Keywords

1 Introduction

As the world's population and economy continue to grow, so does the pressure on the oceans for food and services such as recreation, transportation and waste disposal. There is general consensus that the oceans are in crisis; examples include the increase in “dead” coastal areas [14], the collapse of important fisheries [29], the extensive damage that has affected diverse habitats and ecological communities, and the increasing losses of biodiversity associated with these areas [19]. Despite their remote location, Patagonian fjords and channels have been severely affected by numerous anthropogenic activities since the mid-nineteenth century [28], and in recent decades salmonid aquaculture has become one of the most important sources of anthropogenic pressure [2, 31, 35].

Aquaculture has been the fastest growing food production activity globally in recent years [21]. Most of this activity is concentrated in Asian countries, where extensive production of algae predominates, and secondarily of herbivorous and omnivorous fish and invertebrates such as carp and tilapia [11]. About one-third of aquaculture production occurs in marine environments [17], in contrast, in countries such as Chile intensive farming of marine and carnivorous organisms predominates, primarily salmonids. The footprint of salmonid production on the environment [30] is increased by a greater demand for energy and exogenous inputs (e.g. protein and oils) to the ecosystem of Patagonian fjords and channels where the fattening phase of this productive activity is carried out and where therefore the greatest biomass of its crops is concentrated.

2 Scope and Objectives

While aquaculture in the Patagonian fjords and channels has been experiencing sustained growth over the last four decades, we still do not fully understand the magnitude and intensity of its impacts. This chapter reviews and summarizes the main negative impacts of aquaculture in the Patagonian fjords and channels, organized in five sections: (i) an overview of the current development of aquaculture in Chilean Patagonia; (ii) an overview of the general environmental impacts; (iii) the magnitude of local impacts (in concession sites); (iv) the magnitude of regional impacts (impacts beyond concession boundaries); (v) aquaculture control and mitigation strategies under a scenario of global change. We provide four recommendations aimed at reducing the risks of severe impacts on the Patagonian fjords and channels in the context of climate change, highlighting the urgent need to prevent regional and ecosystem impacts on them.

3 Methods

The available scientific literature on the main negative impacts of aquaculture in Chilean Patagonia between Reloncaví Sound and the Diego Ramírez islands (41° 42′ S 73° 02′ W; 56° 29′ S 68° 44′ W) was reviewed. The authors’ experience in these topics, both in Patagonia and elsewhere in Chile, is added to this research. This work is based on studies carried out over the last 20 years, incorporating some recent publications on the subject.

4 The Impacts of Aquaculture in Patagonian Fjords and Channels

4.1 Aquaculture Development in Chile

More than 1,200,000 tons (t) of aquaculture products were harvested in Chile in 2017, generating revenues of over US$ 4.91 billion FOB (“Free on Board”), equivalent to 14.3% of the country's non-copper exports. Salmonids accounted for 880,000 t (US$ 4.63 billion) of this total; the vast majority was Atlantic salmon (Salmo salar) (Fig. 1). Salmon farming has grown almost uninterruptedly since 1978, positioning the country since 1991 as the world's second largest producer. However, there has been a certain slowdown in its growth rate, which averaged 5% per year between 2007 and 2017. In contrast, in the same period mussel aquaculture showed an average growth of 8.6%, reaching a harvest of 338,000 t of Mytilus chilensis mussel in 2017 (Fig. 1).

Fig. 1
A stacked bar graph of aquaculture production. It plots harvest versus year 1998 to 2017. The data is for Atlantic salmon, others salmonids, Chilean mussel, Pelillo, and others. The bar for 2014 is the highest with a high proportion of Atlantic Salmon.

Aquaculture production of Atlantic salmon, other salmonids, the blue mussel (Mytilus chilensis) the red seaweed pelillo (Gracilaria chilensis) and other species in Chile from 1998–2017 [16]. Although the figures represent production for the entire country, production outside the Patagonian fjord and channel system is marginal

Full size image

Unlike the salmon and mussel industries, and despite Law 20.925 which encourages its cultivation, alga aquaculture has had little development in Chile. The national harvest of pelillo, the only commercially cultivated seaweed in the country, has declined by an average of 7% per year during the last decade (Fig. 1). Although aquaculture production statistics suggest an incipient diversification process in the country, with small production of various marine fish such as corvina, turbot and yellow-tail amberjack, as well as oysters, abalones, and other species of bivalves and microalgae, it is evident that the productive focus continues to be on salmonids and mussels (Fig. 1).

All Chilean salmonid and mussel production has been developed in sheltered and semi-sheltered areas of the Patagonian fjord and channel system. There has been an evident process of territorial expansion of salmon farming from the Los Lagos Region (40°–43° 38′ S) to the south (Fig. 2), triggered by the serious sanitary and productive crisis in the sector derived from the appearance of the ISA virus toward the end of the 2000s [31]. Salmonid production in the Aysén Region (43° 38′– 49° S) has risen sharply, becoming the main production area in the country by 2015 ([37]; in Spanish Servicio Nacional de Pesca, SERNAPESCA). The Magallanes Region (49°–56° S) shows sustained growth in its contribution to national production starting in 2010, reaching a 13% share of the national harvest in 2017 [37].

Fig. 2
3 maps of Patagonia for evolution of the spatial distribution of authorized concessions of salmonids. Los Lagos and northwestern Aysen have highest densities of aquacultures.

Evolution of the spatial distribution of authorized aquaculture concessions of salmonids in the Patagonian fjord and channel system (1980–2019), according to the date of approval by the Undersecretariat of Fisheries and Aquaculture (SUBPESCA)

Full size image

4.2 Overview of the Environmental Impacts of Aquaculture in Chilean Patagonia

Most scientific, governmental and public concern about the environmental impacts of aquaculture in Chilean Patagonia has been focused on the salmon industry (Table 1). More than 1,150,000 t of artificial food are distributed annually among the more than 320 farming centers operating in the Patagonian fjords and channels (Fig. 2), using net pens open to the environment. This feed, based on fishmeal, fish oil and various vegetable products, generates 80,400 tons of solid waste (mainly feces and residues of uneaten food) that precipitate in the environment under the cages, producing evident local impacts on the seabed [41]. In addition to these wastes, a minimum of 23,900 t of ammonium and other metabolites are released directly into Patagonian ecosystems, whose capacity to assimilate such discharges remains unknown [4, 35]. Of growing concern is the escape of hundreds of thousands of salmon, which during the last two decades has averaged 487,000 individual year−1, with a recorded maximum of more than 1,700,000 individuals escaping in 2013 [38]. As discussed below, these escaped fish have the potential to prey on a very large fraction of the native fauna [31], and also to generate permanent feral populations, Chinook salmon have already invaded all of Patagonia's watersheds [12]. These escapes also lead to a flow of pathogens and parasites whose health consequences on native fauna are not well known [4]. The salmon industry uses several chemotherapeutics (e.g. antiparasitics, antibiotics, antifungal agents) whose environmental effects and risks on the human population have caused public alarm [10, 47].

Table 1 Main environmental impacts of salmon farming and associated research requirements. Modified and expanded from [35]
Full size table

The environmental aspects associated with blue mussel aquaculture have received less attention than those of salmon farming, both in terms of the regulatory framework, which is basically designed for the salmon industry, and in terms of scientific research and the perception of society, which views it as a smaller industry and therefore one with less environmental impact. Although its environmental effects have not been systematically studied in Chile, the available evidence indicates that these effects should be of lesser magnitude than those generated by the salmon industry [39]. This is due to the fact that mussel farming does not require artificial feed, thus avoiding problems derived from the incorporation of inorganic matter and exogenous nutrients into the ecosystem and limiting its direct impacts to the cultivation area itself. Notwithstanding this, mussel species channel and concentrate local organic matter, part of which is precipitated as feces and pseudofeces, organically enriching the sediments under the cultivation lines [27, 32]. Added to the above is the forced detachment of fouling organisms, an unregulated activity that also contributes to the accumulation of organic matter under cultivation systems [26]. In addition to increasing the sedimentation of organic matter in these culture sites and depending on both the scale of production and local circulation patterns, mussel farming can decrease the availability of phytoplankton for other filter feeders, including fish such as southern sardines, other bivalves, and zooplankton, affecting the rest of the marine food chain. These activities generally do not use chemicals or pharmaceuticals to control pathogens, which means lower levels of environmental impact. In terms of interaction with birds and mammals, there is concern about illegal hunting of seabirds such as the steamer duck (Tachyeres spp.) and physical obstruction of feeding and breeding areas for small cetaceans [24].

An aerial photograph of an ocean shore with an island.

The cultivation of algae generally has a lower environmental impact than other types of crops because it does not introduce elements exogenous to the system being exploited [11]. However, pelillo, the main agar-producing alga cultivated in Chile, has been observed to modify the substrate. This has complex repercussions, modifying the abundance of herbivores and predators and generating substrates for the settlement and recruitment of mussels and epiphytic algae (see Fig. 6 in [3]). Shellfish and salmon farming share the problem of incorporation of plastics into the marine environment and their deposition on the surrounding beaches [22]. Although there is little information available on the subject, the potential use of alga cultivation to recover part of the nitrogen, phosphorus, and dissolved inorganic carbon emissions from marine animal aquaculture will be described later in the chapter.

4.3 Magnitude of Local Aquaculture Impacts

An important portion of the environmental impact of aquaculture affects the immediate surroundings of the concessions of the production sites (0–100 m); we describe these as local impacts, while other impacts reach scales of tens of kilometers which we call regional impacts [50]. Among the local-scale impacts (Table 1), that is, in and near concessions (tens of meters), we found the accumulation of organic and chemical residues, where a significant increase in carbon, phosphorus and nitrogen was observed. This has led to a significant decrease in macroinvertebrate biodiversity, from average species richness values of 7.8 (with maxima above 20) to average values of 3.5 [41]. In addition to these changes in macroinfauna, there are biogeochemical changes in sediments [7], decreased bacterial diversity [23] and accumulation of heavy metals and drugs, such as copper and antibiotics, respectively [6].

In addition to organic matter, the immediate surroundings of the cage ponds show evidence of antibiotic residues in sediments and living organisms, which have been found up to 7 km from the nearest salmon farming center [6]. Added to this are the potential risks of massive and recurrent application of antiparasite dips for farmed salmonids [47]. While antibiotic residues can affect the structure and function of microbial communities and pose potential risks to human health, antiparasitics can affect different primary plankton consumers, including larvae of commercially important arthropod populations such as crabs and spider crabs [47]. The potential for the accumulation of antiparasitics along the trophic web has been demonstrated in other regions of the world [49]. All this points to the fact that the effects of chemical use at different stages of the salmonid production cycle can go beyond the local environment alone, but more scientific research is required to confirm this.

Local impacts are considered to be generally severe and relatively permanent; nevertheless, they are mainly confined to the ca. 275 km2 of aquaculture concessions in the Patagonian fjords and channels (as of December 2019). While this area represents a small fraction of the entire Patagonian system, the key question that remains unanswered is what specific sites are being impacted and what have been the additive effects of the suite of concessions on vulnerable habitats, species and communities such as cold-water coral reefs [25]. This is particularly relevant given the limited knowledge of the biological diversity of the exploited area and the limited number of marine protected areas (MPAs) within the Patagonian fjord and channel system. It is worth noting that in Chilean Patagonia there are 11 MPAs with coverage equivalent to 11,000 km2, representing 6% of the Patagonian coastal zone [44]. With the exception of the Kawésqar National Reserve, designated in 2019 for the protection of the inland waters of the former Alacalufes Forest Reserve, the protection of marine protected areas adjacent to existing terrestrial protected areas remains legally unclear and there are unresolved policy discussions [44].

4.4 Magnitude of the Regional Impacts of Aquaculture

Regional-scale impacts are those that have an effect several kilometers from the concession area. These impacts include nutrient enrichment, introduction of exotic and pathogenic species, fish escapes, garbage deposition and incidental death of seabirds and marine mammals (Table 1). It has been estimated that despite significant improvement in feed conversion rates, uneaten feed, fecal production and excretion of inorganic metabolites (e.g. ammonium) produce 35–78 t of nitrogen and 6–13 t of phosphorus per 1000 t of salmonids produced, which are disposed of in the environment [31]. More than 70% of this waste (28 t, Fig. 3) is released directly into the water column as ammonium and urea, becoming available for immediate use by primary producers [2, 34, 46], which can support algal growth in a radius of up to 1.0 km [1]. The remaining nitrogen and most of the phosphorus precipitate to the bottom, affecting the habitat and the biogeochemical cycles of the bottom sediment, and can be dissolved and/or suspended back into the water column and become available to primary producers. The production of 855,000 t of salmon (2017 harvest, Fig. 1) implies the discharge of at least 23,865 t of nitrogen in the form of ammonium into the Patagonian fjord and channel system (Table 2), an amount that exceeds by more than 140 times the 170 t of nitrogen that entered the Pacific Ocean from the controversial disposal of 5,000 t of salmon off the Chiloé coast in 2016 [8]. This comparison becomes even more relevant if one considers that aquaculture discharges occur within a mosaic of semi-closed oceanographic systems which present large differences in volume, circulation patterns and productive load, which means that dilution is not always sufficient to minimize their environmental consequences.

Fig. 3
A diagram of a fish for C, N, and P transport pathways. Feed leads to respiration, and production + mortality. Feed losses and feces production lead to resuspension of N, P, and C.

Salmon farm present in the Región de Los Lagos in southern Chil

Full size image
Table 2 Production value of the ammonium load (NH4) produced by salmonid farming in the three Patagonian salmonid-producing regions in Chile in 2017. Estimated values for production of 1000 tons according to Olsen and Olsen [33] (see Fig. 3)
Full size table

Despite the large variability between production areas and the high magnitude of nutrient inputs, inorganic nitrogen is rapidly diluted to undetectable levels, even in the vicinity of farming systems [46]. However, there is evidence that coastal eutrophication processes could occur in the vicinity of salmon farming sites, even without detectable increases in ammonium in the water column [5]. This evidence is related to the higher growth rates and nitrogen concentrations in macroalga tissues collected around salmon farming sites compared to non-salmon control sites [1, 46]. These effects would be expected to be greater in summer, when nitrogen limits primary productivity [1, 46]. Experimental evidence with experimental mesocosms suggests that effluent (water flowing in streams from aquaculture sites) from salmonids can increase the productivity of different phytoplankton species and reverse the abundance ratio of diatoms and dinoflagellates, causing the latter to predominate [4].

In summary, considering that in many production areas the salmon fattening centers are only three kilometers away from each other and that the mussel aquaculture centers that are located between them also contribute inorganic nitrogen, there may be a continuous enrichment that could trigger massive eutrophication phenomena and important changes in the abundance and/or specific composition of macroalgae and microalgae, as suggested by Buschmann et al. [4]. These aspects should be investigated with greater depth and speed, given the sustained growth of production levels and therefore their nutrient discharges.

Salmon escapes have a significant potential for predation on native fish and pelagic invertebrates. Given the current level of production, annual escapes of approximately 1.28 million individuals are predicted, which could consume approximately 15,700 t of invertebrates and native fish per year, including important forage species such as the channel prawn (Munida spp), silverside (Odontesthes regia) and the austral sardine (Sprattus fuegensis) [31]. Although the trophic and ecosystem impacts of feral and escaped salmonids on native fish and invertebrate populations have not been sufficiently studied [31], it is evident that the trophic impact of escaped salmonids affects not only their prey but also their counterparts, including other fish, and especially birds and marine mammals [31]. There is also a growing risk that, given the recurrent entry into the ecosystem of potentially reproductive escaped individuals, self-sustaining wild populations of farmed species may become established. This has already occurred with the Chinook salmon (Oncorhynchus tsawytscha), which has invaded all of Chilean Patagonia, and seems to be happening with the Coho salmon (Oncorhynchus kisutch) in Tierra del Fuego.

Farming facility interactions with marine mammals and seabirds are another area of growing concern [24, 36]. While avoiding consumption losses and/or damage to cages by sea lions Otaria flavescens, cormorants Phalacrocorax spp. and other species has become an important issue for the industry, there is growing concern about the levels of accidental death and/or illegal hunting of these animals on fish farms. Thus, it is of utmost importance to advance in the evaluation and systematic and mandatory monitoring of the levels of incidental mortality, the effectiveness of prevention measures and systems, and the implications of this mortality for the conservation of the affected species. In addition, the effects of the physical obstruction of breeding and feeding areas of small coastal cetaceans such as the Chilean dolphin (Cephalorhynchus eutropia) have not yet been evaluated [48].

Some additional aspects, thus far little addressed and quantified, are the discharge of inorganic waste (plastics) from the farm sites [22, 24], and the indirect effects of diseases and parasites partially transferred from farmed fish to wild organisms. It is necessary to address the interactions between productive systems such as salmon, mussels and algae that share the ecosystem, we do not know the complexities that may exist when they are co-cultured in the same body of water.

The manner and magnitude in which each of the environmental changes described above has affected ecologically relevant populations and communities in Chilean Patagonia remain poorly understood. Moreover, the complex interactions between the different sources of disturbance and the affected communities in the context of climate change are unknown [35].

4.5 Control and Mitigation Strategies Under Global Change Scenarios

The main axes of vulnerability to climate change in Patagonian ecosystems exploited by aquaculture are related to increased risks of harmful algal blooms, increased incidence of diseases associated with specific changes in temperature and salinity, and the multidimensional effects of the decrease in dissolved oxygen in the water [40]. The scientific literature has pointed out that as a consequence of temperature increases, ocean acidification and transient phenomena (e.g. heat waves) associated with climate change, the temperature tolerance responses and growth potential of various species used by aquaculture today will have a greater probability of having negative effects on aquaculture production in the future [17]. Changes in precipitation and sea and air temperature in Chile will affect freshwater inputs and the stratification, circulation and retention patterns of fjords and channels, with probably opposite directions in the Lagos and Aysén regions with respect to the Magallanes region [20]. There is insufficient information to predict how these changes will affect habitats, vulnerable species, and ecologically relevant processes such as primary production. However, it expected that the reduced fluvial input will reduce silica input to the fjord and channel system and thus affect diatom production and the associated trophic webs. This would negatively impact mussel aquaculture activities and significantly increase the risk of harmful dinoflagellate blooms. Detecting and responding in time to these and other changes requires immediate precautionary measures and a redesign of the coverage, frequency and characteristics of existing environmental and red tide monitoring programs in Chilean Patagonia. These monitoring programs should include marine protected areas.

Chile currently has an environmental regulatory framework for aquaculture that focuses almost exclusively on its local effects through the monitoring of existing environmental conditions under each concession [2], but ignores the cumulative, additive and/or synergistic effects that the collection of farms exerts on the region or ecosystem. Something similar occurs with environmental certification systems that are based on the promotion and certification of good practices in individual farms but neglect the regional or ecosystem problems. Thus, caution is warranted regarding the effectiveness of these certification systems in achieving global or regional conservation objectives, despite their growing importance for the salmon industry [45].

Considering the current regulatory limitations, the potential magnitude of aquaculture impacts on Patagonian ecosystems, the great uncertainty associated with their quantification and the possible aggravating effects of climate change, we consider it urgent to apply the precautionary principle and place an immediate limit on any increase in cultured biomass, nutrient discharges and areas used by salmonid and mussel aquaculture in Patagonia. The above measure should be maintained until the following conditions are met: carrying capacities (i.e. under scenarios of different levels of oxygen consumption or nutrient release) are understood and allow the establishment of objective limits for the environmentally acceptable biomass loads in the exploited ecosystems, identification and protection of the most vulnerable ecosystems including through marine protected areas; and a national monitoring system based on ecosystem indicators such as those proposed by Soto et al. [40] has been implemented which is capable of providing early warnings for the affected areas.

The proposed moratorium on the increase in the current levels of production and discharge of nutrients and chemicals should be immediate but progressively relaxed as the country develops a new regulatory system that limits the total load of cultivated biomass or the total discharge of nutrients permissible in each ecosystem, neighborhood or other management unit. All such measures are aimed at preventing unacceptable changes or risks at different scales of time and space and based on an adequate and sufficient knowledge of the relationships between the level of activity and the potential magnitude of the possible negative effects such as harmful algal blooms [35], hypoxia, escapes, incidental death of birds and mammals [31] and transmission of antibiotic resistance to human populations [9]. Under a regulatory scheme based on carrying capacity it would be possible to increase the permissible levels of productive load to the extent that there are effective technologies or measures to reduce and/or recover nutrient emissions and/or mitigate other impacts.

Mitigation measures have been proposed to reduce the vulnerability of currently exploited areas, redistribute production among areas or communities and develop a more diversified aquaculture matrix [40]. While this redistribution should not be understood as expansion to new areas, the diversification of the production matrix could be oriented to the mitigation of impacts through alga farming for nutrient recovery and oxygen production. This strategy has already been implemented in other countries such as China, where the cultivation of Gracilaria spp. has been demonstrated to improve water quality and decrease the quantity of nutrients and the production of phytoplankton, including species that cause harmful algal blooms [51]. It has been shown for more than two decades that it is possible to use algae such as pelillo (Gracilaria chilensis) and the seaweed huiro (Macrocystis pyrifera) to remove part of the nitrogenous inputs generated by salmon farming [7], and perhaps also have a positive effect on carbon sequestration [13, 18]. Cultivation of mussels and other filter feeders has also been proposed as an indirect way to remove nutrients of anthropogenic origin, although this option requires careful evaluation of costs and benefits, given the potential environmental effects of mussel aquaculture [42]. However, the great potential of integrated crops, the existence of legal restrictions on multispecies cultivation, the absence of regulations that oblige the industry to remove nitrogen discharged into the environment and the lack of economic incentives to move in this direction have kept this strategy merely theoretical. These co-cultivation systems could be even more relevant to maintain sustainable production under a scenario of ocean warming and acidification, as proposed by Strand et al. [43] and Fernández et al. [15].

5 Recommendations

Salmon farming has local and immediate environmental impacts, which affect biodiversity and sediments under production facilities [23, 41]. However, there are important larger spatial and temporal effects that have not been adequately quantified or addressed by current regulations (Table 1). Nor have the environmental effects of mussel and seaweed farming been quantified or addressed normatively. Under a precautionary approach, the partial and limited knowledge of the real and complex interactions of aquaculture on the coastal ecosystems of Chilean Patagonia is a great challenge that should not be a justification for inaction, especially given the rapid expansion of this activity and the threats of global change.

This chapter provides four priority recommendations to advance the conservation of Chilean Patagonia in relation to aquaculture activities:

  • Halt the current production levels of salmon farming until: (i) the overall capacity of this system to receive higher nutrient discharges has been evaluated; (ii) there are estimates of carrying capacity by productive area and (iii) there is an effective system for protecting the diversity of communities and species present in this system.

  • Some concrete and complementary actions to achieve this objective would be: (i) establish global or regional quotas for the production and/or discharge of nutrients (e.g. nitrogen); (ii) limit the use of products such as antibiotics and antimicrobials by defining annual quantities and developing new control mechanisms, including strategies to reduce potential health risks to local communities; and (iii) freeze the granting of new concessions for this purpose, particularly in the Magallanes Region.

  • Legislate and implement as soon as possible an environmental liability system that: (i) regulates and penalizes economically the environmental damage caused by salmon escapes, stimulates preventive measures and technologies and the effective recapture of the largest possible number of escaped salmon, either directly or through third parties; and (ii) internalizes the environmental costs of nutrient discharges and stimulates the development of mitigation measures such as integrated farming with algae and/or filter feeders.

  • Install a new biological, environmental, and productive monitoring system, with open databases that are transparent and validated by a panel of experts that allow the study, evaluation of changes, processes and impacts and the generation of early warning systems at the ecosystem level. This system can include the current environmental system, but it must go far beyond it for the concessions.

  • Promote research and development of technologies and productive strategies that reduce and mitigate the environmental impacts of aquaculture, considering the current and future challenges that adaptation to global change will demand.