Abstract
By supporting the fishmeal industry, are we competing with marine predators? Should we be taking away food from marine predators to subsidize agriculture? If not for human consumption, should forage fish be left in the sea for predators? Are there more sustainable alternatives to fishmeal; can the fishing industry be part of developing these? These are all pressing questions being posed by marine scientists, particularly in the light of the increasing aquaculture industry and associated increasing demand in recent decades for fishmeal and oil to sustain cultured fish. We concisely summarize the global context of marine sourced fishmeal and then use the South African marine ecosystem as a working example. This article draws on research into the trophic role of forage fish in marine ecosystems and ponders whether a reduced demand for fishmeal, given increasing global pressures such as climate change, could benefit marine ecosystems, fisheries on predatory species, and vulnerable marine predators.
Introduction
Supply of fish for human consumption has more than doubled since 1995, peaking at 151.2 million tons in 2016, largely due to aquaculture (). World food fish aquaculture production had risen to around 80.4 million tons in 2016, reflecting the increased contribution of aquaculture to fish supply for human consumption from 7% in 1974 to 53% in 2016 (). It is important to note that around 64% of fishmeal and fish oil used to feed aquaculture species is obtained directly from fish (largely forage fish – ) that are captured specifically for this purpose, as opposed to by-products of fisheries (see Figure 1A). This has sparked intense discussion around direct versus indirect consumption (for land farming and aquaculture) of small pelagic fish (e.g., ; ). Close to 70% of farmed finfish production is dependent on artificial feeding rather than on the natural environment for sustenance (Food and Agriculture Organization [FAO], 2014; , chapter 12). This has food-web and socio-economic implications; for example removal of forage fish from the natural ecosystem to support farming/culturing of animals (marine and livestock) has implications for predatory fish relying on these fish as prey, and the fisheries that target these predatory fish. In fact, it has been estimated that 90% of the fish not directly used for human consumption is food-grade fish (). Nevertheless, economically, it has made sense to direct fish to the reduction fisheries in some cases (; ). The IFFO (the Marine Ingredients Organization)1 reported that in 2018, 73% and 75% of fish oil and fishmeal respectively went to supporting the aquaculture industry. modeled the local drivers of fishmeal and oil production and their markets, concluding that the industry cannot be viewed in isolation from the global interconnections and context in which it operates.
FIGURE 1
Thus, not only are forage fish important providers of fish as human food and feed for agri/aquaculture industries, they are also a major food source for fish predators [many of which themselves support valuable commercial fisheries – , ], marine birds and marine mammals, and directly or indirectly contribute to varied ecotourism industries. Further, they play important roles in regulating ocean carbon, and contribute to community wellbeing and culture (). Global economic value of forage fish (to include a wide array of contributions of forage fish to people and the ecosystem) was estimated to be 18.7 billion USD per annum, which is more than triple the direct catch value of these fish ().
With respect to sustaining ecosystem functioning, there is high variability in both direction and magnitude of change in biomass of predatory fish in response to changes in catch of forage fish, dependent on ecosystem, local predator-prey relationships, and the spatial and temporal scales examined (e.g., ; ). Seabirds and marine mammals often show biomass (and also foraging and breeding) responses closely reflecting forage fish availability (; ; ). Further, it is no simple matter to compare economic trade-offs between forage fish and their predators (; ), and a full socio-economic analysis is warranted at the local scale. Nevertheless, it is important to acknowledge that the conversation needs to extend beyond only considering the changes in predator biomass, and even beyond also considering economic and social (stakeholder – see ) trade-offs in forage fisheries versus conservation for the sake of their predators. The discussion also needs to include how forage fisheries impact ecosystem functioning and the state of marine ecosystems across the world (e.g., ).
This article draws on research into the trophic role of forage fish in marine ecosystems and explores whether a reduced demand for fishmeal may benefit marine ecosystems, fisheries on higher trophic level species, and vulnerable marine predators. We concisely summarize the global context of marine sourced fishmeal and then use the South African marine ecosystem as a working example from which to draw support for ideas currently being debated worldwide.
A Brief Overview of the Role of Small Pelagic Fish in Marine Ecosystems
Small pelagic fish have been described as “wasp-waist” species by virtue of their large abundances yet constrained species numbers, which act to channel energy both up and down marine food webs (). An extensive ecosystem modeling study showed that forage fisheries operating at the normal maximum sustainable yield levels can still have large, detrimental impacts on marine ecosystems, largely related to the notable biomasses of forage fish, as well as the strong linkages between these species and their predators and prey (). Homing in on seabirds, a global comparative study based on observational data showed a significant decline in the breeding success of seabirds across multiple marine ecosystems when their prey bases dropped to below one third of maximum abundance levels (). Furthermore, a recent study drawing on data from the same ecosystems suggests that forage fish should be carefully managed so as to remain at levels above 18% of maximum abundance levels, since predation mortality inflicted on forage fish by seabird predators significantly increases below this fish abundance level (). The need for conservative management measures at low stock levels may be even more crucial as we suffer the effects of climate change. Given the pivotal role of small pelagic fish in upwelling ecosystems such as the Northern and Southern Benguela systems, for example, the well-being of forage fish stocks and their reliant fisheries may be further exacerbated by the added effects of climate change acting on these low trophic level species (). This is a wide-ranging, global concern; in its global biodiversity assessment, the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) specifically noted that climate change is a direct driver that is increasingly exacerbating the impact of other drivers (exploitation, land/sea use change, pollution, and invasive species) on nature and human well-being (, ).
Several marine species inhabiting South African waters, and relying on forage fish as prey, are either charismatic and important for ecotourism, commercially valuable and/or are species of conservation concern, including three endemic species of endangered seabirds (African penguin Spheniscus demersus, Cape gannet Morus capensis, and Cape Cormorant Phalacrocorax capensis), great white shark Carcharodon carcharias, Bryde’s whale Balaenoptera edeni, common dolphin Delphinus delphis, dusky dolphin Lagenorhynchus obscurus, and Cape fur seal Arctocephalus pusillus. Sardine Sardinops sagax and anchovy Engraulis encrasicolus comprise notable portions of the diet of many top predators off South Africa: African penguin – 79%, Cape gannet – 58%, Cape Cormorant – 98%, and snoek Thyrsites atun - 46%, Cape hake Merluccius capensis and M. paradoxus – 10 to 40% depending on hake size class considered, yellowtail Seriola lalandei - 30%, geelbek Atractoscion aequidens - 20%, Bryde’s Whale - 82%, cetaceans in general – 37%, and Cape fur seal - 30% (). Economically valuable predatory fish include geelbek and yellowtail, both especially caught in the line fishery, and both heavily dependent on availability of anchovy and sardine prey. Functional relationships have been demonstrated for geelbek and sardine, and also for yellowtail and anchovy (). Time-dynamic trophic model simulation incorporating altered anchovy availability between 1978 and 2015 supports the latter finding in particular (). Further, have undertaken Principal Component analyses of the diet and life history parameters of the three South African seabirds heavily reliant on sardine and anchovy prey, deriving a Forage Availability Index to provide thresholds required to maintain numbers of Cape gannet and Cape cormorant, and survival of adult penguins.
A Brief Overview of the Fishmeal Industry, Potential Fishmeal Alternatives, and Possible Industry Response
Fishmeal and oil serve the following markets: aquaculture (feed), land animal farming (feed), pharmaceuticals (human consumption), and fish oil capsules (human consumption) (). Currently, fishmeal is largely composed of whole fish, with just 25–33% comprised of fishery by-products or unwanted discards, although this fraction is likely to increase in the future ()2. In the 1960s, fish oil was mostly used in margarine and shortenings whereas by 2010, over 70% of fish oil production was directed to aquatic feeds, although the demand for fish oil for direct human consumption (nutrition and pharmaceutical uses) may increase ().
The growing aquaculture industry may be placing unsustainable demands on the fishmeal (and oil) industry (e.g., ). It may be viewed as encouraging that there has been a change in use of some fish species like Atlantic herring, away from fishmeal and oil to direct human consumption (). discuss the complex factors driving the global use of forage fish catches for fishmeal/oil versus for human consumption, and show a clear increasing trend in forage fish being consumed by humans in the period 1987–2007. However, although the proportion of global fish production that is used by humans for purposes excluding food has steadily declined from 30% in the 1990s () to around 12% in 2016, it still lies at around 20 million tons per year, most of which is comprised of fishmeal and oil (). Perhaps on a positive note, the IFFO report that supply of fishmeal and oil has not increased despite the increasing demand. This is largely a result of the decline in catches of fish that are usually destined for the reduction fishery (particularly in Peru and Chile ()).
In addition to weighing up the direct versus indirect uses of forage fish and the pressures imposed on forage fish stocks by the growing aquaculture industry (Figure 1A), aquaculture operations have a range of environmental impacts that need to be taken into consideration (, chapter 12). Marine aquaculture, for example, is noted for reducing coastal esthetics, depositing effluent including medicines and pollutants into the ocean, propagating disease, and genetic alterations from farmed to wild stocks, amongst other impacts (see e.g., for a review of environmental impacts and their regulation in marine aquaculture operations in Europe). However, mariculture if appropriately managed, can enhance provisioning and regulating as well as protect cultural ecosystem services and can even have positive effects on marine habitat and coastal ecosystems ().
Given the increased demand for fishmeal and oil, alternative sources of protein for aquafeeds are being sourced and the sustainability of forage fish stocks will be influenced by this (e.g., ; ; ). Alternatives include byproducts from the squid (), poultry and cattle industry, but most notably plant oils and seeds, especially soya bean-based feeds. This trend is reflected in the fishmeal:soybean price ratio, which despite large fluctuations, has increased linearly since 1993 (; Figure 2). Much research is going into plant-based substitutes in aquafeeds to meet the challenges of supplying a nutritionally balanced and suitable feed for aquaculture purposes (e.g., ). However, simulations suggest that by 2050, crop and land use required to sustain increased aquaculture to account for up to a third of food security for the World’s increasing population will be lower than if terrestrial farming supplies these needs (). Nevertheless, there are recognized environmental trade-offs including deforestation arising from soy-based industries () if we are to rely more heavily on land-based, plant-based substitutes, such that alternative ingredients like microbes and algae may be more promising prospects (). In recent years, insect larvae are being explored as a suitable alternative protein source (; ). Pacific White shrimp fed a diet comprising a substantial proportion of Insect-based protein as opposed to fishmeal-based feed showed higher growth rates and improved immunity (). Alternative ingredients to fishmeal and oil, and fuller utilization of fish byproducts in meal production, have reduced the global contribution to feeds for aquatic farming since the 1990s (). This is captured by various methods of estimating the “Fish-in:Fish-out” ratio, which generally suggest that globally, most fish-producing aquaculture industries are now largely net producers of fish rather than net users (). Nevertheless, the importance of considering nutrient ratios, ratios of protein, and energy content between fish directed to feed versus fish grown on that feed, could help improve the efficiency and ethics of the world’s aquaculture industry ().
FIGURE 2
Apart from sourcing alternative protein sources for feeds, how else could the move away from our dependence on forage fish be influenced? One mechanism that can be used to encourage sustainable use of forage resources is through environmental and social governance (ESG) criteria. ESG criteria are an increasingly popular way for investors to evaluate companies in which they might want to invest (
In South Africa, anchovy is a reduction fishery i.e., all anchovy caught is used for fishmeal and oil, not for direct human consumption, whereas sardine is channeled for direct human consumption (see Figure 1B). Further, over 90% of this fishmeal/oil is exported (SAPFIA)3, thus the fishery is driven by global supply-demand dynamics (currently demand exceeds supply). By comparison, only 12% of the sardine processed and canned in South Africa is exported, and this is mainly to SADC countries (South African Pelagic Fishing Industry Association (SAPFIA) website)3. To provide an estimate of value of this fishery, a 2020 report compiled by the small pelagics fishing industry (
As mentioned earlier, forage fish are crucial for a number of marine species. If one considers criteria for investing in a fishing company engaged in fishing for forage fish, environmental criteria might include indicators that give clear information as to how ecosystem considerations are dealt with in the management of the fishery and criteria on managing top predator conflict, etc. For the Oceana Group4, one of the top seafood companies in the world, five sustainability focus areas have been developed with admirable targets set for each. However, while an acknowledgment is made of bird mortality being reduced from their lines and that 91% of their catch by volume is on the South African Sustainable Seafood Initiative green list (
Putting the Picture Together
Fish or Feed? – The South African Case
In South Africa, sardine are canned for human consumption, processed for pet consumption or used as bait. Anchovy and redeye round herring Etrumeus whiteheadi are largely reduced to fishmeal and oil.
Although no definitive results are available yet, it is encouraging that collaborative research between social scientists, food technologists and industry is on the cards in South Africa to explore possibilities for products that would make use of anchovy or redeye for human consumption, as well as possible alternative sardine products that would make use of the whole fish rather than fillets, the latter aimed at the lower end of the consumer market (Prof Mafa Hara, University of the Western Cape, pers. comm.). Furthermore,
To Increase or Decrease Fishing on Small Pelagics?
A question worth pursuing here may be whether it would be economically advantageous to leave forage fish in the water so that fisheries based on predator species could potentially benefit from larger catches? Alternatively, in some cases where piscivorous fish are heavily fished, fishing simultaneously on forage fish can be beneficial, in contrast to the situation where more lightly fished piscivorous stocks fair better under low levels of fishing on forage fish stocks (
The South African small pelagics fishery contributes the largest catches (and second largest commercial value) of any South African fishing sector and provides full time employment to over 5000 people, excluding seasonal workers (
The Added Complexity of Climate Change
The impact of climate change on small pelagic fisheries has been highlighted in a recent publication by
In addition to the impacts of climate change on small pelagic fish, the regionally specific implications of climate change on aquaculture itself also needs serious consideration with respect to vulnerability and adaptation of the industry in its endeavors to address the increasing global food demand (
Weighing Up the Discussion
By supporting the fishmeal industry, are we competing with marine predators? The reliance by marine predators on forage fish has been demonstrated, as too has the dominance of reliance on forage fish to support the fishmeal industry. The question remains as to whether we should be taking away food from marine predators (fished and non-fished predators) to subsidize agriculture/aquaculture, or whether there are potential sustainable alternatives to ensure more balanced mutual benefits for humans and ecosystems. The recent report on “A Sustainable Ocean Economy in 2030” (
Given the ecological and socio-economic intricacies and feedbacks, it may well turn out that further unpacking of this complicated and sensitive conundrum reverts to an ethical debate. Notwithstanding, as curators of the ocean and its marine resources, we will be forced to start tackling these kinds of complex questions head-on. Addressing issues of social justice and social responsibility together with environmental/ecological responsibility is increasingly being recognized as a necessity in marine conservation and fisheries (
In summary, we propose that curbing any increase in forage fisheries, whether for direct or indirect human consumption, may address the multiplicity of factors that are currently at play in small pelagic fisheries and their management, including addressing their impact on vulnerable marine top predators reliant on forage fish. However, we acknowledge that on the local scale, productivity regimes related to climate change may facilitate expansion of low trophic level fisheries, depending on how the higher trophic levels are fished and/or managed. We propose that investors pay careful attention to the environmental and social governance (ESG) criteria against which they evaluate the fishing companies in which they invest, thereby encouraging industry contributions to ecosystem based fisheries management. We also propose that industry plays a more active role in facilitating the use of alternatives to forage fish in fishmeal, partnering with companies that are using alternative forms of protein production. We applaud environmentally beneficial initiatives such as the Cape Town based companies Inseco and AgriProtein; food waste that would normally end on landfills is used to farm black soldier flies Hermetia illucens, and the fly larvae (maggots) are harvested and ground into a high protein meal palatable to pets, fish and chickens5,6. All in all, it is our opinion that the argument condenses into an ethical one. Given the urgent need for poverty alleviation through creation of jobs and affordable food products for vulnerable human communities, we advocate for direction of a greater proportion of forage fish catches to direct human consumption while ensuring marine ecosystem functioning and sustainability, with more specific ESG investment criteria being developed to address this, and we encourage bio-recycling as a sustainable alternative to fish-based feed.
Statements
Data availability statement
The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author.
Author contributions
LS conceptualized and wrote the manuscript. LW was active in discussions of the article ideas and developing of the article outline, and contributed to the text and literature. Both authors contributed to the article and approved the submitted version.
Funding
This work was undertaken with funding from United Kingdom Research and Innovation (UKRI) Global Challenges Research Fund (GCRF) One Ocean Hub (Grant Ref: NE/S008950/1), the European Union’s Horizon 2020 Research and Innovation Program under Grant Agreement No. 8862428 (Mission Atlantic) administered through the South African Research Chair Initiative at the University of Cape Town, and the Leiden Conservation Fellowship administered through SANCOBB.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Footnotes
3.^https://sapfia.org.za/facts-figures/
4.^https://oceana.co.za/about-oceana/our-company/
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Summary
Keywords
fishmeal, ecosystem, forage fish, South Africa, anchovy
Citation
Shannon L and Waller L (2021) A Cursory Look at the Fishmeal/Oil Industry From an Ecosystem Perspective. Front. Ecol. Evol. 9:645023. doi: 10.3389/fevo.2021.645023
Received
22 December 2020
Accepted
31 March 2021
Published
22 April 2021
Volume
9 - 2021
Edited by
Sebastian Villasante, University of Santiago de Compostela, Spain
Reviewed by
Konstantinos Tsagarakis, Hellenic Centre for Marine Research (HCMR), Greece; Laura Koehn, National Marine Fisheries Service (NOAA), United States; Marta Albo-Puigserver, University of Algarve, Portugal
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Copyright
© 2021 Shannon and Waller.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Lynne Shannon, lynne.shannon@uct.ac.za
This article was submitted to Conservation and Restoration Ecology, a section of the journal Frontiers in Ecology and Evolution
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