquatic products. The ideal approach involves the physical blending of established natural pigments to achieve the desired color of ready-to-eat seafood and the combination of fat-soluble colors with fish oil to develop nutritionally enhanced high-end aquatic products. These advancements could transform the food industry by providing more vibrant and stable natural coloring options, thus enhancing the visual appeal and perceived quality of food products while aligning with consumer preferences for natural ingredients. However, this necessitates optimal stability and a sufficient level of purity, both of which are closely associated with the extraction method employed for obtaining the natural pigment.

      (4) The utilization of natural colors in both edible and smart packaging necessitates adherence to food safety and regulatory standards. There will be a growing emphasis on conducting thorough safety assessments to identify and mitigate potential allergens or hazardous substances in natural pigments. As consumer demand for natural and safe food additives increases, regulatory frameworks will likely evolve to support and ensure the safe use of these pigments, including establishing clear guidelines and standards for their production, application, and labeling. Commercial application of smart packaging technology that integrates natural pigments could enhance consumer confidence and satisfaction.

      Overall, the integration of natural pigments into food products holds promising potential for transforming the food industry. Addressing these challenges, pigment applications emerge as a key facet in shaping the future of high-quality, visually appealing, and nutritionally rich aquatic offerings.

    • Aquatic products are highly susceptible to quality deterioration, which may lead to economic loss and health risks. The prospect of incorporating natural pigments in aquatic processing and storage is increasingly realized, which includes enhancing visual appeal and customer perception, maintaining the overall quality of aquatic products, prolonging their shelf life, and indicating freshness. These pigments' multifunction and nontoxic nature confirms their ubiquitous application range in the aquatic industry as natural additives and preservatives. With increased focus on transparency in food labeling, natural pigments will play a crucial role in providing recognizable ingredient lists and preservatives without harming the human body.

    • The authors confirm contribution to the paper as follows: conceptualization: Ding N, Tan Y; visualization: Ding N, Zhou Y; formal analysis, investigation: Zhou Y; writing – original draft: Ding N; writing – review & editing: Chang S, Feng R, Hong H, Luo Y; Tan Y; funding acquisition: Luo Y, Tan Y. All authors reviewed the results and approved the final version of the manuscript.

    • Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

      • This review was supported by the National Key R&D Program of China (2023YFE0122800) and the Earmarked Fund for China Agriculture Research System (CARS-45).

      • The authors declare that they have no conflict of interest.

      • Authors contributed equally: Ning Ding, Yongjie Zhou

      • Copyright: © 2024 by the author(s). Published by Maximum Academic Press on behalf of China Agricultural University, Zhejiang University and Shenyang Agricultural University. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
    Figure (5)  Table (1) References (83)
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    Ding N, Zhou Y, Dou P, Chang SKC, Feng R, et al. 2024. Colorful and nutritious abundance: potential of natural pigment application in aquatic products. Food Innovation and Advances 3(3): 232−243 doi: 10.48130/fia-0024-0023
    Ding N, Zhou Y, Dou P, Chang SKC, Feng R, et al. 2024. Colorful and nutritious abundance: potential of natural pigment application in aquatic products. Food Innovation and Advances 3(3): 232−243 doi: 10.48130/fia-0024-0023

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