The aquaculture industry as a global network of perturbation experiments

Aquaculture is a global industry that enriches the surrounding aquatic environment in nutrients, namely carbon, nitrogen, and phosphorus. Because these inputs are spatially and temporally defined, cage culture farms act as perturbation experiments for understanding the ecological impacts of nutrient enrichment on aquatic ecosystems. Individual farms form an existing, though underutilized, global network of experiments with established continuous monitoring of ecosystem impact metrics. This network covers both freshwater and marine environments and spans numerable environmental gradients. We propose that this global coverage provides an opportunity to better understand heterogenous aquatic ecosystem response to nutrient enrichment in the context of other current global changes. With increased data sharing efforts and interdisciplinary collaboration, this existing global network of perturbation experiments provides an opportunity to expand fundamental understanding of diverse ecosystem response to nutrient enrichment. The industrial production of finfish (e.g., salmon, tilapia, and carp) has well documented ecological consequences (Ottinger et al. 2016; Carballeira Braña et al. 2021). Negative impacts of the aquaculture industry include excessive nutrient loading (Islam 2005) and subsequent eutrophication, disease introduction (Kennedy et al. 2016), heavy metals pollution (Emenike et al. 2022), and the assimilation of escapee fish into wild populations (Toledo-Guedes et al. 2014). Despite ecological concerns, the aquaculture industry has continued to grow in recent decades (Naylor et al. 2021, FAO 2022), driven by increasing market demands and rapidly declining wild fisheries. The continued pursuit of a sustainable future for aquaculture is critical not only to meet global food demands, but also to support local economies and communities. Though by no means a silver bullet for solving systematic inequities, aquaculture can play a critical role in improving public health and well-being by increasing access to nutrition (Gephart et al. 2021), providing employment opportunities, especially for women (Gopal et al. 2020), and contributing to sustainable development overall (Subasinghe et al. 2009). In terms of the United Nation's Sustainable Development Goals (SDGs), truly sustainable aquaculture (i.e., continued production in farms that do not adversely alter the ecosystem they inhabit) is well suited to tackling several of the 17 goals, including Zero Hunger (SDG 2) (Stead 2019) and those related to economic opportunities, particularly zero poverty, and good jobs and economic growth (SDGs 1 and 8, respectively), as well as many of the targets and related indicators associated with the SDGs (Griffin et al. 2019). In addition to the above costs and benefits, we posit that global-scale aquaculture operations constitute an untapped research opportunity that goes beyond the study of environmental impacts of aquaculture and the development of more sustainable methods. We propose that aquaculture operations, in particular cage culture farms, act as perturbation experiments and are therefore well suited for fundamental research in ecology, biogeochemistry, limnology, and oceanography (among other fields). In the following sections we explore this "aquaculture as perturbation experiments" framework. We first identify the elements of cage culture farms that make them good candidates for replicable, global-scale perturbation experiment-based research. We then explore potential research opportunities enabled by the framework to advance our understanding of ecosystem and community ecology, global biogeochemical cycling, and carbon sequestration. "Aquaculture," in the broadest sense, refers to the captive rearing of over 600 different species (including mollusks, crustaceans, marine finfish, and freshwater finfish, Troell et al. 2014). However, global freshwater and marine finfish production is dominated by fewer than 30 species (FAO 2022), resulting in reduced heterogeneity in farming practices across globally diverse ecosystems. Industry best practices combined with commonly shared sustainability certification criteria mean that inputs and impacts are both defined and largely comparable across effected ecosystems. The relatively limited number of species and cultivation methods suggests that, with careful consideration, geographically disparate operations may be interpreted as experimental replicates. In cage culture farms, fish are raised in large floating enclosures within a larger body of water (Fig. 1). The water from the surrounding ecosystem interacts fully with the cages, rendering the treatment of effluent (i.e., organic matter in the form of uneaten feed pellets and fish waste) impossible. While potentially deleterious environmental impacts are associated with nearly all aquaculture production systems, cage culture systems are typically more problematic because of this inability to treat effluent. Whereas terrestrially sourced nutrients are transformed and retained as overland and subsurface flows interact with the watershed's landscape before encountering the riparian zone, uneaten feed pellets, and fish metabolic waste products (both fecal matter and gill excretion) enter pelagic ecosystems without these precursive biogeochemical transformations. This connectivity with the surrounding ecosystem makes cage culture farms excellent candidates for serving as perturbation experiments. Aquaculture is by no means unique in its introduction of anthropogenic materials to aquatic ecosystems. The unsustainable loading of eutrophying nutrients from agriculture, heavy metal contamination from mining, and microplastic pollution from industrial processes are hallmarks of other anthropogenic activities. However, cage culture aquaculture differs from many other anthropogenic disturbances in that inputs are explicitly quantified by the producer as well as spatially and temporally defined. Aquaculture introduced nutrients are quantified due to the profit margin fueled nature of the industry which necessitates the ratio of feed to biomass harvest be optimized, and therefore thoroughly recorded. This allows us to accurately quantify nutrient inputs using methods such as: (1) mass balance approaches (i.e., known elemental content and quantity of feed supplied to fish less elemental content and quantity of biomass harvested), (2) comparison of near cage conditions to reference (control) sites required by regulatory agencies or in instances where certification was sought from the onset of production, comparison to pre-production conditions, and (3) estimation of loading from known feed nutrient ratios combined with documented food conversion ratios. Defining spatial boundaries relative to parameters of interest can be characterized numerous ways such as by assessing changes in the water column or, more commonly, sediment characteristics (Christensen et al. 2000; Castine et al. 2009; Farmaki et al. 2014, among others). Temporal boundaries may be characterized by the regular intervals of introduced materials (i.e., feed supply and fish restocking rates) or changes in ecosystem characteristics compared to the duration of aquaculture perturbation (Feng et al. 2022). Aquaculture is a global industry with cage culture farms occupying marine, coastal, and inland waters across nearly all latitudes (Fig. 2). This global coverage means that perturbation experiments are occurring across physical and geochemical gradients (e.g., latitude, temperature, salinity, intensity of disturbance, and residence time). Furthermore, there is a legacy of common metadata across farms due to state regulations and sustainability certifications. The prevalence of such sustainability certifications (Osmundsen et al. 2020) as well as hybrid governance in aquaculture (i.e., regulations established by both state and third-party certifiers, Vince and Haward 2017) has resulted in a wealth of continuous monitoring data collected in waters surrounding individual farms. Dissolved oxygen, chlorophyll a (a proxy for algal abundance), and inorganic nutrients such as ammonium and nitrate are typically monitored to assess environmental impact. Therefore, the aquaculture industry not only acts as a global network of nutrient loading experiments, but is also coupled to existing, complimentary monitoring work, supplying a currently underutilized global dataset. Presently, no such collated public global dataset exists, with data being available largely at the scale of individual operations. Increased open data practices and support for data sharing platforms would facilitate the use of this global dataset. While this framework is advantageous in studying ecosystem perturbation across latitudes, it is currently limited in its equitable application across countries, with rates of certified farming practices being heavily skewed towards developed economies. For example, among the United Nation's list of Least Developed Countries only Uganda has an Aquaculture Stewardship Council (ASC) certified finfish farm. However, when considering emerging economies more broadly, this framework does indeed provide research opportunities in traditionally data-poor regions, with ASC certified finfish farms (as well as farms in the initial audit stage) operating in Mexico, Honduras, Indonesia, and Vietnam. Expanding the presented framework beyond finfish aquaculture to include shrimp production sites would further benefit ecological research in emerging economies given the presence of ASC certified shrimp farms in Bangladesh, Belize, Guatemala, Honduras, India, Indonesia, Mexico, Nicaragua, Nigeria, Sri Lanka, and Vietnam. Mechanisms of eutrophication as well as the eutrophying effects of aquaculture have been well documented (Gowen 1994; Smith and Schindler 2009, among others), even where top sustainability certifications have been achieved (Amundsen et al. 2019; Fadum and Hall 2022). Eutrophication is driven by the increased nutrient loading (carbon, phosphorus, nitrogen, and micronutrients) from mineralized constituents of organic matter (i.e., uneaten feed pellets and fecal matter) as well as N-rich gill excretion. Operations supporting year-round, multi-year production effectively act as a press experiment (rather than the alternative "pulse" method of nutrient enrichment experiments). This press experiment gradually applies both organic matter (OM) and nutrient loading stress which potentially drives an ecosystem closer to a regime shift. The causal relationship between increased nutrient availability and/or the alleviation of nutrient limitation and accelerated primary productivity has been well established. However, with the exception of large-scale experiments such as those done in the Experimental Lakes Area (Emmerton 2015), opportunities to assess such regime shift thresholds and the cascading effects of eutrophication in situ and at an ecosystem scale are rare. This is partially due to a paucity of eutrophic systems with continuous datasets, which span the years of nutrient additions. Furthermore, considering aquaculture as a global perturbation experiment provides a unique opportunity to understand the impacts and implications of ecosystem disturbance at a scale, which would be otherwise unfeasible (given the quantity of additions needed to achieve a given threshold) or environmentally irresponsible or unethical (such as induced eutrophication). The proposed "aquaculture as perturbation experiments" framework applies the concept of learning from ecosystem manipulation and broadens the scale at which we can pursue fundamental ecological questions. Below, we identify three research opportunities aimed at developing a deeper mechanistic understanding of ecosystem response to anthropogenic OM and nutrient loading stress more broadly. Aquaculture drives changes in microbial community composition (Verhoeven et al. 2016; Chen et al. 2022). The consequences of this change may be phenotypic and easily identifiable (i.e., changes in dominant phytoplankton species), while others may be more cryptic (i.e., altered ecosystem biogeochemistry). Microbial communities are shaped and altered by both quantitative and qualitative changes in nutrient availability, such as shifts in the dominant forms of OM (Foreman and Covert 2003; Fasching et al. 2020). As microbial communities are the engines of ecosystem biogeochemical cycling, understanding the emergent characteristics of microbiomes (and potential changes to these characteristics) offers key insights into the role that microbial communities play in shaping ecosystem form and function (Hall et al. 2018). OM enrichment can alter microbial community metabolic function (a key emergent property of microbiomes) by increasing electron donor availability. This may precipitate a shift in competing metabolic pathways, and may shift the autotroph : heterotroph ratio, and thus fundamental aspects of carbon cycling. The abundance of OM also impacts the competition between nitrate reduction pathways, denitrification and dissimilatory nitrate reduction to ammonium (DNRA). Under conditions of high OM availability, DNRA has been shown to be favored over denitrification (Jia et al. 2020), altering the ratio of loss to retention of reactive N in the surrounding ecosystem. High nutrient inputs often lead to increased biomass of phytoplankton, including the taxa that produce harmful algal blooms (HABs), both in marine and freshwater systems (Wurtsbaugh et al. 2019). As HAB taxa are often associated with high nutrient levels, aquaculture may stimulate HABs (Hallegraeff et al. 2021). In addition, warming may exacerbate the stimulatory effects of nutrients on HABs, as HAB species tend to have higher optimum temperatures for growth compared with other phytoplankton (Paerl and Huisman 2009, Litchman 2023). Thus, in a warming climate, ecosystems with significant nutrient contributions from aquaculture may be especially vulnerable to HABs. In turn, high prevalence of HABs may significantly impact entire food webs and biogeochemical cycling (Briland et al. 2020). Cage culture farms can thus provide a geographically distributed platform to study the role of nutrient enrichment and its interaction with other stressors, such as warming, in producing and maintaining HABs, and their consequences for food web structure and ecosystem functioning. Understanding the impact of OM on microbial communities is critical to understanding global biogeochemical cycling. One important component of microbially driven biogeochemistry in aquatic ecosystems is the production of greenhouse gases, namely nitrous oxide (N2O) and methane (CH4). Both N2O and CH4 are produced through anaerobic metabolisms. Sinking particulate OM creates anoxic microsites which support these anaerobic metabolisms in otherwise oxygenated water columns (Karl et al. 1984; Broman et al. 2021), thus shifting microbial metabolic function at an ecosystem scale. The shift between aerobic and anaerobic pathways, and inorganic molecular speciation with and without oxygen, fundamentally alters all biogeochemistry in the surrounding ecosystem. Therefore, elevated OM not only supplies an ecosystem with mineralizable nutrients, but also manipulates redox conditions at a microscale, thus supporting enhanced greenhouse gas production. Greenhouse gas emissions from aquaculture farms remain largely unknown. Current best estimates rely on studies of wastewater treatment plants, which are likely suitable proxies for pond production systems (MacLeod et al. 2020), but are ill-suited to estimating cage culture farm emissions, particularly in coastal and marine ecosystems. Other estimates of emissions may be more accurate but are regionally constrained (Xu et al. 2022). An increased global effort to document emissions from aquaculture operations would not only improve understanding of the industry's climate impact but would address the extent to which global ocean models should consider point sources of OM and nutrients (such as aquaculture activity), as global terrestrial models have accounted for agricultural land alterations. Furthermore, documenting emissions related to OM enrichment across varying gradients in aquatic ecosystems could improve estimates of global CH4 and N2O flux from aquatic ecosystems, regardless of OM source. While eutrophication has largely been regarded as a deleterious effect of the aquaculture industry, it also offers the opportunity to assess the potential role of ocean fertilization for carbon (C) sequestration and climate stabilization (Scott-Buechler and Greene 2019). Fertilization, or enhanced primary productivity, may increase the export of organic C to the deep ocean, removing it from the atmospheric reservoir for centuries or millennia (Volk and Hoffert 1984; Nowicki et al. 2022). With marine and coastal cage culture farms operating at a global scale, these farms are effectively fertilizing surrounding ocean ecosystems and could possibly be leveraged to better understand the role of ocean fertilization in sequestering C (Chisholm et al. 2001). Should enhanced C sequestration prove feasible, placing marine aquaculture farms with respect to dominant currents and physical mixing dynamics may be to the mutual benefit of both farm operators and climate stabilization efforts, mediating nutrient loading from farms (and thus allowing for higher production quotas) while simultaneously contributing to C sequestration efforts. Similarly, some lakes and reservoirs may serve as C sinks, with some seasonal and inter-annual variability (Knoll et al. 2013; Reed et al. 2018). While there is a high degree of heterogeneity across inland lentic system ecologies and morphologies which dictate the degree to which a body of water may serve as a C sink or source, it has been suggested that some tropical reservoirs (Sikar et al. 2009) as well as lakes with increasing nutrient loads (Anderson et al. 2020) may be important contributors to the continental C sink. By assessing C sink/source dynamics in lakes and reservoirs which support active aquaculture operations, a more complete understanding of inland aquatic C sequestration across different ecosystems, and temperature and trophic state gradients could be established. Interdisciplinary collaboration between the aquaculture industry, researchers studying the impacts of aquaculture, and scientists pursuing fundamental research in fields such as biogeochemistry and ecology will help to illuminate how anthropogenic disturbance interfaces with the varied and pressing impacts of global change. In addition to OM and nutrient loading, other inputs from aquaculture farms such as heavy metals which are introduced through antifouling agents and formulated feed (Emenike et al. 2022), microplastics from farming equipment (Chen et al. 2021), antibiotics (Pepi and Focardi 2021; Adenaya et al. 2023), pathogens (Ahne et al. 1989), and contaminants of emerging concern (Ahmad et al. 2022) could similarly be used to investigate other types of anthropogenic disturbance in aquatic ecosystems. In recommending such research, we acknowledge two simultaneous positions: that the aquaculture industry, even within highly accredited operations, is often unsustainable and that it provides a research opportunity. Aquaculture is an environmental sustainability challenge, a means of meeting sustainable development goals, and also a research platform. The proposed "aquaculture as perturbation experiments" framework has the potential to dramatically improve our understanding of OM and nutrient enrichment in aquatic ecosystems at the global scale. No original data were produced or analyzed in the presented work. This work was supported by the Simons Foundation (Award #993455, awarded to JMF) and the National Science Foundation (Awards #2120441, awarded to EKH, and #2124800 and #1754250, awarded to EL). None declared.