© 2006 International Council for the Exploration of the Sea
A review of the impacts of salmonid farming on marine coastal ecosystems in the southeast Pacific
a i-mar, Universidad de Los Lagos Casilla 556, Puerto Montt, Chile
b Departamento de Acuicultura y Recursos Acuáticos, Universidad de Los Lagos Casilla 933, Osorno, Chile
c Departamento de Ciencias Básicas, Universidad de Los Lagos Casilla 933, Osorno, Chile
d Instituto de Investigaciones Oceanológicas, Facultad de Recursos del Mar, Universidad de Antofagasta Casilla 170, Antofagasta, Chile
*Correspondence to A. H. Buschmann: tel: +56 65 322429; fax: +56 65 322418. e-mail: abuschma{at}ulagos.cl.
The production of farmed salmonids in Chile reached 550 000 t in 2004. The industry is considered to be consolidated, but with potential for further expansion to the south into pristine coastal areas. The environmental impacts of the salmonid farming industry in Chile were reviewed in 1996, and evidence at that time did not suggest significant adverse effects. However, after almost ten years of sustained growth, current evidence indicates that significant loss of benthic biodiversity and localized changes in the physico-chemical properties of sediments have occurred in areas with salmonid farms. Furthermore, the presence of these farms significantly increases in pulses the density of dinoflagellates. Data suggest that escaped farmed fish may have an impact on native species, although their survival in the wild appears low. The abundance of omnivorous diving and carrion-feeding marine birds increased from twofold to fivefold in areas with salmon farms compared with control areas without them. It is urgent that an ecosystem approach be implemented to assess all impacts of salmonid farming on coastal ecosystems in southern Chile.
Keywords: biodiversity, Chile, environmental effects, fish escapees, nutrient loads, salmon culture
Received 17 September 2005; accepted 17 April 2006.
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Introduction |
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 Top Introduction Developments in salmon farming...Impacts of salmonid farming...ConclusionsReferences |
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During the past ten years, salmonid aquaculture has become the fourth largest economic activity in Chile after mining, forestry, and fruit production. Gross production in 2004 was 550 000 t, and the three most important farmed salmonids are Atlantic salmon, Salmo salar, coho salmon, Oncorhynchus kisutch, and rainbow trout, O. mykiss (Figure 1). Farming of Atlantic salmon is the main aquaculture activity in Chile, accounting for 92.5% of all exported aquaculture biomass and 94.9% of the total export revenue derived from aquaculture products. The location of the salmon farming industry in Chile is shown in Figure 2. Concern has been expressed about the environmental impacts of salmon farming in Chile and worldwide. These impacts include modification of benthic communities, increased nutrient loads in coastal waters and the associated problem of harmful algal blooms, increased harvests of wild fish populations for the production of fish feed, use of different types of chemicals, and escapes of farmed salmon into the wild (e.g. Gowen and Bradbury, 1987; Hallaegraeff, 1993; Folke et al., 1998; Naylor et al., 2000; Goldburg and Naylor, 2005). Currently, the environmental effects of intensive salmonid cultivation in Chile are little understood (Castilla et al., 2006), and consequently, industry regulation has been criticized for failing to implement an integrated ecosystem approach to environmental conservation.
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In 1996, a review of the environmental effects of salmon farming in Chile concluded that the industry did not have a significant environmental impact (Buschmann et al., 1996). However, the industry has expanded considerably during the past ten years and is now considered to be economically and technologically consolidated. The industry may expand farther into pristine southern environments of high conservation value. This paper summarizes recent research on the most important environmental effects of salmon farming in Chile, based on published and unpublished information, and makes suggestions for the sustainable management of intensive salmon farming in the southeast Pacific.
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Developments in salmon farming in Chile |
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TopIntroductionDevelopments in salmon farming...Impacts of salmonid farming...ConclusionsReferences |
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Commercial salmon farming began in Chile with the importation of eggs from the northern hemisphere. In recent years, the use of innovative technologies, particularly for Atlantic salmon culture, e.g. photoperiod and temperature manipulation, has permitted the transfer of fish to sea at different times of the year and harvesting throughout the year, reducing the need to import ova and, consequently, reducing the risk of introducing exotic parasites and diseases. Other positive developments include improvements in feed quality and conversion rates (ca. 1.2). Notwithstanding these improvements, several environmental issues remain unstudied or unregulated, resulting in pressure on producers and the government from environmental groups (Buschmann et al., in press).
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Impacts of salmonid farming on the Chilean coastal environment |
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TopIntroductionDevelopments in salmon farming...Impacts of salmonid farming...ConclusionsReferences |
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Research conducted since 1996 suggests that there have been localized adverse impacts on the seabed in the licensed farming areas associated with physico-chemical changes to sediments and significant losses of benthic biodiversity (Buschmann, 2002; Soto and Norambuena, 2004). Research at eight salmon farm sites located along 300 km of coastline demonstrated that the benthic biodiversity was reduced by at least 50% on average in the licensed salmon farming areas in southern Chile. This loss of biodiversity appears related not only to organic matter loading and low oxygen levels in the sediments (Soto and Norambuena, 2004), but also to the deposition of copper (Buschmann, 2002). Recently, the channels and fjords of southern Chile have been shown to possess a unique benthic fauna comprising endemic cold-water corals, anemones, and other species (e.g. Försterra et al., 2005). Interest in protecting these ecosystems has increased, and a network of conservation areas has been proposed (Castilla, 1996).
The Chilean regulations require that any farm causing the formation of anoxic sediments must reduce its production by 33% and, if the sediments have not recovered after one year, production must be reduced by a further 33%. Thereafter, if the level of oxygen in the sediments does not recover, the farm must close. However, benthic wastes have high levels of phosphorus (Soto and Norambuena, 2004), and it is not known how long these accumulations can persist and remain a source of nutrients in Chilean waters.
The occurrence of harmful algal blooms resulting from the input into coastal waters of nitrogen from salmonid farms is another major topic of concern in Chile. Harmful algal blooms have been recorded in Chile during the past three decades and have affected human health and natural and cultured marine resources (Table 1). The first instances to affect human health were reported in 1970 and 1972, and involved the species Dinophysis acuta and Alexandrium catenella; in 1993, diatoms of the genus Pseudo-nitzschia were implicated in a harmful algal bloom. These algae are sources of diarrhoetic, paralytic, and amnesic shellfish poisons, respectively. A. catenella blooms have affected Chile's austral region (42°S–52°S), whereas D. acuta and Pseudo-nitzschia have resulted in blooms in various enclosed coastal areas (Table 1). The algal species that have affected marine resources include Dinophyceae (Prorocentrum micans, Gymnodinium cf. cloroforum, and Gymnodinium spp.); Bacillariophyceae (Leptocylindrus minimus, Chaetoceros convulutus, and Chatonella sp.); Raphydophyceae (Heterosigma akashiwo); and Chrysophyceae (Dictyocha speculum) (Table 1). These blooms have mainly affected the channels and fjords of the Chiloé region (41°S–43°S), causing behavioural changes and mortality in wild and cultured aquatic resources. Although the number of these harmful species appears to have declined in Chile, reports of new harmful species and bloom events have increased in the past three decades; the impacts of species in Chile that are recognized as being harmful in other parts of the world (Table 1) must be given careful consideration.
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In most locations, there have been no detectable increases in nitrogen concentration in the water column near salmon farms (Soto and Norambuena, 2004). However, in an intensively farmed channel in southern Chile (Calbuco), significantly higher concentrations of ammonium nitrogen were detected near the cages, compared with control areas without fish pens (Figure 3). Seaweeds were shown to exhibit faster growth rates and higher nitrogen content in their tissues when cultured near fish farm cages (Figure 4), suggesting higher nitrogen availability as a result of the presence of the farms (Troell et al., 1997). In an experiment to assess the effect of salmon farms on phytoplankton communities, 1500-l tanks, filled with either effluent from salmon farms (see Buschmann et al., 1994, for details of the experimental protocol) or with seawater pumped directly from the sea, were used to culture dinoflagellates. The results indicated that the density of dinoflagellates increased significantly (p < 0.05) when reared in fish farm effluent, while diatoms tended to disappear (Figure 5). In addition, a study using the "beyond BACI" (Before-After-Control-Impact) methodology (Underwood, 1994) suggested that salmon farms enhanced dinoflagellate abundance for short periods (Figure 6). An analysis of variance showed that no persistent effect could be detected on dinoflagellate abundance because the ratios of F-values T(Aft) x I/T(Bef) x I = 38.61 (Table 2) and T(Aft) x I/T(Aft) x C = 48.28 (Table 2) are both significant (p
0.05), whereas T(Aft) x C/T(Bef) x C = 0.24 (p 
0.05) is not significant. These results indicate that the presence of salmon farms led to a significant increase in the abundance of dinoflagellates in short-term pulses and suggest that, to detect any increases in abundance of phytoplankton associated with them, it is necessary to implement an appropriate sampling protocol that facilitates detection of these pulses.
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The use of various chemical compounds in salmonid farming has also raised public concern in Chile, particularly following the detection of some compounds at high levels in other countries (Easton et al., 2002; Hites et al., 2004; Foran et al., 2005). In this context, initiatives between the government and private companies in Chile have been set in motion. The effects of antibiotics on the microbial flora have received little attention, although resistance to antibiotics is a problem for the salmon farming industry, e.g. Miranda and Zemelman (2001). Statistics on the imports of antibiotics to Chile suggest their usage in large quantities in salmon farming (Cabello, 2003). It is necessary to reduce this usage to avoid a major environmental sanitary problem (Wolff, 2004). The environmental impacts of using malachite green, antifouling paints, and other chemicals have not been studied.
Escaped farmed salmon
The reported number of fish escaping from salmon farms in Chile varies annually, but the existing regulations have not led to a reduction in the reported biomass of escapees (Table 3). Independent assessment of the validity of the reports is necessary. Farmed salmon released into the wild appear to have a rather short life expectancy (<1 y) in Chilean coastal waters (Soto et al., 2001), as has been reported for the North Atlantic (Fleming et al., 1996). Previous attempts at salmon ranching in Chile were not successful, owing to the low survival of the released fish.
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There is concern in Chile, however, about the impact of escaped farmed salmon on the native fish fauna, although, because there are no natural populations of salmonids in Chile, escapees should not have the genetic impacts on indigenous populations reported in the North Atlantic (e.g. Fleming and Einum, 1997; Gross, 1998; Youngson and Verspoor, 1998; McGinnity et al., 2003; Roberge et al., 2006). Ecological interactions have been reported between farmed Atlantic salmon escapees and native Pacific salmon species (Volpe et al., 2000), and understanding the ecological effects that escapees have on native fish communities in Chile is a research priority. Although limited studies of the prey of escapees have been undertaken, existing studies indicate that benthic invertebrates are the main prey items.
Commercial fishing for salmon is prohibited in Chile, although illegal fishing does occur. It has been proposed that fishing for salmon by craft fishers could be used to reduce the impact of escaped farmed fish (Soto et al., 2001), although efforts to recapture escapees in the 1980s were unsuccessful. It has been suggested, however, that a legal fishery for escapees will encourage premeditated destruction of net pens to increase the availability of fish to support the fishery. The lack of clear evidence about the environmental impact of escapees and the absence of political support for a fishery targeting escapees (Buschmann et al., in press) suggest that this management tool is unlikely to be introduced.
Other impacts of salmonid farming
Salmonid farms can alter the natural transmission dynamics of sea lice to wild juvenile salmon with infestation pressures four orders of magnitude greater than the natural ambient level (Krko
ek et al., 2005). In Chile, preliminary data indicate that salmon farming can increase sea louse infestations on native fish populations (Sepúlveda et al., 2004).
The abundance of marine birds is also affected by the presence of salmon farms, with the observed abundance of omnivorous diving and carrion-feeding birds increasing twofold to fivefold in some areas with salmon farms (66.2–77.2 birds h–1) compared with control areas without them (13.8–31.0 birds h–1). However, the top-down ecological consequences of these changes remain unstudied. In addition, the effects of salmon farms on marine mammals have not been evaluated. The South American sea lion, Otaria flavescens, frequently attacks salmon farms, although the frequency of attacks varies markedly and is not correlated with the proximity of the nearest sea lion colony (Sepúlveda and Oliva, 2005). It is important that the impacts of salmon farms on marine mammals be considered in future research.
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Conclusions |
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TopIntroductionDevelopments in salmon farming...Impacts of salmonid farming...ConclusionsReferences |
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Salmon farming is one of the most important economic activities in Chile, but its development has environmental impacts (Buschmann and Pizarro, 2001) that should be taken into account in regulating the industry. Further research is urgently required in Chile to increase understanding of these impacts, especially if the industry is to expand to the far south, a pristine coastal area that needs a sound conservation policy. It is important that a balance is maintained between further aquaculture development in Chile and environmental conservation through the development of integrated cultivation of extractive (i.e. macroalgae and filter-feeders) and fed organisms (fish) in the same waterbodies (e.g. Buschmann et al., 2001; Chopin et al., 2001; Troell et al., 2003; Neori et al., 2004). Ideally, Chile's low level of research capacity should be increased to improve current understanding of aquaculture–environment interactions.
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Acknowledgements |
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This study was financially supported by Sarec-Conicyt, Fundación Terram, the British Embassy, Universidad de Los Lagos (i-mar Research Center), and FONDECYT 1050550 (Chile). The first author acknowledges earlier discussions with Daniel López, Nils Kautsky, Max Troell, Cristina Halling, Thierry Chopin, Amir Neori, and Charles Yarish. Support to attend the symposium in Bergen and the invitation from Malcolm Beveridge is gratefully acknowledged. We thank Leonardo Nuñez of the Fisheries Subsecretariat in Chile for data on salmon escapees and are grateful for the assistance of Marcos Villanueva and Adrián Villarroel in catching escapees and analysing the salmon stomach contents, and for the technical assistance of Richard Pinilla. We appreciate the review of this manuscript by Barbara Buschmann and Sandra Pereda.
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