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AQUACULTURE ENVIRIONMENT INTERACTIONS
Aquat Environ Interact
Vol. 1: 71–83, 2010
doi: 10.3354/aei00008
Published online August 12
INTRODUCTION
Definition of escapes from aquaculture
Escapes of fish from sea-cage aquaculture have typ-
ically been thought of as referring to juvenile and adult
fish. Such escapes have been reported for almost all
species presently cultured around the world, includ-
ing Atlantic salmon Salmo salar, Atlantic cod Gadus
morhua, rainbow trout Oncorhynchus mykiss, Arctic
charr Salvelinus alpinus, halibut Hippoglossus hippo-
glossus, sea bream Sparus aurata, sea bass Dicentra-
chus labrax, meagre Angyrosomus regius and kingfish
Seriola lalandi (e.g. Soto et al. 2001, Naylor et al. 2005,
Gillanders & Joyce 2005, Moe et al. 2007a, Toledo
Guedes et al. 2009). Recently, a second form of escape
has come into focus, involving the escape of viable, fer-
tilised eggs spawned by farmed individuals from sea-
© Inter-Research 2010 · www.int-res.com*Corresponding author. Email: tim.dempster@sintef.no
REVIEW
Escapes of fishes from Norwegian sea-cage
aquaculture: causes, consequences and prevention
Ø. Jensen
1
, T. Dempster
1, 2,
*
, E. B. Thorstad
3
, I. Uglem
3
, A. Fredheim
1
1
Centre for Research-based Innovation in Aquaculture Technology (CREATE), SINTEF Fisheries and Aquaculture,
7465 Trondheim, Norway
2
Department of Zoology, University of Melbourne, Victoria 3010, Australia
3
Norwegian Institute for Nature Research, 7485 Trondheim, Norway
ABSTRACT: The escape of fish from aquaculture is perceived as a threat to wild fish populations. The
escapes problem is largely caused by technical and operational failures of fish farming equipment. In
Norway, 3.93 million Atlantic salmon Salmo salar, 0.98 million rainbow trout Oncorhynchus mykiss
and 1.05 million Atlantic cod Gadus morhua escaped from 2001 to 2009. Salmonids primarily escape
after structural failures of containment equipment, while a far greater proportion of cod than salmon
escape through holes in the nets. Correlative evidence suggests that after the Norwegian technical
standard (NS 9415) for sea-cage farms took effect in 2004, the total number of escaped Atlantic
salmon declined from >600 000 (2001 to 2006) to <200 000 fish yr
–1
(2007 to 2009), despite the total
number of salmon held in sea-cages increasing by 44% during this period. No similar decrease in
escaped cod has occurred, suggesting that other measures, such as improved netting materials for
sea-cages, are required. In addition to escaping as juveniles or adults, cod may reproduce in sea-
cages, and thus fertilised eggs escape to the environment. The ecological effects of ‘escape through
spawning’ are unclear, and methods to inhibit escape by this mechanism are being explored. To pre-
vent escapes of juvenile and adult fish as sea-cage aquaculture industries develop, we recommend
that policy-makers implement a 5 component strategy: (1) establish mandatory reporting of all escape
incidents; (2) establish a mechanism to analyse and learn from the mandatory reporting; (3) conduct
mandatory, rapid, technical assessments to determine the causes of escape incidents involving more
than 10 000 fish; (4) introduce a technical standard for sea-cage aquaculture equipment coupled with
an independent mechanism to enforce the standard; and (5) conduct mandatory training of fish farm
staff in escape-critical operations and techniques.
KEY WORDS: Salmonids · Cod · Technology · Regulation · Standard · Competition · Disease ·
Interbreeding · Fish farming
Resale or republication not permitted without written consent of the publisher
O
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Aquacult Environ Interact 1: 71–83, 2010
cage facilities, or so-called ‘escape through spawning’
(Jørstad et al. 2008). This phenomenon has forced a
redefinition of the term ‘escapes from aquaculture’ to
include the escapement of fertilised eggs into the
wider marine environment.
Review scope
Here, we document the current status of knowledge
on the extent and causes of escapes, provide a short
summary of their economic and environmental conse-
quences, and discuss measures to prevent escapes. We
address both escapes of juvenile/larger fish and es-
cape through spawning. As most of the research and
development on the escapes issue over the past 2
decades has been related to the Norwegian fish farm-
ing industry, we use Norway as a case study to de-
scribe the development and implementation of mea-
sures to deal with escapes. Finally, we provide a series
of recommendations for policy makers to implement
measures to prevent escapes as sea-cage aquaculture
industries develop in other countries.
Background: the Norwegian fish farming industry
The Norwegian marine aquaculture industry, which
commenced in 1969–1970, is widely considered a com-
mercial success story. Today, Norway is a world leader
in the culture of salmon in sea-cages; 582 farms oper-
ated in coastal waters in 2008 and produced 797 000 t
of Atlantic salmon and 92 000 t of rainbow trout (Kjøn-
haug 2009). Approximately 310 million individual
Atlantic salmon and rainbow trout were held in sea-
cages in Norway at any given time during 2009 (Nor-
wegian Directorate of Fisheries 2009). The Atlantic cod
aquaculture industry is comparatively small and pro-
duced approximately 10 000 t across 40 farms in 2008,
corresponding to 25 million fish held in the sea (Nor-
wegian Directorate of Fisheries 2009).
Farm sites
In the early phase of sea-cage salmonid aquaculture,
farm sites were located next to the shore and in very
sheltered areas with little water exchange or flushing
(Oppedal et al. in press). Expansion of the industry in
terms of both farm number and size demanded sites
with greater water exchange both to ensure good
water quality for the fish and reduced impact on the
benthos from the accumulation of farm wastes. Mod-
ern sites are located farther from the shore, but are still
partly sheltered within bays, sounds and fjords or scat-
tered amongst islands within archipelagos.
Sea-cage technology
Significant advances in containment technologies
have been made since the industry commenced, with
modern production and fish transportation systems
now typically large and highly mechanised. Salmonids
and cod are kept in either square or rectangular sea-
cages of 20 to 40 m sides, 20 to 35 m deep or circles of
90 to 157 m in circumference and 15 to 48 m deep.
Cage volumes range from 20 000 to 80 000 m
3
. Square
cages are typically clustered together in a steel plat-
form with between 4 and 28 cages site
–1
with little dis-
tance (2 to 4 m) between adjacent cages. Circular
cages (typically 6 to 12 site
–1
) are arranged in mooring
grids in single or double rows but with typically
greater space between them (>20 m) than square
cages. Initially, cage arrangements within sites were
chosen based on logistical considerations such as
moorings, shelter and accessibility. Present-day cage
arrangements have moved towards positioning cage
grid mooring systems perpendicular to the dominant
current direction to maximise water flow, oxygen sup-
ply and the removal of wastes from individual cages.
Biomasses and stocking densities
Based on the maximum allowable stocking density of
25 kg m
–3
in Norway (Norwegian Ministry of Fisheries
and Coastal Affairs 2008) and normal harvest weights
of 4 to 5 kg, individual cages in the 1970s held ~10 000
fish. Individual cages may now contain 200 000 to
400 000 fish. In practice, the largest Norwegian sites
produce more than 10 000 t of salmon biomass, consti-
tuting more than 2 million individual salmon. In con-
trast, individual cod farms are much smaller, produc-
ing 100s rather than 1000s of tons site
–1
.
EXTENT OF ESCAPES
Norway has the most comprehensive national
record of escapes in the world; official numbers exist
back to 2001 for salmonids and to 2004 for Atlantic
cod. In the 9 yr of production from 2001 to 2009, 3.93
million Atlantic salmon (436 000 yr
–1
) and 0.98 million
(110 000 yr
–1
) rainbow trout were reported to have
escaped from Norwegian farms (Fig. 1). In addition, in
the 6 yr from 2004 to 2009, 1.05 million Atlantic cod
(175 000 yr
–1
) escaped. The percentage of fish re-
ported to escape relative to the overall numbers of
fish in the sea vary greatly among these 3 species,
with escape rates lowest for Atlantic salmon and
highest for Atlantic cod: average escaped proportion
2001–2009 = (total no. escaped fish reported)/(esti-
72
Jensen et al.: Escapes of fish from sea-cage aquaculture
mated total no. fish held in sea-cages); salmon: 0.19%,
trout 0.40%, cod 1.02%.
From 2005 to 2009, the number of salmonids held at
individual farming locations increased industry-wide
by approximately 50% (Fig. 2). As the number of fish
within individual cages and individual farming sites
increases, the potential consequences due to individ-
ual cage or farm breakdown increases. However, the
farmers claim that with fewer units in the sea, the
probability of escape events decreases. Independent of
these contradicting factors regarding escape risks, the
total reported number of salmon escaping from sea-
cage farms has recently declined. Escapes of salmon
climbed in number (272 000 to 921 000) and as a per-
centage of the total number of fish held in cages (0.15
to 0.38%) from 2001 to 2006, before declining substan-
tially to <200 000 fish yr
–1
and 0.07% on average for
2007 to 2009 (Fig. 1). This reduction in the total number
of escapees occurred despite a marked 44% increase
in the total number of fish held in sea-cages in the
2007–2009 period compared to the 2001–2006 period.
The marked decrease in the reported number of
escapes is primarily due to a decrease in the number of
large escape events involving >10 000 fish.
For rainbow trout and Atlantic cod, trends in the total
number and proportion of escaped fish over time are
less clear than for Atlantic salmon (Fig. 1). As the num-
bers of fish in the sea for both these species are at least
an order of magnitude less than salmon, the occur-
rence of a single large escape event can skew the
escape statistics in individual years. Between 7000 and
315 000 rainbow trout escaped in any given year from
2001 to 2009, with the escape percentage varying from
0.03 to 0.92%. In the year with the greatest number
(315 000) and highest proportion (0.92%) of escapes,
only 3 escape incidents were recorded, yet 1 of these
was responsible for the loss of 300 000 fish. Similarly,
for cod, year to year reported escapes totalled 20 000 to
304 000 from 2004 to 2009, representing 0.22 to 1.89%
of the fish held in sea-cages. Years with high total
numbers of escaped fish were characterised by having
1 or more escape events where >100 000 fish escaped.
Our analyses of total numbers of escaped fish and
the percentage of fish that escape rely on the officially
reported statistics, which have been speculated to sig-
nificantly underestimate the true level of escapes
(Fiske et al. 2006, Torrissen 2007), because not all
escape incidents are detected and/or reported. Debate
exists regarding the extent to which large-scale escape
events and smaller, less detectable escape events con-
73
Fig. 1. Salmo salar, Oncorhynchus mykiss and Gadus morhua.
Estimated numbers of cultured fish (Atlantic salmon, rainbow
trout and Atlantic cod) held in sea-cages (J) in Norway as of
31 December each year from 2001 to 2009 and numbers of
escaped fish (J) reported to the Norwegian Fisheries Direc-
torate. Numbers within each figure give the proportion of fish
that escaped each year calculated as the number of reported
escapees divided by the total estimated number of fish in
the sea-cages
Fig. 2. Salmo salar. Average number of Atlantic salmon held
per location from 2001 to 2009 based on estimated number
of fish in the sea-cages and the number of sea-cage locations
in operation
Aquacult Environ Interact 1: 71–83, 2010
tribute to the overall number of escaped fish. We do not
address this debate in detail here; however, future
studies that address this issue will provide greater per-
spective on the official statistics. In addition, recent
advances in Norway on tracing escaped fish with
genetic techniques and their subsequent successful
use in court cases against farms that have not reported
escapes (Glover 2010), may lead to greater detectabil-
ity and an increase in the reporting of escapes in the
future. Regardless of the inherent limitations of the
data set, there is no reason to suggest that the sources
of error in reporting have varied over time; thus the
official statistics provide a solid baseline of data for
comparisons across time.
CAUSES OF ESCAPES
Escapes are caused by a variety of incidents related
to farming equipment and its operation. Reports by fish
farming companies to the Norwegian Directorate of
Fisheries following escape events during the period
from September 2006 to December 2009 indicate that
escapes of Atlantic salmon (by total number of fish
escaped) are dominated by structural failures of equip-
ment (68%), with operational related-failure (8%),
escapes due to external factors (8%) and escapes from
land-based facilities (11%) making up lesser propor-
tions (Fig. 3). Structural failures may be generated by
severe environmental forcing in strong winds, waves
and currents, which may occur in combination with
component fatigue or human error in the way farm
installations have been installed or operated (Jensen
2006). The dominance of structural failures as the main
cause of escape of Atlantic salmon is also visible in the
seasonal pattern of escape incidents (Fig. 4), with the
greatest number of large-scale escape events (>10 000
individuals) occurring in the autumn months when
coastal storms are most frequent and intense. For rain-
bow trout, structural failures accounted for 36% of
escapees, while a predation event by seals at 1 farm
which subsequently caused 132 634 fish to escape
through a net tear was the reason for the high contri-
bution of biological causes (56%) in this period (Fig. 3)
For cod, evidence suggests that additional reasons
for escape exist beyond those present for salmonids
(Moe et al. 2007a). This stems from behavioural differ-
ences in the way cod interact with cages, through bit-
ing of the netting, which may increase wear and tear
and contribute to the creation of holes (Moe et al.
2007a), and a far greater level of exploratory behaviour
near the net wall, which may increase the chances of
cod swimming through a hole (Hansen et al. 2008). Of
the 56 escape events reported from September 2006 to
December 2009, external (38%) and biological (25%)
causes accounted for the greatest numbers of escaped
cod. In addition, the reason for escape was undeter-
mined for a significant proportion of the total number
of fish that escaped (27%). In contrast to salmon, there
was no specific seasonality in the occurrence of large
(>10 000 individuals) or medium (1000 to 9999 individ-
uals) escape incidents (data not shown).
Large-scale escape events of salmon, trout and cod
(>10 000 individuals) represented only 19% of the
escape incidents reported, but accounted for 91% of
the number of escaped fish (Fig. 5), indicating that a
focus on preventing this small proportion of large-scale
incidents will have a great effect in diminishing the
consequences of escapes. Structural failures, while rel-
atively infrequent, lead to the greatest number of fish
escaping (10s to 100s of thousands of fish per incident);
therefore, they are the area of greatest focus in pre-
74
Fig. 3. Causes of escape based on reports by fish farming
companies to the Norwegian Fisheries Directorate from 1
September 2006 to 31 December 2009. n
1
: total number of
reported escape incidents upon which the % of fish escaped
by cause is based. n
2
: total number of escaped fish reported
from 1 September 2006 to 31 December 2009 upon which the
% of fish escaped by cause is based
Fig. 4. Salmo salar. Seasonality of escape events for Atlantic
salmon reported to the Norwegian Fisheries Directorate from
1 September 2006 to 31 December 2009
Jensen et al.: Escapes of fish from sea-cage aquaculture
venting escapes. Operational errors that cause escapes
are more frequent, but typically lead to spills as small
as a few individuals to thousands of fish, so they are of
secondary importance in mitigating the escapes prob-
lem. Below, we document in detail the status of knowl-
edge on 3 of the main causes of structural failures lead-
ing to escapes and provide examples.
Progressive mooring failure
Today, flexible circular tubes made of polyethylene
are the most commonly used floating collars in Norwe-
gian aquaculture. The major part of the flexible float-
ing collars is moored using either a grid or a ladder
mooring system. The floaters are connected to the
mooring using bridles (Fredheim & Langan 2009). Tra-
ditionally, the grid mooring system was oriented to
minimise the total drag force on the fish farm, i.e. with
the direction of the main current running through the
length of the fish farm. Orienting the farm in this man-
ner reduces the total drag, as only the front nets are
fully exposed to the current (the subsequent ones are
in the shadow of those in front and will experience a
reduced current velocity). However, when the farm is
oriented in this manner, the number of mooring lines in
the same direction as the main current is limited. Dur-
ing a storm, the current velocity increases, especially
in the upper water layers, exerting large forces on the
nets. These forces are transferred to the mooring lines
through the bridles. If 1 mooring line breaks or 1
anchor drags, the loads on the remaining mooring lines
might be exceeded and they will rupture one by
one, resulting in a complete failure of the fish farm
(Fig. 6A). This was the cause of the complete break-
down of a fish farm in which close to 500 000 salmon
escaped in central Norway in August 2005.
Breakdown and sinking of steel fish farms
Hinged steel fish farms are popular work stations as,
due to their buoyancy, they allow the use of heavy aux-
iliary equipment and fork lifts on the farm. Due to their
construction, steel farms in general have no or limited
flexibility in the horizontal plane (Fredheim & Langan
2009). This gives rise to structural problems when
exposed to short-crested irregular waves, as the waves
induce forced vertical displacement of the bridges and
introduce large stresses and strains in the structure.
Fatigue and crack propagation in or close to the hinges
often result and can lead to separation of the bridges
75
Fig. 5. Salmo salar. Numbers of Atlantic salmon escaped by
size of the escape incident from 2006 to 2009. n
1
: number of
reported escape incidents causing 1 to 9999 fish to escape.
n
2
: number of reported escape incidents causing >10 000 fish
to escape
Fig. 6. Examples of the major structural causes of escape inci-
dents: (A) progressive mooring failure; (B) breakdown and
sinking of steel fish farms; and (C) abrasion and tearing of nets
Aquacult Environ Interact 1: 71–83, 2010
(Fig. 6B) and tearing of the net. In January 2006, close
to 150 000 cod escaped from a fish farm in northern
Norway during a storm. The fish escaped after the
farm collapsed under the combined loading from wind,
waves and ice (Jensen 2006). Due to forced displace-
ment induced by the waves and ice, the farm was torn
apart and the fish escaped.
Abrasion and tearing of nets
Net failure, and the subsequent formation of a hole,
is by far the dominant means of reported escape for
fish from Norwegian aquaculture. Approximately two-
thirds of reported escape incidents and number of fish
escape due to holes in the nets. Multiple reasons exist
for the formation of holes. Biting by predators or caged
fish, abrasion, ‘collisions’ with boats, flotsam and cage
handling procedures (e.g. lifting) are among the most
common causes of holes in the nets (Fig. 6C). The trend
in Norway is that fish farms are moving into areas with
stronger and steadier currents in order to improve
water quality. As a result, forces on the net increase
and net deformation increases accordingly (Lader et al.
2008). Several large-scale escapes have occurred over
the past 2 to 3 yr due to contact (and thus abrasion) be-
tween the net and the sinker tube chain (Moe 2008a,b,
2009). In one of them, more than 80 000 fish escaped.
ECONOMIC CONSEQUENCES TO FISH FARMERS
Relatively little information exists on the direct costs
of escapes, although the European Union’s 7th Re-
search Framework project Prevent Escape (www.sintef.
no/preventescape) is currently assessing the cost of es-
cape to the fish farming industry across Europe, and the
true cost of escapes is thus likely to be known by 2011.
In Norway, as reported escapes of salmon on average
account for losses of <0.2% of the fish held in sea-cages
each year, the relative direct economic cost to the in-
dustry is small, even when the cost of replacing dam-
aged equipment or paying for recapture efforts is ac-
counted for. Insurance claims are likely to offset these
costs (Naylor et al. 2005). This may mean that little di-
rect economic incentive exists for salmon farmers to in-
vest further time and resources to prevent escape
events. As the proportion of cod that escape is consider-
ably greater than that of salmon, direct economic losses
are more significant (Moe et al. 2007a) and may stimu-
late investments in containment technologies.
The greatest cost of escape to the industry, however,
is indirect, as escapes damage the industry’s reputa-
tion. The popular press often report escape events
widely, which sheds negative light on the industry’s
environmental credentials and fuels criticism from
environmental groups (e.g. WWF 2005). The extent to
which this restricts the industry from expanding the
number of sites it uses and the amount of fish it pro-
duces is immeasurable, but is likely to be significant,
as the threats that escapes pose to wild populations are
strong counterpoints in debates regarding industry
expansion (Naylor et al. 2005, Hindar et al. 2006).
While the economic consequences of reduced produc-
tion caused by escaped salmon are not known for Nor-
way, a review of the general economic consequences
of escapes to wild salmon populations is given by
Naylor et al. (2005).
ENVIRONMENTAL CONSEQUENCES
Escapees can have detrimental genetic and ecologi-
cal effects on populations of wild conspecifics, and the
present level of escapees is regarded as a problem for
the future sustainability of sea-cage aquaculture (Nay-
lor et al. 2005). Over 325 million Atlantic salmon are
held in sea-cages in Norway at any given time (Norwe-
gian Directorate of Fisheries 2009), which outnumbers
the ~500 000 to 1 million salmon that return to Norwe-
gian rivers from the ocean each year to spawn (Scien-
tific Advisory Committee 2009). A single sea-cage may
hold 100s of thousands of cultured fish, meaning that
sites with multiple cages may contain more than 1 mil-
lion fish. Due to the large numerical imbalances of
caged compared to wild populations, escapement
raises important concerns about ecological and genetic
impacts. Evidence of environmental effects on wild
populations is largely limited to Atlantic salmon, as
these interactions have been intensively studied, with
more limited information for Atlantic cod.
Atlantic salmon
In a comprehensive review of the effects of escaped At-
lantic salmon on wild populations, Thorstad et al. (2008)
concluded that while outcomes of escapee–wild fish
interactions vary with environmental and genetic factors,
they are frequently negative for wild salmon. As fish farm
areas are typically located close to wild fish habitats, and
escaped fish may disperse over large geographic areas
(e.g. Furevik et al. 1990, Hansen 2006, Whoriskey et al.
2006, Skilbrei et al. in press), escaped salmon may mix
with their wild conspecifics and enter rivers 10s to 100s of
kilometers from the escape site during the spawning
period. The average proportion of escaped salmon in
Norwegian rivers monitored close to the spawning period
varied between 11 and 35% during 1989 to 2008, with
the highest proportions during the late 1980s and early
76
Jensen et al.: Escapes of fish from sea-cage aquaculture
1990s (Scientific Advisory Committee 2009). Conse-
quently, the potential exists for escapees to interact
negatively with wild populations, through competition,
transfer of diseases and pathogens, and interbreeding.
Transfer of diseases and pathogens
Escape incidents may heighten the potential for the
transfer of diseases and parasites, which are consid-
ered to be amplified in aquaculture settings (e.g.
Heuch & Mo 2001, Bjørn & Finstad 2002, Skilbrei &
Wennevik 2006, Krkoˇsek et al. 2007). Escapees from
salmon aquaculture in Norway have been identified as
reservoirs of sea lice in coastal waters (Heuch & Mo
2001). In addition, 60 000 salmon infected with infec-
tious salmon anaemia and 115 000 salmon infected
with pancreas disease escaped from farms in southern
Norway in 2007, yet whether these precipitated infec-
tions in wild populations is unknown. The ability for
escaped fish to transfer disease to wild fish depends on
the extent of mixing between the 2 groups, which in
turns varies with the life stage, timing and location of
the escape (summarised by Thorstad et al. 2008). How-
ever, while escaped and wild fish mix, little direct evi-
dence for disease transfer from escapees to wild
salmon populations exists, other than for the possible
case of furunculosis, a fungal disease accidently intro-
duced to Norway from Scotland in the 1990s with the
transfer of stock and then believed to have been
spread from farmed to wild populations by escapees
(summarised by Naylor et al. 2005).
Interbreeding
Successful spawning of escaped farmed salmon in
rivers both within and outside their native range has
been widely documented (see review by Weir & Grant
2005). The ability of escaped salmon to interbreed with
wild salmon depends on their ability to ascend rivers,
access spawning grounds and spawn successfully with
wild partners. While the spawning success of farmed
female salmon may be just 20 to 40% that of wild
salmon and even lower for males (1 to 24%; Fleming
et al. 1996, 2000), high proportions of escaped fish in
many rivers can lead to a high proportion of farm ×
wild hybrids. Escaped female salmon may also inter-
fere with wild salmon breeding through the destruc-
tion of spawning redds of wild fish due to later spawn-
ing (Lura & Sægrov 1991, 1993).
Wild Atlantic salmon are structured into populations
and meta-populations with little gene flow between
them, and evidence for local adaptation in wild Atlantic
salmon is compelling (reviewed by Garcia de Leaniz et
al. 2007). Farmed salmon differ genetically from wild
populations due to founder effects, domestication selec-
tion, selection for economic traits and genetic drift (re-
viewed by Ferguson et al. 2007). Hybridisation of
farmed with wild salmon and later backcrossing of hy-
brids may change the level of genetic variability and
the frequency and type of alleles present. Hence, hy-
bridisation of farmed with wild salmon has the potential
to genetically alter native populations, reduce local
adaptation and negatively affect population viability
and character (Ferguson et al. 2007). Several studies
have shown that escaped farmed salmon breeding in
the wild have changed the genetic composition of wild
populations (e.g. Clifford et al. 1998, Skaala et al. 2006).
Hindar & Diserud (2007) recommended that intrusion
rates of escaped farmed salmon in rivers during spawn-
ing should not exceed 5% to avoid substantial and def-
inite genetic changes of wild populations.
Large-scale field experiments undertaken in Nor-
way and Ireland showed highly reduced survival and
lifetime success of farm and hybrid salmon compared
to wild salmon (McGinnity et al. 1997, 2003, Fleming
et al. 2000). The relative estimated lifetime success
ranged from lowest for the farm progeny to highest for
the local wild progeny with intermediate performance
for the hybrids. Farmed salmon progeny and farm ×
wild hybrids may directly interact and compete with
wild juveniles for food, habitat and territories. Farm ju-
veniles and hybrids are generally more aggressive and
consume similar resources in freshwater habitats as
wild fish (Einum & Fleming 1997). In addition, they
grow faster than wild fish, which may give them a com-
petitive advantage during certain life stages. Invasions
of escaped farmed salmon have the potential to impact
the productivity of wild salmon populations negatively
through juvenile resource competition and competitive
displacement. Fleming et al. (2000) determined that in-
vasion of a small river in Norway by escapees resulted
in an overall reduction in smolt production by 28% due
to resource competition and competitive displacement.
Local fisheries could therefore suffer reduced catches
as wild fish stocks decline (Svåsand et al. 2007).
Competition for food
Escaped salmon consume much the same diet as
wild salmon in oceanic waters (Hislop & Webb 1992,
Jacobsen & Hansen 2001) and could potentially com-
pete for food with wild stocks. Substantial competitive
interactions in the ocean, however, appear unlikely to
occur, as ocean mortality of salmon appears to be den-
sity-independent (Jonsson & Jonsson 2004), although
limited information exists to assess if this is also the
case for coastal waters (Jonsson & Jonsson 2006).
77
Aquacult Environ Interact 1: 71–83, 2010
Atlantic cod
At present, little direct evidence exists for negative
interactions of escaped and wild Atlantic cod juveniles
or adults, despite predictions that negative conse-
quences will result (Bekkevold et al. 2006). Cod farm-
ing is a relatively new industry; thus if negative conse-
quences exist, they may not have had sufficient time to
manifest and/or be detected. Telemetry studies of sim-
ulated cod escapes have indicated that escapees,
regardless of whether they originated from stocks of
coastal or oceanic origin, mix with wild populations in
fjord environments and can move to spawning grounds
in the spawning season (Uglem et al. 2008, 2010).
Behavioural studies have further indicated that es-
caped farmed cod are likely to hybridise with wild cod
(Meager et al. 2009). However, farmed cod may have
limited reproductive success in sperm competition
with wild cod, which lowers the risk of genetic intro-
gression from escapees (Skjæraasen et al. 2009). Fur-
ther, they may occupy different strata in the water col-
umn at breeding time relative to wild cod (Meager et
al. 2009).
Other possible ecological effects of escaped farmed
cod include increased predation pressure on out-
migrating wild salmon smolt (Brooking et al. 2006) and
transmission of pathogens and parasites to wild pop-
ulations (Øines et al. 2006), although direct evidence
for these effects is at present lacking. Recaptures of
Atlantic cod escapees equipped with acoustic transmit-
ters in local commercial and recreational fisheries in
Norway are high (~40%; Uglem et al. 2008), indicating
that local fisheries receive temporary increases after
escape events and may be partially effective in reduc-
ing escaped cod numbers.
‘Escape through spawning’ of Atlantic cod
In the culture of Atlantic cod, some fish mature dur-
ing the first year of culture, while a majority of farmed
cod are believed to mature during the second year.
This means that almost the entire culture stock in any
particular farm has the potential to spawn in sea-cages
before they are slaughtered. Spawning of Atlantic cod
within a small experimental sea-cage containing 1000
farmed cod and dispersal of their spawned eggs up to
10 km away in a fjord system has been demonstrated
(Jørstad et al. 2008). In the proximity of this experimen-
tal sea-cage, 20 to 25% of the cod larvae in plankton
samples were determined by genetic analyses to have
originated from the 1000 farmed cod (Jørstad et al.
2008). Furthermore, preliminary results indicate that 4
to 6% of juvenile cod (35 to 40 cm total length) caught
in the area around the farm in following years were
offspring of the farmed cod (van der Meeren & Jørstad
2009). This illustrates that if spawning occurs within
commercial cod farms where numbers of farmed indi-
viduals are far greater, the contribution of ‘escaped’
larvae to cod recruitment within fjord systems may be
substantial.
Escape of large quantities of eggs from caged cod
could lead to ecological and genetic effects in wild
populations (Bekkevold et al. 2006, Jørstad et al. 2008),
as (1) coastal cod populations in some areas of Norway
are presently weak, most likely due to overfishing
(ICES 2008); (2) coastal cod have a high fidelity to spe-
cific spawning grounds (e.g. Wright et al. 2006); and (3)
sea-cage cod farms are often located within short dis-
tances of known wild cod spawning grounds (Uglem et
al. 2008). Recent research also suggests that cod eggs
may be entrained in the vicinity of the spawning
grounds long after spawning (Knutsen et al. 2007).
Therefore, there is considerable potential for larvae
from escaped cod eggs to experience favourable con-
ditions for survival and recruitment to coastal cod
stocks if spawning in sea-cages occurs during the nat-
ural spawning season of wild cod.
PREVENTING ESCAPES: THE NORWEGIAN
EXPERIENCE
Adult fishes
Over the past decade, Norway has established a
range of processes and tools to deal with the problem
of escapes. These include: (1) mandatory reporting of
all escape incidents; (2) establishment of the Norwe-
gian Escapes Commission to learn from past escape
events and disseminate knowledge to both fish farmers
and aquaculture equipment suppliers; (3) introducing
enforceable technical regulations for the design,
dimensioning, installation and operation of sea-cage
farms; (4) ongoing investment in research and devel-
opment projects to improve the design and material
properties of sea-cage equipment; and (5) training of
fish farm operators in the different aspects of why and
how to prevent escapes. Here, we detail these efforts,
describe their effect on dealing with the escapement
issue, and discuss improvements that can be made.
Mandatory reporting
Mandatory reporting of escape incidents was intro-
duced by Norway in the 1980s, with a national statis-
tics database established in 2001. This has enabled: (1)
assessment of the overall status of the escapes problem
at an industry-wide scale from year to year (e.g. Fig. 1);
78
Jensen et al.: Escapes of fish from sea-cage aquaculture
(2) assessment of the causes of escapes (e.g. Fig. 3);
and (3) efforts to recapture escapees to be made. With-
out this basic process in place, coordinated action to
deal with escapes is unlikely because the scale of the
problem cannot be estimated. Establishing that es-
capes are of sufficient magnitude to have an ecological
impact will drive mechanisms for change in practices
or regulations. However, while mandatory reporting
does provide useful, general information, understand-
ing the detailed causes of escapes requires different
processes. In addition, an evaluation of the proportion
of real losses reported through such a mandatory
reporting system should be performed, both in Norway
and elsewhere. To be able to fully evaluate the causes
for escapes, the proportion of unreported escapes, and
the reasons for these escapes, should also be known.
Norwegian Aquaculture Escapes Commission (AEC)
Official statistics collated from mandatory reporting
and other sources of information which apportion
causality to escape events typically provide little ex-
plicit detail to support technological development to
improve farming equipment and modify operations to
avoid mistakes that cause escapes. Categorisation of
causes from mandatory reporting forms may also be
inaccurate, as causes are rarely investigated in detail
by individual farmers (Valland 2005). Such detail only
comes through careful investigation of the causes of
escape incidents on a case-by-case basis. For example,
Jensen (2006) visited 8 fish farms in northern Norway
after 2 severe storms in January 2006 caused damage
to numerous farms in the region. While ‘storm’ was
listed as the official cause of these escapes, the spe-
cific circumstances behind each event varied widely.
Storms may damage surface floaters, tear nets through
net deformation or rubbing of the nets on net weights
in the strong currents they generate, and overload the
mooring structures that hold the farm in place. At a
smaller scale, an understanding of how individual
components perform in the mooring system (such as
anchors, shackles, ropes, bolts and mooring coupling
plates), the cage system (net material, cage ropes and
cage weights) and the steel platform or polyethylene
floaters is crucial to ensure each element is engineered
to match the particular characteristics of each farm
type and location.
To meet the challenge of more accurately determin-
ing causes of escapes, the Norwegian government es-
tablished the AEC in September 2006. Since its estab-
lishment, the AEC has compiled data on all reported
escape occurrences in Norway and has a mandate to
conduct more thorough investigations of individual
escape events when required. The AEC disseminates
information to manufacturers of fish farming equip-
ment when improvements have been identified, and
may issue warnings to fish farmers regarding the use
of specific sea-cage technologies.
Norwegian technical standard (NS 9415)
The Norwegian technical standard NS 9415 (Marine
fish farms: requirements for site survey, risk analyses,
design, dimensioning, production, installation and
operation regulations; Standard Norge 2009) was
implemented through Norwegian legislation on 1 April
2004 and introduced requirements for the technical
standard of marine fish farms in Norwegian waters. NS
9415 specifies requirements for the design of feed
barges, floaters, net cages and mooring systems neces-
sary to cope with environmental forces (e.g. wind,
waves, currents) at fish farm sites and the handling
and use of equipment. From 1 April 2004, the main
components (floater, net cage, feed barge and mooring
system) of new farms must be independently certified
against the standard. In addition, farming sites needed
to be classified (wind, waves and current conditions)
with 10 and 50 yr return periods. For existing farms
and equipment in use before 1 April 2004, there is
a transitional system which began to take effect on
1 January 2006 and runs until 2012.
Specially accredited independent companies assess
the fish farms, carry out mooring and other technical
analyses and use these data to evaluate the capability
of the fish farm to meet the requirements of NS 9415
and to withstand the environmental forces at the spe-
cific fish farm site. If the equipment is proven capable
for the site, the fish farm will receive a certificate stat-
ing proof of capability. This proof of capability is valid
for up to 3 yr and can be reissued repeatedly until
2012. From 2012, all the main components of a fish
farm have to be certified. A revision occurred in 2009
and resulted in significant strengthening of the NS
9415 standard.
As an immediate result of introduction of NS 9415 in
2004, several farms replaced their existing equipment
in the 2 to 3 following years, and all new equipment
acquired post-2004 had to be independently certified
as per the standard. This appears to have precipitated
a dramatic reduction in the number of major escape
incidents in Norway (Fig. 1), although with a time lag
of several years after the standard was introduced, as
old equipment was gradually replaced with new. Since
the last major escape events in 2005 and 2006, the
number of reported escaped salmon has been signifi-
cantly reduced both in terms of the total number of
escapees and as a proportion of the stocked number of
salmon in sea-cages. This reduction is principally due
79
Aquacult Environ Interact 1: 71–83, 2010
to a sharp decline in large-scale escapes resulting from
the full breakdown of whole cages or whole fish farms
when floaters and/or mooring systems fail. Such fail-
ures are becoming increasingly uncommon as the NS
9415 standard is modified and strengthened over time.
Research and development to make equipment more
robust
Development of the NS 9415 standard has been in-
formed by a significant amount of industrial research to
improve the materials, structures and designs of sea-cage
farms (e.g. Fredheim 2005, Jensen 2005, 2006, Jensen &
Lien 2005a,b, Lien & Jensen 2005, Moe et al. 2005,
2007a,b, 2009a,b, Lader & Fredheim 2006, Lader et al.
2007, 2008). This research has come about through signif-
icant investments by the Norwegian Research Council
and the Norwegian Fishery and Aquaculture Industry
Research Fund (e.g. SIKTEK, IntelliStruct, SECURE,
CodNet, CodNet2 and WaveNet projects) and recently
the European Union’s 7th Research Framework (e.g. Pre-
vent Escape project; www.preventescape.eu).
Training
As a relatively large portion of the reported escape
incidents are either due to operational errors or to oper-
ations damaging equipment and thus leading to es-
capes, an increased focus on how operations are per-
formed is appropriate. Some farming companies have
good and well documented systems for training and ed-
ucation of employees, but in general, more focus is nec-
essary. Fish farming is a complicated multi-disciplinary
activity in which expertise on several different topics is
required. So far, education has focused mainly on the
biological aspects of farming, with comparatively less
attention given to the more technical aspects.
To address this gap, several times a year the Norwe-
gian Seafood Federation (FHL) arranges voluntary anti-
escape workshops which are attended by fish farmers,
technology producers, the Norwegian Fisheries Direc-
torate and accredited aquaculture equipment certifica-
tion companies. Technical aspects of the workshops are
often led by industrial engineers from SINTEF Fisheries
and Aquaculture. Typical topics for the workshops are
information about regulations, escape causes and prac-
tical measures to prevent escapes.
Atlantic cod eggs
At present, the culture of Atlantic cod in sea-cages in
Norway is a relatively new activity of limited size com-
pared to the large Atlantic salmon industry. Further,
the possibility that escaped fertilised eggs may have
genetic and ecological effects on wild populations has
only recently been recognised (Jørstad et al. 2008).
Much remains to be documented before the likely
importance of this effect is known.
Measures to prevent the escape of fertilised eggs
from sea-cages are in the research and development
phase. Mechanical methods of removal, such as filtra-
tion, are unlikely to prove practical or affordable at the
scale of modern cod farming. Halting sexual matura-
tion through manipulation of the light regime in sea-
cages has been trialled with some success, but it is dif-
ficult to inhibit maturation completely (e.g. Karlsen et
al. 2006, Taranger et al. 2006) as natural light levels
may override artificial lights during the daytime, thus
reducing the efficacy of artificial light regimes. Hybri-
disation, sterilisation and polyploidy (e.g. Feindel et al.
2010) are possible alternate strategies, but higher ini-
tial mortality, greater fingerling costs, poorer growth
and uncertainty about consumer acceptance mean that
these techniques are not preferred by the industry (Tri-
antafyllidis 2007). As no clear solution exists, investi-
gating techniques to stop cod from spawning in sea-
cages remains a research and development priority for
Norwegian aquaculture.
RECOMMENDED ACTIONS
Based on the Norwegian experience of dealing with
the escapes problem, we recommend a range of mea-
sures for other countries to introduce effective anti-
escape measures. Essentially, many of the components
of the strategy to tackle escapes already in place in
Norway can be directly transferred to industries in
other countries. We outline these principles below in 5
steps, and discuss how some of these measures may
also be improved within Norway:
1. Mandatory reporting of all escape events, includ-
ing: (1) the number of fish that escaped and their size;
(2) a description of the sea-cage technology involved;
(3) categorisation of the operational circumstances or
environmental conditions at the time of escape; and (4)
an estimated cause of escape.
2. A defined mechanism to collect, analyse and learn
from the mandatory reporting. This information must
then be effectively disseminated to equipment suppli-
ers and fish farmers so improvements can be made.
Within Norway, the AEC has this role, although the
formation of a full commission to achieve this may not
be necessary in other countries.
3. As causes of escapes estimated by farmers are
often inaccurate, we recommend mandatory, technical
assessments to determine the causes of ‘large-scale’
80
Jensen et al.: Escapes of fish from sea-cage aquaculture
escape incidents. Based on escape statistics in Norway,
‘large-scale’ escape events can be considered to be
those that cause the loss of more than 10 000 fish. The
technical assessment must occur rapidly (within 48 h)
after the escape event. At present, no mechanism for
this is in place in Norway. When technical assessments
are made, they are often done weeks to months after
the incident. This can lead to a loss of evidence, often
making the root cause difficult to ascertain. Learning
from each large-scale escape event would assist rec-
ommendations for the design and properties of sea-
cage systems and help improve technical standards.
4. Introduction of a technical standard for sea-cage
aquaculture equipment coupled with an independent
mechanism to enforce the standard. Within Norway,
the highly detailed NS 9415 technical standard has
perhaps been the most useful tool at an industry-wide
scale to prevent escapes. Voluntary standards are
unlikely to be effective; therefore, we recommend
enforcement through legislation. Within the next few
years, NS 9415 is likely to be developed into an inter-
national standard (ISO), which will facilitate imple-
mentation in sea-cage industries worldwide.
5. Certain operations within fish farming (e.g. correct
anchoring and mooring, connecting net-cages to
floaters and correct weighting of net-cages in currents)
are likely to pose a higher risk of an escape event
occurring if they are done incorrectly. Therefore, these
key processes should be identified, and mandatory
training of staff who undertake these processes would
likely reduce human errors that lead to escapes. Many
other industries have similar mandatory training
requirements for operators to perform particular tasks,
and thus legislative precedents would likely exist in
most countries that could be drawn upon.
Acknowledgements. We thank the Norwegian Directorate of
Fisheries and the Norwegian Aquaculture Escape Commis-
sion (AEC) for providing data and Fig. 6B. Funding was pro-
vided by the European Union’s 7th Research Framework to
the Prevent Escape project (no. 226885) and by the Norwe-
gian Research Council’s ‘Havbruk’ programme to the Secure
project (no. 184974/S40).
LITERATURE CITED
Bekkevold D, Hansen MM, Nielsen EE (2006) Genetic impact
of gadoid culture on wild fish populations: predictions,
lessons from salmonids, and possibilities for minimizing
adverse effects. ICES J Mar Sci 63:198–208
Bjørn PA, Finstad B (2002) Salmon lice, Lepeophtheirus
salmonis (Krøyer), infestation in sympatric populations of
Arctic char, Salvelinus alpinus (L.), and sea trout, Salmo
trutta (L.), in areas near and distant from salmon farms.
ICES J Mar Sci 59:131–139
Brooking P, Doucette G, Tinker S, Whoriskey FG (2006) Sonic
tracking of wild cod, Gadus morhua, in an inshore region
of the Bay of Fundy: a contribution to understanding the
impact of cod farming for wild cod and endangered
salmon populations. ICES J Mar Sci 63:1364–1371
Clifford SL, McGinnity P, Ferguson A (1998) Genetic changes
in Atlantic salmon (Salmo salar) populations of northwest
Irish rivers resulting from escapes of adult farm salmon.
Can J Fish Aquat Sci 55:358–363
Einum S, Fleming IA (1997) Genetic divergence and interac-
tions in the wild among native, farmed and hybrid Atlantic
salmon. J Fish Biol 50:634–651
Feindel N, Benfey T, Trippel E (2010) Competitive spawning
success and fertility of triploid male Atlantic cod (Gadus
morhua). Aquacult Environ Interact 1:47–55
Ferguson A, Fleming I, Hindar K, Skaala Ø, McGinnity P,
Cross TF, Prodöhl P (2007) Farm escapes. In: Verspoor E,
Stradmeyer L, Nielsen JL (eds) The Atlantic salmon:
genetics, conservation and management. Blackwell Pub-
lishing Ltd, Oxford, p 357–398
Fiske P, Lund RA, Hansen LP (2006) Relationships between
the frequency of farmed Atlantic salmon, Salmo salar L., in
wild salmon populations and fish farming activity in Nor-
way, 1989–2004. ICES J Mar Sci 63:1182–1189
Fleming IA, Jonsson B, Gross MR, Lamberg A (1996) An
experimental study of the reproductive behaviour and
success of farmed and wild salmon (Salmo salar). J Appl
Ecol 33:893–905
Fleming IA, Hindar K, Mjølnerød IB, Jonsson B, Balstad T,
Lamberg A (2000) Lifetime success and interactions of
farm salmon invading a native population. Proc Biol Sci
267:1517–1523
Fredheim A (2005) Current forces on net structures. PhD the-
sis, Norwegian University of Science and Technology
(NTNU), Trondheim
Fredheim A, Langan R (2009) Advances in technology for off-
shore and open ocean aquaculture. In: Burnell G, Allen G
(eds) New technologies in aquaculture: improving pro-
duction efficiency, quality and environmental manage-
ment. Woodhead Publications, Cambridge, p 914–944
Furevik D, Rabben H, Mikkelsen KO, Fosseidengen JE (1990)
Migratory patterns of escaped farm-raised Atlantic
salmon. ICES CM 1990/F:55. ICES, Copenhagen
Garcia de Leaniz C, Fleming IA, Einum S, Verspoor E and oth-
ers (2007) A critical review of inherited adaptive variation
in Atlantic salmon. Biol Rev Camb Philos Soc 82: 173–211
Gillanders BM, Joyce TC (2005) Distinguishing aquaculture
and wild yellowtail kingfish via natural elemental signa-
tures in otoliths. Mar Freshw Res 56:693–704
Glover KA (2010) Forensic identification of fish farm
escapees: the Norwegian experience. Aquacult Environ
Interact 1:1–10
Hansen LP (2006) Migration and survival of farmed Atlantic
salmon (Salmo salar L.) released from two Norwegian fish
farms. ICES J Mar Sci 63:1211–1217
Hansen LA, Dale T, Uglem I, Aas K, Damsgård B, Bjørn PA
(2008) Escape related behaviour of Atlantic cod (Gadus
morhua L.) in a simulated farm situation. Aquac Res 40:
26–34
Heuch PA, Mo TA (2001) A model of salmon louse production
in Norway: effects of increasing salmon production and
public management measures. Dis Aquat Org 45:145–152
Hindar K, Diserud O (2007) Vulnerability analysis of wild
salmon populations towards escaped farm salmon. Nor
Inst Nat Res Rep 244:1–45 (In Norwegian with English
summary)
Hindar K, Fleming IA, McGinnity P, Diserud O (2006) The
genetic and ecological effects of salmon farming on wild
salmon: modelling from experimental results. ICES J Mar
Sci 63:1234–1247
81
➤
➤
➤
➤
➤
➤
➤
➤➤
➤➤
➤
➤
➤
➤
➤➤
➤
➤
Aquacult Environ Interact 1: 71–83, 2010
Hislop JRG, Webb JH (1992) Escaped farmed Atlantic salmon
(Salmo salar) feeding in Scottish coastal waters. Aquacult
Fish Manag 23:721–723
ICES (2008) Report of the ICES Advisory Committee, 2008.
Book 6, North Sea. ICES, Copenhagen
Jacobsen JA, Hansen LP (2001) Feeding habits of wild and
escaped farmed Atlantic salmon, Salmo salar L., in the
Northeast Atlantic. ICES J Mar Sci 58:916–933
Jensen Ø (2005) Ice loads — ice growth and suggestions for
measures. Report no. SFH80 A064062. SINTEF, Trond-
heim (in Norwegian)
Jensen Ø (2006) Assessment of technical requirements for
floating fish farms — based on escape incidents January
2006. Rep no SFH80 A066056. SINTEF, Trondheim (in
Norwegian)
Jensen Ø, Lien E (2005a) Risk — design loads and safety. Rep
no SFH80 A064059. SINTEF, Trondheim (in Norwegian)
Jensen Ø, Lien E (2005b) Environmental loads at sites. Rep no
SFH80 A064058. SINTEF, Trondheim (in Norwegian)
Jonsson B, Jonsson N (2004) Factors affecting marine produc-
tion of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci
61:2369–2383
Jonsson B, Jonsson N (2006) Cultured Atlantic salmon in
nature: a review of their ecology and interaction with wild
fish. ICES J Mar Sci 63:1162–1181
Jørstad KE, van der Meeren T, Paulsen OI, Thomsen T,
Thorsen A, Svåsand T (2008) ‘Escapes’ of eggs from
farmed cod spawning in net pens: recruitment to wild
stocks. Rev Fish Sci 16:285–295
Karlsen Ø, Norberg B, Kjesbu OS, Taranger GL (2006) Effects
of photoperiod and exercise on growth, liver size, and age
at puberty in farmed Atlantic cod (Gadus morhua L.).
ICES J Mar Sci 63:355–364
Kjønhaug AF (2009) Production figures for salmon and rain-
bow trout 2008. Kyst og Havbruk 2009:128–130 (in Nor-
wegian)
Knutsen H, Moland OE, Ciannelli L, Heiberg ES, Knutsen JA,
Simonsen JH, Skreslet S, Stenseth NC (2007) Egg distrib-
ution, bottom topography and small-scale cod population
structure in a coastal marine system. Mar Ecol Prog Ser
333:249–255
Krkoˇsek M, Ford JS, Morton A, Lele S, Myers RA, Lewis MA
(2007) Declining wild salmon populations in relation to
parasites from farm salmon. Science 318:1772–1775
Lader PF, Fredheim A (2006) Dynamic properties of a flexible
net sheet in waves and current — a numerical approach.
Aquac Eng 35:228–238
Lader PF, Olsen A, Jensen A, Sveen JK, Fredheim A, Ener-
haug B (2007) Experimental investigation of the inter-
action between waves and net structures — damping
mechanism. Aquac Eng 37:100–114
Lader P, Dempster T, Fredheim A, Jensen Ø (2008) Current
induced net deformations in full-scale sea-cages for
Atlantic salmon (Salmo salar). Aquac Eng 38:52–65
Lien E, Jensen Ø (2005) Interaction — total systems. Rep no
SFH80 A064060. SINTEF, Trondheim (in Norwegian)
Lura H, Sægrov H (1991) Documentation of successful spawn-
ing of escaped farmed female Atlantic salmon, Salmo
salar, in Norwegian rivers. Aquaculture 98:151–159
Lura H, Sægrov H (1993) Timing of spawning in cultured and
wild Atlantic salmon (Salmo salar) and brown trout (Salmo
trutta) in the River Vosso, Norway. Ecol Freshw Fish 2:
167–172
McGinnity P, Stone C, Taggart JB, Cooke D and others (1997)
Genetic impact of escaped farmed Atlantic salmon (Salmo
salar L.) on native populations: use of DNA profiling to
assess freshwater performance of wild, farmed, and
hybrid progeny in a natural river environment. ICES J Mar
Sci 54:998–1008
McGinnity P, Prodohl P, Ferguson K, Hynes R and others
(2003) Fitness reduction and potential extinction of wild
populations of Atlantic salmon, Salmo salar, as a result of
interactions with escaped farm salmon. Proc Biol Sci 270:
2443–2450
Meager JJ, Skjæraasen JE, Fernö A, Karlse Ø, Løkkeborg S,
Michalsen K, Utskot SO (2009) Vertical dynamics and
reproductive behaviour of farmed and wild Atlantic cod
Gadus morhua. Mar Ecol Prog Ser 389:233–243
Moe H (2008a) Inspection of net cages — assessment of condi-
tion and possible causes of damage. The Norwegian
Aquaculture Escapes Commission, Bergen. Available at:
www.rommingskommisjonen.no/uploads/sintefrappnot-
070109.pdf (accessed 6 Aug 2010) (in Norwegian)
Moe H (2008b) Inspection of net cages at Austevoll — assess-
ment of condition and possible causes of damage. The
Norwegian Aquaculture Escapes Commission, Bergen.
Available at: www.rommingskommisjonen.no/uploads/
sintefrappnot-200209.pdf (accessed 6 Aug 2010) (in Nor-
wegian)
Moe H (2009) Inspection of net cages for the Aquaculture
Escape Commission — assessment of condition and possi-
ble causes of damage. The Norwegian Aquaculture
Escapes Commission, Bergen. Available at: www.
rommingskommisjonen.no/uploads/sintefrappnot-240409.
pdf (accessed 6 Aug 2010) (in Norwegian)
Moe H, Gaarder R, Sunde LM, Borthen J, Olafsen K (2005)
Escape-free net cages for cod. Report no. SFH A 054041,
SINTEF, Trondheim
Moe H, Dempster T, Sunde LM, Winther U, Fredheim A
(2007a) Technological solutions and operational measures
to prevent escapes of Atlantic cod (Gadus morhua) from
sea-cages. Aquac Res 38:91–99
Moe H, Olsen A, Hopperstad OS, Jensen Ø, Fredheim A
(2007b) Tensile properties for netting materials used in
aquaculture net cages. Aquac Eng 37:252–265
Moe H, Gaarder RH, Olsen A, Hopperstad OS (2009a) Resis-
tance of aquaculture net cage materials to biting by
Atlantic Cod (Gadus morhua
). Aquac Eng 40:126–134
Moe H, Hopperstad OS, Olsen A, Jensen Ø, Fredheim A
(2009b) Temporary-creep and post-creep properties of
aquaculture netting materials. Ocean Eng 36:992–1002
Naylor R, Hindar K, Fleming IA, Goldburg R and others (2005)
Fugitive salmon: assessing the risks of escaped fish from
net-pen aquaculture. Bioscience 55:427–437
Norwegian Directorate of Fisheries (2009) Statistics for Aqua-
culture 2008. Norwegian Directorate of Fisheries, Bergen.
Available at: www.fiskeridir.no/fiskeridir/kystsone_og_
havbruk/statistikk (accessed 6 Aug 2010) (in Norwegian)
Norwegian Ministry of Fisheries and Coastal Affairs (2008).
Aquaculture operations regulations with remarks. Norwe-
gian Ministry of Fisheries and Coastal Affairs, Bergen.
Available at: http://www.lovdata.no/cgi-wift/ldles?doc=/
sf/sf/sf-20080617-0822.html (in Norwegian)
Øines Ø, Simonsen JH, Knutsen JA, Heuch PA (2006) Host
preference of adult Caligus elongatus Nordmann in the
laboratory and its implications for Atlantic cod aquacul-
ture. J Fish Dis 29:167–174
Oppedal F, Dempster T, Stien L (in press) Environmental dri-
vers of Atlantic salmon behaviour in sea-cages: a review.
Aquaculture
Scientific Advisory Committee (2009) The status of Norwe-
gian salmon stocks in 2009 and catch advice. Report from
the Scientific Advisory Committee for Atlantic Salmon
Management in Norway No. 1. Vitenskapelig råd for
82
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤➤
➤
➤
➤
➤
➤
➤
➤➤
➤
➤
➤
➤
➤
➤
Jensen et al.: Escapes of fish from sea-cage aquaculture
lakseforvaltning, Trondheim (In Norwegian with English
summary)
Skaala Ø, Wennevik V, Glover KA (2006) Evidence of tempo-
ral genetic change in wild Atlantic salmon, Salmo salar L.,
populations affected by farm escapees. ICES J Mar Sci 63:
1224–1233
Skilbrei O, Holst JC, Asplin L, Mortensen S (in press) Hori-
zontal movements of simulated escaped farmed Atlantic
salmon (Salmo salar) in a western Norwegian fjord. ICES
J Mar Sci doi:10.1093/icesjms/fsq027
Skilbrei O, Wennevik V (2006) Survival and growth of sea-
ranched Atlantic salmon, Salmo salar L., treated against
sea lice before release. ICES J Mar Sci 63:1317–1325
Skjæraasen JE, Mayer I, Meager JJ, Rudolfsen G, Karlsen Ø,
Haugland T, Kleven O (2009) Sperm characteristics and
competitive ability in farmed and wild cod. Mar Ecol Prog
Ser 375:219–228
Soto D, Jara F, Moreno C (2001) Escaped salmon in the inner
seas, southern Chile: facing ecological and social conflicts.
Ecol Appl 11:1750–1762
Standard Norge (2009) Norwegian standard NS 9415.E:2009
Marine fish farms — requirements for site survey, risk
analyses, design, dimensioning, production, installation
and operation. Standard Norge, Lysaker
Svåsand T, Crosetti D, García-Vázquez E, Verspoor E (eds)
(2007) Genimpact — evaluation of genetic impact of aqua-
culture activities on native populations. Final scientific
report, EU contract no. RICA-CT-2005-022802. Available
at: http://genimpact.imr.no/__data/page/7649/genetic_
impact_of_aquaculture.pdf (accessed 6 Aug 2010)
Taranger GL, Aardal L, Hansen T, Kjesbu OS (2006) Continu-
ous light delays sexual maturation and increases growth of
Atlantic cod (Gadus morhua L.) in sea cages. ICES J Mar
Sci 63:365–375
Thorstad EB, Fleming IA, McGinnity P, Soto D, Wennevik V,
Whoriskey F (2008) Incidence and impacts of escaped
farmed Atlantic salmon Salmo salar in nature. Nor Inst Nat
Res Spec Rep 36:1–110
Toledo Guedes K, Sanchez-Jerez P, Gonzalez-Lorenzo G,
Brito Hernandez A (2009) Detecting the degree of estab-
lishment of a non-indigenous species in coastal eco-
systems: sea bass Dicentrarchus labrax escapes from sea
cages in Canary Islands (Northeastern Central Atlantic).
Hydrobiologia 623:203–212
Torrissen OJ (2007) Status report for Norwegian aquaculture
2007. Kyst og Havbruk 2007: 11-12 (in Norwegian)
Triantafyllidis A (2007) Aquaculture escapes: new DNA
based monitoring analysis and application on sea bass and
sea bream. CIESM Workshop Monogr 32:67–71
Uglem I, Bjørn PA, Dale T, Kerwath S and others (2008)
Movements and spatiotemporal distribution of escaped
farmed and local wild Atlantic cod (Gadus morhua L.).
Aquac Res 39:158–170
Uglem I, Bjørn PA, Mitamura H, Nilsen R (2010) Spatiotempo-
ral distribution of coastal and oceanic Atlantic cod (Gadus
morhua L.) sub-groups after escape from a farm. Aquacult
Environ Interact 1:11–20
Valland A (2005) The causes and scale of escapes from
salmon farming. In: Hansen LP, Windsor M (eds) Inter-
actions between aquaculture and wild stocks of Atlantic
salmon and other diadromous fish species: science and
management, challenges and solutions. NINA Special
Report 34. Norwegian Institute for Nature Research
(NINA), Trondheim, p 29
van der Meeren T, Jørstad K (2009) Fanger torsk på vidvanke.
Nytt fra havbruk 2009(2):1
Weir LK, Grant JWA (2005) Effects of aquaculture on wild fish
populations: a synthesis of data. Environ Res 13: 145–168
Whoriskey FG, Brooking P, Doucette G, Tinker S, Carr JW
(2006) Movements and survival of sonically tagged farmed
Atlantic salmon released in Cobscook Bay, Maine, USA.
ICES J Mar Sci 63:1218–1223
Wright PJ, Galley E, Gibb IM, Neat FC (2006) Fidelity of adult
cod to spawning grounds in Scottish waters. Fish Res 77:
148–158
WWF (2005) On the run — escaped farmed salmon in Norwe-
gian waters. WWF-Norway Rep 2/2005. WWF-Norway,
Oslo. Available at: http://wwf.no/dette_jobber_med/hav_
og_kyst/akvakultur/romt_fisk_og_introduserte_arter/
(accessed 6 Aug 2010)
83
Editorial responsibility: Pablo Sánchez-Jerez,
Alicante, Spain
Submitted: April 30, 2010; Accepted: July 23, 2010
Proofs received from author(s): August 9, 2010
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